Medical Parasitology
in the Philippines
 

 
 

Medical Parasitology
in the Philippines

Vicente Y. Belizario, Jr.

Winifreda U. de Leon
EDITORS  

The University of the Philippines Press

Diliman, Quezon City
 

THE UNIVERSITY OF THE PHILIPPINES PRESS

E. de los Santos St., UP Campus, Diliman, Quezon City 1101
Tel. Nos.: 925-3243, 926-6642 / Telefax No.: 928-2558
E-mail: [email protected]
E-mail:  [email protected]
h
Website: uppress.com.ph

© 2013 by University of the Philippines Manila ???? (Vicente Y. Belizario, Jr., Winifreda U. de Leon ???????)
All rights reserved.
 No copies can be made in part
part or in whole without prior written
written permission from the author
author and the publishe
publisher.
r.

The data in this book have been verified

verified with
 with reliable sources, and treatment modalities suggested have been
utilized in clinical practice. However, new researches and changes in the medical sciences should be considered.
Readers are advised to consult other sources such as drug i nformation sheets and dosage, contraindications to
administration, and other relevant data.

The National Library of the Philippines CIP Data

Recommended entry:

ISBN 978-971-542-

Book Design by Zenaida N. Ebalan

Printed in the Philippines

 

Toourf ell ow
  F pliinos, f romwhomwederiveinspirat ionand learnnig, espec y
ail t hosewhoarepoorandneg lecet d,
 suferingfromtheburdenofparasitcdiseases
 

vi   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

Table of Contents 

FOREWORD ............................
...........................................
.............................
............................
............................
.............................
.............................
............................
............................ x. 
.............................
................

FOREWORD TO THE SECOND EDITION  ...................................................................................................... x 

FOREWORD TO THE FIRST EDITION ........................
....................................
.......................
.......................
........................
........................
........................
....................... x 
...................
........

PREFACE ...........................
.........................................
............................
.............................
.............................
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............................
.............................
............................. x 
....................
......

ACKNOWLEDGMENTS ...........................
.........................................
.............................
.............................
............................
.............................
.............................
............................
............................x 
.................
...

LIST OF FIGURES ........................
....................................
........................
........................
.......................
.......................
........................
........................
........................
....................... x 
.....................
..........

LIST OF PLATES  ............................................................................................................................................. x 

LIST OF TABLES  ............................................................................................................................................. x 

CHAPTER  1:
 1: I NTRODUCTION TO MEDICAL PARASITOLOGY................................................................................. x 
General Considerations ................................................................................................. x
Host-Parasite Relationships
Relationships......................................
.................. .......................................
......................................
..................................
............... x
Immunology
Immunology of Parasitic Infections...................
......................................
......................................
.......................................
......................
.. x
Groups of Parasites
P arasites with Medical and Public Health Importance....................
....................................
................ x
CHAPTER 2: PROTOZOAN I NFECTIONS ....................................................................................................................................................... x 
Intestinal Amebae ..........................................................................................................x
Commensal Amebae .................................................................................................... x
Free-living Pathogenic
Pathogenic Amebae...................
......................................
......................................
......................................
............................
......... x
Ciliates and Flagellates...................
......................................
......................................
......................................
.......................................
......................
.. x
Coccidians .................................................................................................................... x
Other Intestinal Protozoans ........................................................................................... x
 Plasmodiumspp..........................................................................................................................................................................................................................................................x
Babesia spp ...........
.......................
........................
........................
........................
.......................
.......................
........................
........................
........................
.......................
....................
......... x 
Blood and Tissue Flag
Flagellates
ellates ................................
....................................................
.......................................
.....................................
.................. x
 3: NEMATODE I NFECTIONS  ................................................................................................................. x 
CHAPTER  3:

Intestinal Nematodes ..................................................................................................... x

Tissue Nematodes..........................................................................................................x
vii 

CHAPTER  4:
 4: CESTODE I NFECTIONS  ................................................................................................................... x 

Intestinal Cestodes ....................................................................................................... x

 

vi  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Extraintestinal Cestodes ................................................................................................ x
CHAPTER  5:
 5: TREMATODE I NFECTIONS  ............................................................................................................... x 

Blood Flukes ................................................................................................................ x

Lung Flukes .................................................................................................................. x

Intestinal Flukes ........................................................................................................... x
Liver Flukes ................................................................................................................. x
CHAPTER  6:
 6: ARTHROPODS AND MOLLUSKS OF MEDICAL IMPORTANCE ...........
.......................
........................
.......................
...........................x 
................

Introduction to Arthropods of Medical Importance

Importance .................
.....................................
.......................................
................... x
Arthropods as Direct Causes of Injury .......................................................................... x
Arthropods as Vector
Vectorss of Disease ............................................
......................... .......................................
......................................
.................. x
Introduction to Medical
Medical Malaco
Malacology
logy ........................
..........................................
......................................
...................................
............... x
 7: DIAGNOSTIC P ARASITOLOGY  ....................................................................................................... X. 
CHAPTER  7:

Examination of Stools
Stools and B
Body
ody Fluids ...................
.....................................
......................................
...................................
............... x
Examination of Tissues ................................................................................................. x
Recent Advances in Diagnosis of Parasitic IInfections
nfections ................
....................................
....................................
................ x
Quality Assurance in a Parasitology Laboratory...................
......................................
.......................................
......................
.. x
CHAPTER  8:
 8: SPECIAL TOPICS IN PARASITOLOGY ............
.......................
.......................
........................
........................
........................
....................... x 
.......................
............

Parasitic Zoonoses ........................................................................................................ x

Immunocompromise
Immunocompromised
d Hosts and P
Parasitic
arasitic Infections .................
.....................................
....................................
................ x
 Neglected Tropical Diseases ...................
......................................
......................................
......................................
....................................
................. x
Preventive Chemotherapy.............................................................................................. x
Emporiatrics
Emporiatri cs for the Filipino Trave
Traveler
ler ...........
......................
.......................
........................
........................
.......................
.......................
................
.... x
APPENDICES ................................................................................................................................................................................................................................... x 

WHO Bench Aids for the Diagnosis of IIntestinal

ntestinal Parasites ..................
.....................................
..........................
....... x
WHO Bench Aids for the Diagnosis of Filarial Infections
Infections .............................
......... ....................................
................ x
WHO Bench Aids for the Diagnosis of Mala
Malaria
ria Infections...................
......................................
..........................
....... x
Treatment of
of Parasitic Infections ...................
......................................
......................................
......................................
..............................
........... x
List of More Recent National Policies and Guidelin
Guidelines
es on Parasitic Diseases...................
....................x
.x
I NDEX...............
.............................
............................
............................
.............................
.............................
............................
............................
.............................
.............................
................................. x 
...................
 

ix  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Figure 2.1 Life cycle of Ena

t moebahis y
tol it ca.................................................................................................................................................................................................................................x
Figure 2.2 Life cycle of commensa
commensall amebae...................
......................................
......................................
............................
......... x
Figure 2.3 Life cycle of Acanh
t amoebaspp ................................................................................ x
Figure 2.4 Life cycle of Naegleriafowleri.........................................................................................................................................................................................................................x
Figure 2.5 Life cycle of Balantidiumcoli...........................................................................................................................................................................................................................x
Figure 2.6 Life cycle of Giardiaduodenalis
Figure 2.7 Life cycle of Trichomonasvaginalis
Figure 2.8 Life cycle of Cryptosporidiumspp.
Figure 2.9 Life cycle of Cyclosporacayetanensis
Figure 2.10 Life cycle of Cystoisosporabeli
Figure 2.11 Life cycle of Toxoplasmagondi
Figure 2.12 Life cycle of Sarcocystisspp.
Figure 2.13 Life cycle of  Dientamoebafragils
Figure 2.14 Life cycle of Plasmodiumspp.
Figure 2.15 Diagram of the course of malaria infections showing the primary attack, relapses,
and recrudescence
Figure 2.16 A WHO field
field test
 test for response of malaria parasites to chloroquine
Figure 2.17 Global distribution of malaria
Figure 2.18 Distribution of malaria in the WHO Southeast Asia Region
Figure 2.19 Distrib
Distribution
ution of malaria in the WHO Western Pacific
Pacific Region
 Region
Figure 2.20 Malaria cases per 100,000 population in the Philippin
Philippines
es from 2000 to 2009
Figure 2.21 Malaria-related deaths per 100,000 populatio
population
n in the Philippines from 2005 to
2009
Figure 2.22 Macrostratificationof  provinces in the Philippines
Philip pines according to category by average
malaria cases
Figure 2.23 Life cycle of  B
 Ba
abesiaspp.
Figure 2.24 Life cycle of Trypanosomacruzi
Figure 2.25 Life cycle of Trypanosomabrucei
 

ix 
 

List of
o f Figures 
Figure 2.26 Life cycle of  Leishmaniaspp.
Figure 3.1 Life cycle of Ascarislumbricoides
Figure 3.2 Global distributionof soil-transmittedhelminth (STH) infections and proportion
of children requiring preventive chemotherapy for STH infections in each country
Figure 3.3 Schematic life cycle of soil-transmitted helminths
Figure 3.4 Comparison of cumulative prevalence in San Vicente Elementary School (SVES)
and sentinel schools in Biñan, Laguna from 1999 to 2010
Figure 3.5 Life cycle of Trichuristrichiura
Figure 3.6 Life cycle of hookworms
Figure 3.7 Life cycle of Strongyloidesstercoralis
Figure 3.8 Life cycle of  Enterobiusvermicularis
Figure 3.9 Life cycle of Capilariap p
hilpinensis
Figure 3.10 Life cycle of Wuchereriabancrofti
Figure 3.11 Distribution and status of preventive chemotherapy for lymphatic filariasis,
worldwide, 2010
Figure 3.12 Map of lymphatic filariasis-endemic
filariasis -endemic provinces
provinces in the Philippines, distribution in the
three major island groups, and provinces declared lymphatic filarisis
filarisis-free
-free by the
Department of Health

Figure 3.13 Life cycle of  Parasrt ongyu

l scantonensis
Figure 3.14 Life cycle of Trichinelaspiralis
Figure 3.15 Life cycle of An
 Anisakisspp.
Figure 3.16 Life cycle of Toxocaracanis
Figure 4.1 Life cycle of Taeniaspp. 
Figure 4.2 Life cycle of Taeniasolium(cysticercosis)
Figure 4.3 Life cycle of Hymenolepisnana
Figure 4.4 Life cycle of  Hymenolepisdiminuta
Figure 4.5 Life cycle of  Dipylidiumcaninum
Figure 4.6 Life cycle of  Diphylobothriumlau
t m
Figure 4.7 Life cycle of Echinococcusspp.
Figure 4.8 Life cycle of Spirometraspp.
Figure 5.1 Life cycle of Schistosomaspp.
Figure 5.2 Map of Schistosomajaponicum-endemicprovinces in the Philippines
Figure 5.3 Life cycle of Paragonimuswestermani
Figure 5.4 Life cycle of  FasciolopsisbuskiFigure
Figure
5.5 Life cycle of  Echinostomaspp.
Figure 5.6 Life cycle of heterophyids
 

List of Figures xi 

Figure 5.7 Life cycle of  F

 Fa
asciolaspp.
Figure 5.8 Life cycle of Clonorchissinensis
Figure 5.9 Life cycle of Opisthorchisspp.
Figure 6.1 A generalized diagram of an adult Cyclorraphan fly
Figure 6.2 Parts of an insect head

Figure 6.3 Chewing type of mouthparts

Figure 6.4 Sponging type of mouthparts
Figure 6.5 Piercing-
Piercing-sucking
sucking type of mouthparts
Figure 6.6 Chewing-lappi
Chewing-lapping
ng type of mouthparts
Figure 6.7 Walking leg of an insect
Figure 6.8 Spiracle
Figure 6.9 Cercus
Figure 6.10 Diagram of an insect showing the arrangement of the circulato
circulatory
ry system
Figure 6.11 Diagram showing an insect spiracle and trachea
Figure 6.12 Diagram of an insect showing the arrangement of the nerve cord
Figure 6.13 The digestive and excretory systems
Figure 6.14 Reproductive systems of an insect
Figure 7.1 SYBR Green detection in real-time PCR
Figure 7.2 TaqMa
TaqMan
n real-ti
real-time
me PCR
Figure 7.3 Mode of action of antigen-de
antigen-detecting
tecting malaria rapid diagnostic tests (RDTs)
Figure 7.4 The importance of ensuring quality of laboratory diagnosis of parasitic infections
Figure 8.1 Direct zoonoses
Figure 8.2 Cyclozoonoses subtype 1: man as an obligatory (definitive)
(definitive) host
 host
Figure 8.3 Cyclozoonoses subtype 2: man as a non-obligato
non-obligatory
ry (optional) host
Figure 8.4 Metazoonoses subtype 1: one vertebrate host (definitive)
(definitive) and
 and one invertebrat
invertebratee host
(intermediate)
Figure 8.5 Metazoonoses subtype 2: more than one invertebrate host (first and second
intermediate host) and one vertebrate host

Figure 8.6 Moestas z(oonneodsefis snu b

h ititvye paen3d: oonee iinnvter tm
e ber 
daitaeteh)ost (intermedia
iatte) and two inver te br ate 

Figure 8.7 Zaprozoonoses

Figure 8.8 Life cycle of microsporidia

Figure 8.9 Distribution of malaria

Figure 8.10 Global distributi
distribution
on of neglected tropical diseases (NTDs) by number of NTDs
 per country
 

xii  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Figure 8.11 School teachers administeringdeworming tablets to students in a public elementary

school in Biñan, Laguna
Figure 8.12 Cumulative STH prevalence and heavy intensity infections in school-age children
in Aklan, Antique, and Capiz, 2007-2009
Figure 8.13 Process, performan
performance,
ce, and impact indicators for helminth control
Figure 8.14 Checking for tongue discoloration after administration of deworm
deworming
ing tablets to
school children to ensure compliance
Figure 8.15 Former DOH Secretar
Secretary
y Francisco Duque III and former Antique Governor
Salvacion Per ez administer ing anthelminthics to school childr en in Pandan Centr al
Elementary School, Antique during the launch of the War on Worms — Western Western
Visayas
Figure 8.16 Parade of schoolchildrenand teachersduring the launch of War on Worms — Biñan,
Biñan,
Laguna
 

List of Plates 

Plate 2.1  Entamoebahistolyticacyst

Plate 2.2  En
 Entamoebahistolyticatrophozoite
Plate 2.3  En
 Entamoebahistolyticaquadrinuc
nucleatecy
tec yst
Plate 2.4 Charcot-Le
Charcot-Leyden
yden crystal observed in stool specimen of a patient suffering from
amebiasis
Plate 2.5 Agarose gel showing the 100bp PCR products of  Entamoebahistolytica-positive
stool specimens (lanes 2 – 1
15)
5)
Plate 2.6 Ultrasound showing a solitar
solitaryy hypoechoic mass at the right lobe of the liver
suggesting ALA
Plate 2.7  En
 Entamoebacolitrophozoite
Plate 2.8  Iodamoebabütschlicyst
 
Plate 2.9  Ac
 Acanthamoebatrophozoite exhibiting characteristic acanthopodia
Plate 2.10  Na
 Naegleriafowleritrophozoites in ameboid and ameboflagellate
ameboflagellate forms
 forms

Plate 2.11 Giardiaduodenalistrophozoite

Plate 2.12 Giardiaduodenaliscysts
Plate 2.13 Imma ture oocy st of Cystoisosporabeli recovered from stool sample,
showing a single sporoblast
Plate 2.14 Toxoplasmatachyzoites
Plate 2.15 Binucleate forms of trophozoit es of  Dientamoebafragilisstainedwith trichrome
trophozoites
Plate 2.16  Plasmodiumfalciparumringforms
Plate 2.17  I
 Ixxodessp.
Plate 2.18 Trypanosomacruzitrypomastigotein thin
th in bloo
bl ood
d smea
s mears
rs stai
st aine
nedd w
wit
ith
h Gi
Giem
emsa
sa
Plate 3.1  As
 Ascarisunf
unferti
ertili
lize
zed egg, fferti
ertilize
lized
d eg
egg,
g, and embryon
embryonated
ated egg
Plate 3.2  Ascarisinthe liver
Plate 3.3 Intestinal obstruction with Ascaris
Plate 3.4  Ascarisinthe brain
Plate 3.5 Trichurismaleand
an d fema
fe male
le
Plate 3.6 Trichurisegg
 

xiii 
 

xiv  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Plate 3.7 Rectalprolapse in a 9-yearold female seen at the Philippine GeneralHospital with
heavy Trichurisinfection
Plate 3.8 Buccal capsules of hookworms
Plate 3.9 Hookworm filariform larvae 
larvae 
Plate 3.10 Hookworm egg
Plate 3.11 Cutaneous larva migrans
Plate 3.12 Strongyloidesstercoralis rhabditiform larva
Plate 3.13  Enterobiuscephalic alae
Plate 3.14 D-shaped eggs of Enterobiusvermicularis
Plate 3.15 Male Capillariaphilippinensis
Plate 3.16 Female Capillariaphilippinensis
Plate 3.17 Capillariaphilippinensis egg
egg  
Plate 3.18 Capilariaphilippinensisecondstage larv
larvaa fr
from
om tthe
he ffeces
eces of a pers
person
on wi
with
th intesti
int estinal
nal
capillariasis
Plate 3.19 31-year old female with intestinal capillariasis
capilla riasis before treatment and 1 year after
treatment
Plate 3.20 Proper excreta disposal is important for prevention and control of intestinal
helminthiasess including capillariasis
helminthiase
Plate 3.21  Brugiamalayimicrofilaria
microfilaria  
Plate 3.22 Wuchereriabancrofti microfilaria
microfilaria  
Plate 3.23 Dermatolymphangi
Dermatolymphangioadenitis
oadenitis (acute lymphatic filariasis) 
filariasis)  
Plate 3.24 Elephantiasis
Plate 3.25 Hydrocele
Plate 3.26 Small and big hydroceles in 2 patients suffering from filariasis 
filariasis  
Plate 3.27 Farmer in abaca plantation
Plate 3.28 An axil of abaca: a breeding site of  Aedespoecilus
Plate 3.29  Parastrongylus adults
adults  
Plate 3.30  Achatinafulica, the intermediate host of  Parastrongyluscantonensis
Plate 3.31 Trichinellaspiralislarvae in muscle
Plate 4.1 Taeniasaginatascolex
Plate 4.2 Taeniasaginatagravid segment
Plate 4.3 Taeniaegg
Plate 4.4 Taeniasoliumscolex
Plate 4.5 Cysticercus cellulosae from pork
Plate 4.6  Hymenolepisspp. scolex
Plate 4.7  Hymenolepisspp. gravid segment
 

List of Plates  xv 

Plate 4.8  Hymenolepisnana egg

egg  
Plate 4.9  Hymenolepisdiminuta egg
Plate 4.10  Dipylidiumcaninum gravid segment
Plate 4.11  Dipylidiumcaninum egg capsule
Plate 4.12  Raillietinagarrisoni adult

Plate 4.13 Flour beetle (Triboliumspp.), the intermediate host of  Raillietinagarrisoni

ate . ip y o ot rium atumsco sco ex
Plate 4.15  Diphyllobothriumlatum egg
Plate 4.16 Hydatid sand
Plate 5.1 Schistosomajaponicum male and female
Plate 5.2 Schistosomajaponicum egg
egg  
Plate 5.3 Schistosomajaponicum adults in copula
Plate 5.4 A boy from Leyte with portal hypertensio
hypertensionn and ascites secondary to schistosomiasi
schistosomiasiss
Plate 5.5 Schistosomaegg in the brain
Plate 5.6 Oncomelaniah.quadrasi, intermediate host of Schistosomajaponicum
Plate 5.7  Paragonimuswestermani adult
Plate 5.8  Paragonimuswestermaniegg;note
note the flattened operculum and the abopercular  
 portion
Plate 5.9  Antemelaniaasperata, first intermediate host of  Paragonimuswestermani
intermediate
Plate 5.10 und 
S  a p
hel hu sap p
t  hill p in,athe second intermediat
iate host o P aonmi u sw set r 
f ar  g  mani 
Plate 5.11  Paragonimuswestermani metacercaria in crab heart muscle
Plate 5.12 Trapabicornis, second intermediate host of  Fasciolopsisbuski
Plate 5.13  Pilaluzonica,second intermediate host of Echinostomailocanum
Plate 5.14  Echinostomailocanum adult
Plate 5.15  Artyfechinostomummalayanum adult
Plate 5.16 Heterophyid fluke adult 
adult 
Plate 5.17 Heterophyid egg
Plate 5.18  Fasciola egg 
egg  

Plate 5.19 Opistorchisviverrini adult

Plate 6.1 Bee ( Bombus
 Bombussp.)
Plate 6.2 Wasp
Plate 6.3 Bee stinger

Plate 6.4 Kissing bug (Triatomasp.)

Plate 6.5 Caterpillar, dorsal view
Plate 6.6 Caterpillar head and thorax, lateral view
 

xvi  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Plate 6.7 Centipede

Plate 6.8 Centipede head
Plate 6.9 Scorpion
Plate 6.10 Black widow spider ( Latrodectushasselti)
Plate 6.11 Blackfly (Simuliumsp.)

Plate 6.12 Midge (Culicoidesspp.)

ate . an y e ot
oto
omussp
sppp.
Plate 6.14 Horsefly (Tabanus spp.)
Plate 6.15 Louse ( Pediculushumanuscapitis
 Pediculushumanuscapitis)
Plate 6.16 Pubic louse ( Phthiruspubis
 Phthiruspubis)
Plate 6.17 Bedbug (Cimexsp.)
Plate 6.18 Butterfly scales 
scales 
Plate 6.19 Dust mite ( Blomiatropicalis
 Blomiatropicalis )
Plate 6.20 Dust mite (Glycyphagussp.)
Plate 6.21 Dust mite ( Dermatophagoidespteronyssinus
 Dermatophagoidespteronyssinus )
Plate 6.22 Dust mite (Cheyletusmalaccensis)
Plate 6.23 Maggots
Plate 6.24 Mosquito ( Aedesaegypti
 Aedesaegypti)
Plate 6.25 American cockroach ( Periplanetaamericana
 Periplanetaamericana )
Plate 6.26 German cockroach ( Blatellagermanica
 Blatellagermanica)
Plate 6.27 Oriental cockroach ( Blattaorientalis
cockroach  Blattaorientalis)
Plate 7.1 Cysticercu
Cysticercuss in brain
Plate 7.2 Ovary with incidental finding of Schistosomajaponicumova
Plate 7.3 Fallopian tube with incidental finding of Schistosomajaponicumova
Plate 7.4 Colon with adenocarcinoma and Schistosomaova
Plate 7.5 Adult filaria with microfilaria in an inguinal lymph node 
node 
Plate 7.6 Adult Trichurisidentified by ova in genital tract 
tract  
Plate 7.7 Cysticercus with calcareous corpuscles
Plate 7.8 A fungal spore in a wet mount stool may look like a cyst of  Entamoebaspp.
Plate 7.9 A mite egg in a formalin-con
formalin-concentrated
centrated stool specimen may look like a hookworm
egg
Plate 7.10 A plant cell in a concentrated wet mount of stool may look like a helminth egg

Plate 7.11 A pollen grain in a oides 

of Ascarislumbric concentrated
 Ascarislumbricoides   wet mount of stool may look like a fertiliz
fertilized
ed egg

Plate 7.12 Plant hair in a concentrated wet mount of stool may look like a hookworm or
Strongyloidesstercoralis larva
larva  
 

List of Plates  xvii 

Plate 7.13 Howell-Joll

Howell-Jollyy bodies in a thin blood smear stained with Giemsa may look like
malaria parasites
Plate 7.14 A nucleated red blood cell may look like a schizont of  Plasmodiumspp.
Plate 7.15 Fungal spores o H
f  elicosproriummay be
 be mistaken
mistaken as microfilariae in stained bloo
blood
d
smears
Plate 8.1  Balantidiumcolifrom pig
Plate 8.2 Sarcocyst in sectioned esophageal muscle of water buffalo
Plate 8.3 Cysticercu
Cysticercuss cellulosae freed from muscle of pig
Plate 8.4 Strobilocercusfasciolaris freed from liver of field rat 
rat 
Plate 8.5  Anisakislarva from fish 
fish 
Plate 8.6  Fasciolagiganticaand F.hepaticafrom water buffalo
Plate 8.7  Fasciolametacercariae
Plate 8.8 Schistosomacercariae
Plate 8.9  Dipylidiumcaninum from dog
Plate 8.10  Dirofilariaimmitisfrom dog
Plate 8.11  Macracanthorhynchushirudinaceus from pig
Plate 8.12  Echinostomalindoense from field rat 
rat 

Plate 8.13  Eurytremapancreaticum from cattle

Plate 8.14  Philophthalmusgrallifrom duck

Plate 8.15  Plagiorchisphilippinensis from rat

Plate 8.16 Sparganum of Spirometrafrom muscle of frog
Plate 8.17 Gnathostomadoloresi from pig
Plate 8.18 Gnathostoma larva from frog muscle
Plate 8.19 Toxacaracanis from dog
Plate 8.20 Toxocaracanis embryonated egg (infective)
Plate 8.21  Mammomonogamuslaryngeus in copula from water buffalo
 

xvii MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 
 

List of
o f Tables 

Table 1.1 Classification of protozoan parasites

parasites  
Table 1.2 Classification of  metazoan
  metazoan parasites
Table 2.1 Comparison of bacillary and amebic dysentery
Table 2.2 Selected Philippine data on giardiasis
Table 2.3 Selected Philippine studies on trichomon
trichomoniasis
iasis
Table 2.4 Millennium
Millenniu m development goals: eight goals for 2015
Table 2.5 Comparison of morphological features of malaria parasites
Table 2.6 Clinical features and laboratory findings in severe malaria infection  
Table 2.7 Comparison of sign and symptoms of sever malaria in adults and children
Table 2.8 Macrostratification of
Macrostratification of malaria endemic provinces according to annual incidence
inci dence
Table 2.9 Treatment of malaria infectio
infectionn
Table 2.10 Summary of human cases of babesiosis reported in some Asian countries
Table 3.1 Core indicatorsof mass drug administrationfor soil-transmittedhelminthinfections 
soil-transmittedhelminthinfections  
Table 3.2 The WASHED framewor
framework
k for a comprehe
comprehensive
nsive control of soil-tran smitted
helminth infections
Table 3.3 Comparison of microfilaria of Wuchereriabancroftiand  Brugiamalayi
Table 3.4 Algorithm for the diagnosis of the probabilit
probabilityy of acute trichinel
trichinellosis
losis in humans
Table 4.1 WHO classification for hepatic echinococcal cysts 
cysts  
Table 5.1 Prevalence of schistosomiasis stratified by province (2005-2007)
(2005 -2007)
Table 6.1 List of immediate diagnostic features of arthropods
Table 6.2 Specific injuries
injuries and their causative agents
Table 6.3 Principal differenc
differences
es between mites and ticks

Table 6.4 Arthropods as pests of stored products, food and water sources
Table 6.5 Identifying
Identifying characteristics of some myiasis-produc
myiasis-producing
ing larva
Table 6.6 List of arthropod-
arthropod-associated
associated diseases and their corresponding agents and vectors
Table 7.1 WHOclassification
WHO classification  of intensity of infections with soil-transmitted helminths and
Schistosoma spp.
spp.  
Table 7.2 Organs and parasites isolated

xix 
 

xx  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Table 7.3 Special stains and correspon

corresponding
ding parasites
Table 7.4 Antibody detection tests offered at CDC
Table 7.5 Commercially available parasite antigen detection tests
Table 7.6 Recommended stool examination techniques for specific situations 
situations  
Table 8.1 Philippine fishes found harboring anisakine larvae (from
( from various authors) 
authors)  

Table 8.2 Philippine fishes found harboring metacercariae of heterophyid species  

Table 8.3 Protozoansand helminthic organismsof specialimportanceto immunocompromised  
 patients
Table 8.4 Microsporidial infections in immunoco
immunocompromise
mpromised
d patients
Table 8.5 Neglected tropical diseases targeted by the WHO
Table 8.6 Target
Target population, drug recommended, and mass drug administrat
administration
ion frequency
of health programs in the Philippines
Table 8.7 Categories, usage, and frequency of collection of indicator
indicatorss
Table 8.8 Vaccines for travelers
Table 8.9 Vaccines for selective use by travelers
Table 8.10 Recommended drugs used in the prophylaxis for malaria
Table 8.11 Specific infectious diseases involving potential health risks for travelers 
travelers  
 

Foreword 

o other book published by the University the book all the more relevant to policy makers,
of the Philippines Manila (UPM) has been  practitioners, students,
students, and he
health
alth workers
workers
as widely patronized both by UPM constituents involved in eradicating parasitism in highly
and other health students and professionals affected communities.
throughout the country than the Philippine To this day, parasitic infections are still
Textbook on Medical Parasitology, now entitled considered a major public health problem in
Medical Parasitology in the Philippines.
P hilippines. the Philippines and the rest of the Asian region.
That the response to the first two editions For a developing and tropical country like the
of the book has been overwhelming affirms Philippines,
Philipp ines, the prevalence of parasitic diseases
the value and significance of the material in is worsened by high population density, hot
complementing meager publications on medical and humid climate and other environmental
 parasites with special focus on the local setting. factors, poverty, and socioeconomic conditions
Dr. Vicente Y. Belizario, Jr. and the that provide a conducive setting to the parasites.

cdoen oef  ntdhaet b
r s m
setr r vi  bbe uctom f or f or r e b
ioonok  s pootnhdeindgititoonsthe ggloetswoif thf sigtahntdining  p
stru N haesitdiisf m
g atr  f iicc, ualltliessecatnor ds
need for a locally compiled comprehensive should come together and join efforts to
material on parasitology through their combat the disease because of its grave effects
 painstaking work on this b book.
ook. on the health, productivity
productivity,, and well-being of
It is good to know that the book that first the people.
came out in 1998 has been updated again I am confident that his latest edition of
through this third edition. The additional the book will serve as an accurate and valuable
data and information, fresh insights, and reference material in the continuing war against
new experiences shared by the authors at the  parasites.
global, regional, and national settings, make Thank you again for this gem of a textbook.
MANUEL B. AGULTO
Chance lol r 
 
University of the Philippines Manila

xxi 
 

xxii  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

Foreword to the Second Edition 

Edition 

he preparation of this Philippine health in the Philippines. It must be a valuable

T  Textbook of Medical Parasitology merits
commendation
commend ation for many reasons.It is a precious
reference for those involved in the eradication
of parasitism in communities especially among
 product of collaborative eeffort
ffort among the school children and for all with interest in
top parasitologists in the country, including tropical diseases.
faculty members from different medical and Our teachers have been used to prescribing
prescribi ng
science colleges. The comprehensive biological foreign textbooks in tertiary education and
 presentation (gross,
(g ross, microscopic and
a nd molecular)  professionall courses. This is primarily due
 professiona due to
and the extensive and updated epidemiological a mindset that we are not capable of making
data on each parasite speak of the rigorous our own. This textbook is proof that Filipino
scholarship of the contributors and the editors. authors can and should provide the information
It should have a special place in all public and needed by our students, professionals
professional s and policy
 private health
health libraries. makers. Learning, practice and policy making

ichhise b
 publT alo
thok 
anmd aok tehsear c pcear  imleedticoalmsetuddiceanl,ts
sas b hotauilndi,nagf tienr tahlle, bliefeinantdhethceonetnevxitr oonf m
so b wehnatt oisf
and to various health professionals
professional s and policy the learner and user.
makers important and relevant scientific UP Manila is particularly prou
proud
d to be the
information on parasites
parasit es that impact on human  publisher of this textbook
textbook..

MARITA V. T. REYES
Chancellor  
University of the Philippines Manila

xxiii 
 

xxiv  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

Foreword to the First Edition 

t is a great pleasure and honor to write Parasitic infections constitute a major

I the foreword of a book which addresses a
significant need for information. Definitely
Definitely,,
 public health problem
problem in ththee Philippines
and many parts of the world. No geographic
there is a need to make information on area is spared from colonization by parasites.
medically important parasites more accessible. 
accessible.   The seriousness of the problem is not only
The first
first Philippine
 Philippine Textbook of Medical confined to the morbidity and mortality that
Parasitology
Parasitol ogy is relevant because it isfocused on  parasites can cause. Its effects are also linked to
medical parasites whichwhic h are found in our local different aspects of societal life such as decreased
setting. It is therefore an excellent complement  productivity and growth
growth,, mental retard
retardation,
ation,
to existing books on parasitology which are and malnutritio
malnutrition.
n.
foreign in orientation. All attempts should be made to control
This book is a welcome addition to  parasitic diseases because of their overwhelming
locally published learning resources which at ill effects. These have to be a multidisciplinary

tdhif efim ieesnatnadr etr qau
cuoltm vaitiels m
of eaegdeitr o. r W
s aenr 
deaaluiztehotr 
hse. ar daesr 
un
 p loingigstr se, qaunitr hinr og p, ocolongtir s b
itoak  , teicoonlsogf r 
itsu riso
 tm
s,
I congratulate Dr. Vicente Y. Belizario, Jr. and immunologists,
immunolog ists, clinicians and economists, to
his team for their commitment and dedication name a few.
to our countrymen. It is timely that this book It is my wish that this book receive the
is published in 1998, the 100th year of the attention it deserves because the knowledge
Republic and the 90th year of the University it contains is a powerful means to combat
of the Philippines Manila.  parasitism in our
our country
country..

PERLA D. SANTOS-OCAMPO
Chance lol r 
 
University of the Philippines Manila

xxv 
 

xxvi  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

Preface 

arasitic infections remain as a major Health Organization are included for reference
P challenge to public health especially in
developing countries like the Philippines. While
 purposes.For thefirst
the first  time,relevantpolicies and
guidelines from the Department of Health are
there have been significant advances in terms listed for the guidanc
guidancee of the readers.
of a better understanding of the epidemiology The production of this book would not
of these infections, improved diagnostic tools have been possible if not for the major efforts
and newer approaches to control, in many of the members of the Editorial Team as well
areas where these infections are encountered, as the various contributors of the chapters and
 barriers to early diagnosis, trea
treatment,
tment, control sections who are themselves experts in their
and prevention remain. own respectivefields.
respective fields. Prof.
 Prof. Winifreda de Leon,
The development of this learning resource, withherlong experienc
experienceeinparasiticinfections,
Medical Parasitology in the Philippines, is a remains the Co-Editor of this book, while Dr.
response to these continuing challenges. More Edsel Maurice Salvaña and Dr. Francis Isidore

r ar ionveiedsiinngm
tahnadnt p ubaltiicohnef 
 beadsiicciinnef ,o prm esnintsg,
aoltr hs,tnuudr  Leosttaeñr eC
T s hseur av p
edr oavsidAesdsovciitatleasEsdisittaonr cs.e M . uPsahul
tor 
 p
medical technology, and other allied health this book writing project forward. The Editorial
 professions, this book pro
 professions, provides
vides imp
important
ortant Team is very grateful to Johnson & Johnson
updates of chapters included in the first two Corporate Contributions Committee that
editions of the Philippine Textbook of Medical  provided a grant for the book writing initiative
Parasitology as well as an introduction to in a similar way that it provided support for
important subject areas like neglected tropical the development of the first two editions of
and parasitic infections and emporiatrics. This the book.
 book therefore
therefore may b bee considered as the third With the launching of this book, may there
edition of the book.  be hope that parasitic infections in this
this beloved
In this edition, the life cycles developed
de veloped by country would be better understood, diagnosed,
the United States Centers for Disease Control treated, controlled
controll ed and prevented fora healthier
and Prevention are utilized, and as in the other and more productive populace.
earlier editions, Bench Aids
Aid s developed
develop ed by Wo
Worl
rld
d 
VICENTE Y. BELIZARIO, JR.

xxvii 
 

xxviii  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

 Acknowle
 Ackn owledgmen
dgments
ts 

he Third Edition of the Philippine will lay the foundation for a life of learning in
T  Textbook of Parasitology was made
 possible through a generous educationa
educationall grant
medical parasitology for the next generation of
leaders in this field.
field. Working
 Workingwith you has been
from Johnson & Johnson (Philippines) Inc., a great honor and privilege.
through its pharmaceutical division, Janssen Our deepest gratitude to the University of
Pharmaceutica,
Pharmace utica, our stalwart partners in this the Philippines Press for providing the technical
undertaking. expertise and know-how to produce an excellent
The editors would like to acknowledge the learning resource.
invaluable contributions of the new associate Very special thanks to the Chancellor of
editors, Dr. Edsel Maurice Salvaña and Dr. the University of the Philippines Manila, Dr.
Francis Isidore To
Tota
tañe
ñess for their able assistance in Manuel B. Agulto, for his wholehearted support
this revision. We would also like to acknowledge of this book writing initiative that will provide
the herculean efforts
effor ts of the Edito
Editorial
rial Tea
Team
m for a valuable reference and guide for students

tahned cr oeu
-r netvliessin
s ghomuar ns us pscer ni  ppt tr 
seavsisw
inegll, ar sevm
ieewetin
ingg, aFnildi  p
phineoa p
ltheo p e.fessionals in the ser vice of  the
 pr lo
the tight deadlines. In addition, we recognize We are most grateful to our respective
the contributions of Dr. Carlos Miguel Perez, families for their understandi
understanding
ng and
Dr. Timothy Ting, Dr. Ernesto Balolong, Jr., encouragement in the course of preparing this
and Amelia Breyre in providing inputs for the  book. Thank you for allowing us to work more
improvement
improvem ent of selected articles. than the usual office hours and beyond the
We are
are tremendously indebted to the confines of our  workplace.
 workplace.
individual chapter and section contributors. And finally, we give thanks for the
Your expertise and dedica
dedication
tion to your profession enlightenment and guidancefrom the Almighty,
of teaching and research are the
th e heart and soul to Whom this work is humbly offered.
of this book. The chapters and sections herein
VICENTE Y. BELIZARIO, JR.
WINIFREDA U. DE LEON

xxix 
 

CHAPTER 1 

Introduction
Introduct ion to Medical
Me dical Parasitology 
Parasitology 

Ge n er al Consider ations 
Vic ente Y. Belizar io, Jr .

arasitology is the area of biology concerned  protected from harm, while it does not cause
 
with the phenomenon of dependence of one   any damage to the tissues of its host. Mutua
living organism on another. Medica
 Medicall Para
Parasit
sitolo
ology
gy
 Mutualism
lism
is a symbiosis in which two organisms mutually
is concerned primarily with parasites of humans  benefit from each other like termites and the
 benefit from
and their medical significance, as well as their flagellates in their digestive system, which
importance in human communities. Tropical synthesize cellulase to aid in the breakdown
 Medicine is a branch of medicine that deals of ingested wood.  Parasitism is a symbiotic
with tropical diseases and other special medical relationship where one organism, the
t he parasite,
 problems of tropical regions. A tropical disease lives in or on another, depending on the latter
is an illness, which is indigenous to or endemic  for its survival and usually at the expense of the  
in a tropical area but may also occur in sporadic host. One example of a parasite is Entamoeba
or epidemic proportions in areas that are not   histolytica , which derives nutrition from the  

tropical.
diseases.Many
  tropical diseases are parasitic human host and causes amebic dysentery.  
Parasites 
Biological Relationships 
Parasites are often described according to
Organisms may develop unique relationships their habitat or mode of development. A parasite
due to their habitual and long associations living inside the body of a host is known as an
with one another. These relationships are very endoparasite, whereas a parasite living outside
o utside
important to their survival. Symbiosis is the the body of a host is an ectoparasite . The
living together of unlike organisms. It may also  presence of an endoparasite
endoparasi te in a host is called an
involve protection or other advantages to one infection, while the presence of an ectoparasite
or both organisms.   on a host is called an infestation. A parasite is
Different forms of symbiosis may be  considered erratic when it is found in an organ 

thisetiansgsuoicsihateidononis tdhet b
d asiesntoaf l  wtoheotnhe r   of  r thneot
r im
two organisms. Commensalism is a symbiotic
relationship in which two species live together
t ogether
and one species benefits  from the relationship
without harming or benefiting the other. 
For example, Entamoeba coli in the intestinal
lumen are supplied with nourishment and are 

1
 

2  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

arises. A parasite, which establishes itself in a Vectors

host where it does not ordinarily live, is called
Vectors are responsible for transmitting the
an accidental or incidental parasite. A perman
 permanent
ent
 parasite from one host to another. A biologic
 parasite remains on or in the body of the host
vector transmits the parasite only after the
for its entire life, while a temporary parasite lives
latter has completed its development within
on the host only for a short period of time. A
the host. A biologic vector is therefore an  
 spurious
 spurious parasitee is a
parasit free-living organism that 
 passes through
th rough the digestive
dig estive tract
t ract without easns A  maor tsqouf ith
iael p
enetd   s oes pucakr ass bitleoos dlif f er ocm
’ .W
yclae patiheennt
infecting the host. 
with filariasis, the parasite undergoes several
Hosts  stages of development from first
first stage
 stage larva
to third stage larva before the latter (infective
Hosts can be classified  into various types
classified into stage) is transmitted to another susceptible
 based on their role in the life cycle of the host. A mechanical or phoretic vector , on the
 parasite. A definitive or final host is one in other hand, only transports the parasite. Flies
Flies
which the parasite attains sexual maturity. In and cockroaches that feed on fecal material
taeniasis, for example, humans are considered may carry enteric organisms and transfer these
the definitive host. An intermediate host harbors
harbors to food, which could be ingested by humans.
hum ans. 
the asexual or larval stage of the parasite. Pigs or
cattle serve as intermediate hosts of Taeniaspp., Exposure and Infection 
while snails are hosts of Schistosomaspp. If there Majority of parasites are pathogens
is more than one intermediate
i ntermediate host, these can be  which are harmful and which frequently
classiAfie pdaar safit er sntiacnhdoset coisndonineteir nmwedhiiacthe hthoests.
 s
cause mechanical injury to their hosts. A
carrier harbors a particular pathogen without
 parasite does not develop further to later stages.
However, the parasite remains
remai ns alive and is able manifesting
is the processany signs and symptoms.
of inoculating  Exposure
 Expos
an infective ure
agent,
to infect another susceptible host. For
F or example,
onimussmetace
 Paragonimu
 Parag metacercaria
rcaria in raw wild boar meat while infection connotes the establishment of
the infective agent in the host.  
can pass through the intestinal wall of humans
and complete its development. In this case, the The incubation period is
is the period between
wild boar serves as a paratenic host transferring infection and evidence of symptoms. It is
the infective stage to humans.
hu mans. Paratenic hosts sometimes referred to as the clinical incubation
 period . The pre-patent period , also known as the
 pre-patent
are important because they widen the parasite
biologic incubation period , is the period between
distribution and bridge the ecological gap
infection or acquisition of the parasite and
 between the definitive and intermediate hosts. 
evidence or demonstration of infection.
There are also other animals that harbor
 Autoinfection results when an infected
the parasite other than definitive, inntermediate,
termediate,
inf deicvtiidouna.lI bneecnotm
er eos bhiaissiso, winnf eecdctiir oenct msoayur occecuor f
and paratenic hosts. These are known as
reservoir hosts . They allow the parasite’s
the parasite’s life
 life
cycle to continue and become additional
through hand-to-mouth transmission. Infective
eggs may end up in the hands by scratching
sources of human infection. Pigs are reservoirs
of Balantidium coli , field  rats of Paragonimus
field rats
the perianal areas where the gravid females lay
their eggs. Alternatively, parasites may multiply
westermani , and cats of Brugia malayi. internally, such as Capillaria philippinensis .
Humans are not always the final host.
Superinfection or hyperinfection happens when
Humans may be the most important host in
the already infected individual is further
the spread of the disease or an incidental host of
 parasites prevalent in
in other animals. 
infected with the same species leading to
t o masi
masisv
svee 
 

CHAPTER 1: Introduction to Medical Parasitology   3 

infection with the parasite. An alteration in of infection. Autoinfection where the infected
the normal life cycle of Strongyloides results in  person himself is the source of infection
infecti on is seen
a large increase in worm burden, which may in the life cycles of Capillaria philippinensis,
lead to severe debilitation or even death due to  Enterobius vermic
 Enterobius ularis,  Hymeno
vermicularis  Hymenolepis
lepis n
nana, and
ana
an increase in the proportion of rhabditiform Strongyloides stercoralis. 
larvae that transform into filariform larvae while
Modes of Transmission  
in the gut.
Sources of Infection 
Since the most common source of parasitic
infection is contaminated food and water,
There are various sources of parasitic the most likely portal of entry is the mouth.
infections. The most common sources are Majority of infections with cestodes, trematodes,
contaminated soil and water. Lack of sanitary and intestinal protozoans are foodborne: Taenia
toilets and the use of night soil or human  solium, Taenia saginata, and  Diphyllobothrium
excreta as fertilizer allow the eggs to come in latum from eating food harboring the infective
contact with the soil and favor the development larval stages; Entam
 Entamoeba
oeba hhistolytica and Giardia
istolytica
of Asca
 Ascaris oidess , Trichuris trichiura ,
ris lu mbric oide lamblia from drinking water contaminated with
Strongyloides stercoralis, and hookworm.
hookwor m. Water cysts; andClonorchis, Opistorchis, and Haplor
 Haplorchis
chis
may be contaminated with cysts of amebae or through ingesting raw or improperly cooked
flagellates, as well as cercariae of Schistosoma. freshwater fish
fish  containing infective larvae.  
Another possible source of infection is food, Skin penetration is another route of
which may contain the infective stage of transmission. Hookworms and Strongyloides 

thr eem paatr 
oadseitaen, dasceesxteom
d p edct b
e ilnifif ec ioynsa. Cnounms bum
er  potif on eS nchtei r t ovioameax ps p
 s  s  poescuir 
ees eonf  tsekr inskitno vsioailw, awtehr i.le
of undercooked or raw freshwater fish can Arthropods also serve as vectors and  
result in several intestinal and liver fluke transmit parasites through their bites. Examples
infections. Raw crabs are considered a delicacy are agents of malaria, filariasis, leishmaniasis,
in areas where paragonimiasis is endemic, trypanosomiasis, and babesiosis.  
while raw Bullastra snails are associated with Another way of acquiring infection is
 Artyfechinostomum
 Artyfechinostomu m malayanum infection.  through congenital transmission. Toxoplasma
Arthropods can also transmit infection.  gondii trophozoites can cross the placental
Mosquitoes are vectors of malaria and filarial  barrier during
du ring pregnancy.
pre gnancy. In transmammary
trans mammary
 parasites. Triatoma bugs are carriers of infection with  Ancylo stoma and Strongyloides,
 Ancylostoma
Trypanosoma cruzi causing Chagas disease. the parasites may be transmitted through
Sand flies (e.g.,  Phlebotomus spp.) are the mother’s milk. 
milk.  
natural vectors of all types of Leishmania. Other
 Leishmania Other ways of acquiring the infection
animals, whether wild or domesticated, may include inhalation of airborne eggs of  En
 Enter
terob
obius
ius
also harbor parasites. Cats are direct sources of and sexual intercourse as in the case of
Toxoplasmainfection, while rats may be infected Trichomonas vagi naliss. 
vaginali
with Hymenolepis nana.
nana
Nomenclature 
Other sources of infection include another
 person, his beddings
bedding s and clothing,
clothin g, as well as the Animal parasites are classified according
immediate environment
or even one’s
one’s self. he has contaminated,
 self. Asymptomatic carriers of
to the International Code of Zoological
 Nomenclature. Each phylum is divided into
 Entamoeba
 Entam oeba histo lytica working as food handlers
histolytica classes, which are further subdivided into orders,
in food establishments may be importantsources   families, genera, and species. At times, the  
 

4  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

further divisions of suborder, superfamily, and number of worms per infected

in fected person.
person.This may
subspecies are employed. Scientific names are  be measured directly or indirectly and is also
latinized; family names are formed by adding   referred to as the worm burden. In the case of
-idae to the stem of the genus type; generic soil-transmitted helminths, it can be measured
names consist of a single word written in initial directly by counting expelled worms during
capital letter; the specific name always begins treatment, or indirectly by counting helminth
with a small letter. The names of the genera  eggs excreted in feces. The latter is expressed as 
and species are italicized or underlined when the number of eggs per gram (epg).  
written.  Clinical consequences of infections or  
diseases that affect an individual’s well -being
Life Cycle 
refer to morbidity . 
Through adaptation to their hosts and the
Treatment 
external environment, parasites have developed
life cycles, which may be simple or complicated.  Deworming is the use of anthelminthic
Most parasitic organisms attain sexual maturity drugs in an individual or a public health
in their definitive hosts. Some spend their  program. Cure rate refers to the number
entire lives within the host with one generation (usually expressed as a percentage) of previously
after another, while others are exposed to the  positive subjects found to be egg negative
negative 
external environment before being taken up on examination of a stool or urine sample
 by an appropriate host. The larval stage of the using a standard procedure at a set time after
 parasite may pass through different stages in an  deworming.  Egg reduction rate (ERR) is the 
iAnstethr m
e  leif deiactyechleo bset  b f oer sem
coem itor r eeacohm
es palificnataeldh, othste.  baer secednotnageexaf amllininateiogng  ocf oausnttosoalf oter r udr ienweosar m pinlge
 p
lesser the chances are for the individual parasite using a standard procedure at a set time after
to survive.  the treatment. 
The perpetuation of a species of parasite
p arasite Selective treatment involves
involvesindividual-level
depends upon its ability to ensure transmission deworming with selection for treatment based
from one host to the next. The parasite must,
mu st, on a diagnosis of infection or an assessmentof the
therefore, adapt to protect itself from the host’s intensity of infection, or based on presumptive
defenses and the external environment, and it grounds. This strategy can be used in whole
must overcome the attrition in the species by  populations,
 populat ions, or in defined risk groups. Targeted
 producing numerous progen
progeny. y. treatment is group-level deworming where  
the (risk) group to be treated (without prior
Epidemiologic Measures 
diagnosis) may be defined by age, sex, or other
 Epidemiology is the study of patterns, social characteristics irrespective of infection
distribution, and occurrence of disease. status. Universal treatment is population-level
 Incidence is the number of new cases of deworming in which the community is treated
irrespective of age, sex, infection status, or other
 period of time. Prevalence is the number social characteristics.  Preventive Chemotherapyis
the regular, systematic, large-scale intervention
intervention
involving the administration of one or more
a particular parasite species at a given time.
ti me. drugs to selected population groups with the
Cumulative prevalence is the percentage of aim of reducing morbidity and transmission of
individuals in a population infected with at selected helminth infections. 
Coverage refers to the proportion of the
target population reached by an intervention. It 
 

CHAPTER 1: Introduction to Medical Parasitology   5 

could be the percentage of school-age children reservoirs of disease. It also covers the provision
treated during a treatment day.  of safe drinking water and food safety; housing
 Efficacy  is the effect of a drug against an
 Efficacy that is adequate in terms of location, quality of
infective agent in ideal experimentalconditions shelter, and indoor living conditions; facilities
and isolated from any context.  Effectiveness for personal and domestic hygiene; as well as
is a measure of the effect of a drug against safe and healthy working conditions.  
an infective agent in a particular host, living   Sanitation is the provision of access to  
in a particular environment with specific adequate facilities for the safe disposal of human
ecological, immunological, and epidemiological
epidemiological excreta, usually combined with access to safe
determinants.
determinan ts. Effectiveness is usually measured  drinking water. 
 by means of qualitative and quantitative
Eradication versus Elimination 
diagnostic tests which detect eggs or larvae in
feces or urine after an optimal time interval,  Diseasee eerad
 Diseas radica
icationis defined as a permanent
tion
which is variable for each parasite. Cure rate reduction to zero of the worldwide incidence of
and egg reduction rate are indicators that are infection caused by a specific agent, as a result
commonly used to measure the reduction  of deliberate efforts. Once this is achieved,
in prevalence and reduction in intensity of continued measures are no longer needed. On
infection, respectively.  the other hand,disease eliminationis a reduction
 Drugresistance is a genetically transmitted
resistance to zero of the incidence of a specified disease in a
loss of susceptibility to a drug in a parasite defined geographic area as a result of deliberate
 population
 populat ion that was previously
previousl y sensitive
sensiti ve to the  efforts. Continued intervention or surveillance 
appropriate therapeutic dose.   measures are still required.  
Prevention and Control  References 

 Morbidity
 Morb controll is the avoidance of illness
iditycontro Beaver PC, Jung RC, Cupp EW. Clinical
caused by infections. It may be achieved by  parasitology.. 9th ed. Philadelphia:
 parasitology Philadelphia: Lea and
 periodically deworming individuals
individuals or groups,
groups, Febiger; 1984. 
known to be at risk of morbidity.   Markell EK, John DT. Medical parasitology.  
 Information-education-c
 Information-education-communica
ommunication
tion 8th ed. Philadelphia: W. B. Saunders
(IEC) is a health education strategy that aims Company; 1999. 
to encourage people to adapt and maintain Markell EK, Voge M, John DT. Medical
healthy life practices.  parasitology.
 parasitolo gy. 7th ed.
ed . Philadelphia:
Philad elphia: W. B.
 Environmen
 Environmental
tal m
management is the planning,
anagement Saunders Company; 1992.  
organization, performance, and monitoring   Muller R. Worms and disease: a manual of
of activities for the modification and/or medical helminthology. London: William
manipulation of environmental factors or their Heinemann Medical Books Limited; 1975.  
interaction with human beings with a view to  Neva FA, Brown HW
HW.Basic clinical
clinical par
parasit
asitolo
ology.
gy.
 preventi ng or minimizing
 preventing minimizi ng vector or intermediate
intermedi ate 6th ed. Connecticut: Appleton and Lange;
host propagation and reducing contact between 1994.
humans and the infective agent. Walter-Beck J, Davies J. Medical parasitology.  
 Environmental sanitation involves 3rd ed. Missouri: The C. V. Mosby
interventions
risks includingtothe
reduce environmental
safe disposal health
and hygienic
Company; 1981.
World Health Organization. Prevention and
management of human and animal excreta, control of schistosomiasis and intestinal
refuse, and waste water. It also involves the nematodes. Geneva: World Health
control of vectors, intermediate hosts, and   Organization; 2002.
 

6  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Host-Parasite Relationships
Vicente Y.
Y. Belizario, Jr.

he relationship between parasite and host spp. are hermaphroditic, that is, they contain a
has gradually evolved through the ages. The   
 process has produced changes in i n the parasite
p arasite complete
of setofthousands
producing male and female
of ova.organs capable
Furthermore,
T 
and in its life cycle, consequently affecting the
life of its host. 
flukes undergo asexual reproduction in the
flukes undergo
intermediate hosts to increase the number of
Adaptation causes changes in the molecular  progeny.
 biology, biochemistry, immunology, and Parasitic existence may also result in
structure of the parasite. Parasites that are more  profound biochemical adaptations. Such
specialized have shown the greatest changes, changes include loss of certain metabolic
most of which are essential for survival.    pathways common to free-living organisms.
The most noticeable adaptations are This process is called streamlining, that is the
found in the locomotory and digestive inability of the parasite to synthesize certain
organs. Protozoans belonging to the Phylum cellular components and the need of the parasite
Apicomplexa have no locomotory organelles, to obtain these from a host. Streamlining  
and these organisms are mostly parasitic. Free- is exemplified
exemplified  by
by hemoflagellates
hemoflagellates and
 and other
living flatworms have cilia on their epidermis,  helminth parasites. These changes in metabolic 
nohtilhea pvear ansiyt.icCcessttodessaandtr ter m
w emataotoddeseso bdtoain a paeyu btieccsotm
chatehmwoatyhser m
 p r aetegthiees.tar ge
get  of   f utur e
nutrients through their tegument, which is Some parasites have developed specialized 
 provided with microvilli. Flatworms have mechanisms needed for entry into the body
highly specialized organs of attachment, such or tissues. The trophozoites of  Entamoeba
as hooks and suckers, which anchor the parasite histolytica secrete cysteine proteinases, which
inside the body of the host and facilitate tissue allow the parasite to penetrate the mucosa and
migration. The size and shape of the parasite adhere to the underlying layer and surrounding
are also adapted for maintaining its hold in tissues. No such enzyme has been found in the
the host. Adult Ascaris worms maintain their commensal Entamoeba coli . The cercariae of
 positionn inside the intestinal
 positio intesti nal wall by constant Schistosoma contain penetration glands, which
movement. The integument is thickened to  produce an enzyme capable of digesting
digesti ng the skin
resist enzymes and juices in the digestive tract allowing entry into the body of the host. All
of humans and to protect against dessication  cestode embryos have six hooklets, which aid
and physical injury. In intestinal flukes, the   them in tissue penetration before developing  
tegument is covered with spines to prevent into encysted larvae.  
abrasion. Special coverings of ova, larvae, and Effects of the Parasite on the Host  
cysts protect the parasite during its free-living
stage. These coverings also aid in resisting   Some organisms may live inside the body
digestive juices once the parasite is ingested by of the host without causing any damage, but
the host.  in most instances, they have the ability to
Reproductive systems of flatworms are inflict damage to their
th eir host. There are several
highly elaborate and complicated. Alltapeworms mechanisms by which parasites cause injury
and flukes,
flukes, with
 with the exception of Schistosoma
Schistosoma   to the host. The most common mechanism  
 

CHAPTER 1: Introduction to Medical Parasitology   7 

is by interference with the vital processes of  blood factor

f actor increases
incre ases the susceptibilit
susce ptibilityy of an
the host through parasitic enzymes. Secretory individual to  Plasmodium vivax
vi vax infection. 
and excretory products elaborated by many Another important aspect is the nutritional
 parasites allow
all ow them to metabolize
metaboli ze nutrients
nutrient s status of the host. A diet rich in protein is
obtained from the host and store these for not suitable for the development of intestinal
energy production. This is best exemplified by  protozoans, while a low-protein diet favors
 Entamoeba
 Entamoeba histolytica trophozoites that secrete  
histolytica the appearance of symptoms of amebiasis  
cysteine proteinases,
proteinases, which do not
no t only digest and complications of the disease. A high
cellular materials but also degrade epithelial carbohydrate diet favors the development of
 basement membrane
membrane facilitating
facilitating tissue invasion.
invasion.  some tapeworms. 
Another mechanism is through invasion
i nvasion Immune processes play an important role in
and destruction of host tissue. One example host-parasite relationships. Absolute immunity
is Plasm odium, which invades red blood cells.
 Plasmodium to reinfection occurs rarely following protozoan
After multiplication, the host’s red blood cells infections, and probably never happens with
rupture resulting in the release of merozoites. helminth infections in humans. Acquired
In Schistosomajaponicum infection, cumulative immunity may be very important in modifying
deposition of eggs in the liver stimulates an the severity of disease in endemic areas. 
immune response mechanism resulting in
References 
granuloma formation and then fibrosis  which
leads to portal hypertension and massive Beaver PC, Jung RC, Cupp, EW. Clinical
hemorrhage in the venules. Hookworms have    parasitology.. 9th ed. Philadelphia:
 parasitology Philadelphia: Lea and 
cmuttcionsga palnadtesd,ewsthr iocyhtchaenvaitlltia.cLhatr ogethneuimteestr isnoaf l
n b F pe btoigner D
Cr om ;  1W
98,  4S.avioli  L.  Intestinal  ppar asitic
worms such as Ascari
 Ascariss form tangled masses that infections and urbanization. Bull World
can lead to intestinal obstruction. An Ascaris Health Organ. 1993;71(1):1 – 7 7..
worm in the intestine may invade other organs Markell EK, John DT. Medical parasitology.  
like the appendix and bile ducts and
an d may cause 8th ed. Philadelphia: W. B. Saunders
a surgical emergency.  Company; 1999. 
Parasites can also deprive the host of essential Markell EK, Voge M, John DT. Medical
nutrients and substances. Heavy hookworm  parasitology.
 parasitolo gy. 7th ed.
ed . Philadelphia:
Philadel phia: W. B.B.
infection causes massive intestinal bleeding which Saunders Company; 1992.  
results in chronic blood loss and iron deficiency Muller R. Worms and diseases: a manual of
anemia.  Diphyllobothrium latum lat umcompetes with medical helminthology. London: William
its host f or  the availa ble supply of  Vitamin B12,  Heinemann Medical Books Limited; 1975.  
thus resulting in megaloblastic anemia.    Neva FA, Brown HW HW.Basic clinical
clinical par
parasit
asitolo
ology.
gy.
6th ed. Connecticut: Appleton and Lange;
Effects of the Host on the Parasite   1994.
There are several factors which determine Que X, Reed SL. The role of extracellular  
the outcome of an infection. The genetic make- cysteine proteinases in pathogenesis of
up of the host may influence
influence the
 the interaction  Entamoeba
 Entam oeba h
histolytica invasion. Parasitol
istolytica
 between host and parasite. In falciparum Today. 1997;13(5):190 – 3
3..
malaria, possession
some protection, of sickle-cell
while traitofconfers
the presence D uffy 
Duffy Walter-Beck J, Davies J. Parasitology. 3rd ed.
Missouri: The C. V. Mosby Company;
1981. 
 

8  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Immunology of Parasitic Infections  

Edsel Maurice T. Salvaña, Winifreda U. de Leon, Katerina T. Leyritana

he function of the immune system is The ability of the parasites to cause

infections has evolved through the process of  
to protect
 potential pathogthe
ens.body
pathogens. It isfrom invasion
a tightly byled
ti ghtly-control  
-controlled natural selection, since only a proportion of
T 
 balancing act, in the sense that dysfunction
of the immune system can lead to either a
 parasites are able to accomplish
accompli sh this
this.. In the same
way, the host’s ability to defend itself against a  
 permissivee environment
 permissiv enviro nment for
fo r infection
infecti on on one    parasite
 para ’s invasion is also selected for. Some life
site’s
hand, or to unchecked activation which can cycles are so complicated that the parasite has
harm the organism on the other. Immunity adapted means to survive immune assault in
to parasites, especially eukaryotes such as not just one but a variety of hosts, including
helminths and protozoans, is complicated  the definitive host, intermediate hosts, and
 by the fact that, unlike bacterial pathogens, reservoir hosts. 
eukaryotic organisms are similar in make-  The host-parasite relationship remains
up and physiology. Moreover, parasites have dynamic, and while some parasites become
evolved strategies to evade the immune system specific to
specific  to some hosts over time, accidental
over millions of years, and some are so successful infection of erstwhile non-susceptible hosts
that these organisms not only survive but thrive   may eventually lead to establishment of a new 
itnhetyhea br elosoud b jster cetaemd (teo.gc.,oS ncshtiant ot oam
 s  s a  .) wher e
nd s p
intimate r inesteir mvoeim ene bdieactoe,moer  tdhefidnoitm
r, ianyt er vm ivienhaonstthwohsticf hor
exposure to the body
the  body’s
’s immune system.   that organism. This is exemplified by zoonoses
Parasitic infections in humans and animals such as infections with Trypanosoma sp., and
occur when the parasite successfully establishes the newly discovered human malaria parasite
itself in the host and is not eliminated by many  Plasmodium knowlesi.
host defense systems and is able to continue its Host-Parasite Interactions 
life cycle. However,not
However,n ot all interactions between
the host and parasite relationship result in injury  Natural physical barriers to the entry of the
and pathology. It can result in the following  parasite into the body constitute the first
first line
 line
outcomes:  of defense against pathogens. The skin provides
effective surface protection against invasion
•   Parasite fails to become established in from parasites that initiate infection through
the host. skin penetration. Adaptive mechanisms of
•   Parasite becomes established
established and the some helminths allow them to overcome these
host eliminates the infection.   defenses. The filariform larvae of hookworms
•   Parasite becomesestablished, and the and Strongyloides can synthesize a protein that
host begins to overcome the infection aids in the entry through the skin. Schistosoma
 but is not totally successful.  spp. cercariae are capable of skin penetration
penetration
•   Parasite becomes established and the  because of the presence of glands in the anterior
host, in trying
organism, todamaged
becomes eliminate the 
itself.  part The
of themucous
parasitemembranes
that secrete lytic enzymes.
lining the
 
•   Parasite becomes established and kills respiratory, gastrointestinal, and genitourin
genitourinary
ary
the host. tracts provide external barriers to parasite entry  
 

CHAPTER 1: Introduction to Medical Parasitology   9 

as well. Tight junctions between epithelial cells defenses rely on humoral and cell-mediated
serve to prevent passage of all but the smallest mechanisms of action.  
molecules. The low pH of vaginal secretions The innate response happens when the
and gastric juices present a hostile environment  body detects and eliminates
eliminate s pathogens
pathogen s through
throug h
to many microorganisms. For instance, the non-specific mechanisms that use mechanical,
trophozoites of Trichomonasvaginalis
Trichomonasvaginalisare unable chemical, and cytokine-mediated methods to
to survive the acidic environmentof the vagina,  destroy or disrupt invading organisms with  
and once intestinal secretions envelope Giardia little or no delay from the time of invasion. One
lamblia , its motility is greatly diminished method is through phagocytosis bymacrophages
bymacrophages
reducing injury to the host. To evade this type and dendritic cells with subsequent pathogen
pathogen  
of host defense, the infective stages
s tages of helminths  elimination through oxidative killing and use of
that are ingested, like embryonated eggs of toxic peptides. Some intracellular pathogens are
 Ascaris , Trichuris, and Taeniaspp. are protected able to invade and multiply inside macrophages,
from the acidic environment by thick egg shells. like  Leishmania spp., Toxoplasma gondii, and
gondii
The cystic wall of intestinal protozoa like the Trypanosoma cruzi, in which case cell-mediated
 Entamoeba and Giardia are also resistant to immune mechanisms (whether non-specific
non- specific
acidic pH. such as natural killer cells, or acquire cell-
Chemical components of body fluids play mediated immunity through T-lymphocytes)
a major role in the protection of the host. The are required to identify and destroy them.  
lipase content of breast milk, for example, has Toll-like receptors (TLRs) recognize
 been found to be toxic to Giardia lamblia in specific molecules that are non -native to the 
vit r o. Lysozyme f ound in tear s and saliva is a ble  br eocdoygnaintidonsomr e pchr easneinsm
t  sof m   oaf ththoeg enasr .lieTsot
to destr oy micr o r ganisms, lo g with secr eted or e p
IgA immunoglobulins in these fluids.   date, ten TLRs have been identified
identified and
 and each
Physiologic functions of the body also is activated by a bacterial components [e.g.,
inhibit parasite invasion. Peristalsis, motion LPS (TLR4), diacylated lipoprotein (TLR2
of cilia, and human reflexes all serve to expel and 6) and triacylated lipoprotein (TLR 1
 parasites. Coughin
C oughingg enables expectoration
expector ation of and 2), flagellin (TLR5)], viral RNA (TLR3),
aberrantly situated adult  Ascari
 Ascariss lumb
lumbricoid
ricoides
es and other unfamiliar components. Binding of
and eggs of Paragonimus westermani
westermani, and the a specific
specific  ligand to a TLR causes a cascade of
flushing action of urine decreases the numbers reactions down a common signaling pathway
of Trichomonas vagin alis.
vaginalis which produces cytokines such as interferon
In the event that the parasite is able to gamma and interleukin-1. These cytokines
overcome physical barriers, a second host activate natural killer cells and macrophages,
defense comes into play. The penetration of stimulation of which leads to furtherproduction
the body’s  barriers results in a series of events  of inflammatory cytokines, and co-stimulatory 
that facilitate sensing of the invading parasite molecules. TLRs are therefore largely responsible
via pathogen-associated molecular patterns, or for triggering the initial inflammatory response.
through pattern recognition responses which They function as pyrogens and synthesize
enable the body to mount an immune response   response proteins, which then  
inflammatory response
inflammatory
that acts towards eliminating or limiting the increase the number and function of phagocytic
infection. cells. 
Host-Immune Response 
The host, once infected, is exposed to the
 parasite antigens,
anti gens, which
whi ch in turn can stimulate
sti mulate
The host possesses both innate and the host to mount an acquired specific response
acquired immune defenses. Both kinds of   against the antigen. The expression of acquired  
 

10  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

immunity is the result of a complex series

s eries of Th1 lymphocytes produce gamma
immunoregulatory
immunoregulatory events: activation, induction interferon and interleukin-2 which activate
through proliferation, differentiation, and cytotoxic lymphocytes (with CD8 surface
effector function. The effector function may molecules) and macrophages. This brings about
 be at the end point of a response or it might the cell-mediated immune response.
serve a regulatory function that modulates other Cell-mediated immunity has been observed
functions.  specific  
specific
The parasitic antigens may srcinate from in many parasitic
antigens infections.
induce clonal Parasite-
expansion of parasite-
the surface, from secretions and excretions, and specific T-lymphocytes. They may act by direct
from somatic tissues of the parasite. Following  cytotoxicity on the parasite or indirectly by  
initial contact with antigen (immunologic acting on natural killer cells or the antibody
 priming ), subsequent
 priming), subsequ ent antigen
antig en exposure
exposu re leads  producing B-lymphocytes.
B-lymphocytes. Migrating larvae of
to more rapid and vigorous immune responses, Toxocara canisare killed through cell-mediated
leadingtoimmunologic memory.
memory.Theresponse activity. 
of acquired immunity is either antibody- Th2 lymphocytes produce interleukins
dependent or cell-mediated.  4, 5, and 6 that enhance the proliferation and
Most of the time, immunity is directed differentiation of B-lymphocytes into plasma  
against the antigen that induced the response. cells, which are responsible for immunoglobulin
immunoglobulin
Cross-reactivity does occur. The antigen may  production. The antibodies that are produced
 be present in just one
o ne developmental
develo pmental stage or  bind with specific parasite antigens and can
in just one species of the parasite. There are  activate complement and include the following  
lltoigf  etnhse,sthaogwesevoef  p
an r , atr haasittehdaveeve bloe penmdene teocr teind ainll gEm, iIngtGh,icIignM
classeIns: hIel f e,catinodnsI,gtAh.e most common
members of a genus. It is therefore important responses include eosinophilia and elevated
to remember that an immune response does serum IgE. With lumen-dwelling  Asca
 As ca ris
not always equate with protection, and that lumbricoides and Trichuris trichiura, however,
conversely, immunity to one pathogen may the immune
immu ne response
respons e is not as intense
intense compared
confer immunity to another closely related with lymphatic dwelling Wuchereria bancrofti
species.  and  Brugia malayi
malayi since contact with both
recognition and effector elements of the
Acquired Immune Response 
immune system is less intimate. Immunologic
The immune response to parasitic response is also marked in visceral larval
infections is under well-defined genetic control infections with  Paras
 Parastrongy
trongylus
lus cantonensis and
cantonensis
and has a strong influence over the outcome of Toxocara canis which are less likely to have
infection in terms of resistance,
resistance, susceptibility, immune-evading mechanisms since they are not
and pathology. The major histocompatibility specifically adapted to the human host.
specifically adapted
complex ( MHC ) gene products help regulate IgE antibodies that are bound to the
T-lymphocyte activities.  Human leukocyte
leukocy te mucosal mast cells, eosinophils, and goblet
antigen ( HLA) is also a fact
factor.
or.  cells can mediate the eventual expulsion of
The specific immune response to the adult gastrointestinal helminths. IgE has also  
 parasite begins when parasitic antigens are  been identified on
on inflammatory cells involved
 processed an dwhich
and presented
presente d to belong
the CD4toT-helper
Tthe
-helper in the cytotoxic action on some parasites
lymphocytes, either Th1 like Schistosoma spp. referred to as antibody
or Th2 subset. These subsets of T-helper dependent cell-mediated cytotoxicity (ADCC).
cells are responsible for producing different There are a variety of activating molecules
lymphokines.  expressed by the eosinophils that mediate  
 

CHAPTER 1: Introduction to Medical Parasitology   11 

ADCC. Among these are eosinophil activating  parasite life cycles, location
locati on within body sites
si tes
factor (EAF), interleukin-5, and granulocyte-
g ranulocyte- that are relatively protected from the immune
monocyte colony stimulating factor (GM-CSF). response, and antigenic complexity. 
Destruction of microfilariae
microfilariae among
 among patients In addition, natural selection and
with tropical pulmonary eosinophilia has been adaptation have resulted in deployment by
attributed to ADCC mediated by IgE and the parasite of various mechanisms to avoid
 
eosinophils.
have Cellstolike
been found neutrophils
participate as well.  the
and platelets
in ADCC destructive
These effect of the
major mechanisms host induction
include response.of
 
With homocytotrophic IgG1, IgE can immune suppression, antigenic variation, host
act on mast cells and basophils, which can mimicry, and sequestration among others.  
lead to degranulation and eventual release  A. Resistance to Immune Response  
of pharmacologically active substances.  
Unregulated activation can result in an Protozoa and helminthic parasites that
anaphylactic Type 1 hypersensitivity reaction enter the blood stream or tissue are often
as seen during the rupture of  Echinococcus able to survive and replicate because they are
losus hydatid cysts. The same immediate
 granulosus
 granu resistant to the host innate
in nate immune response.
response.
hypersensitivity reaction has been observed at Parasites in humans are usually resistant to
the site of the bite of several arthropods like complement. Macrophages can phagocytose
mites and ticks.   protozoa, but the cuticle and integument of
The combined activity of IgG and IgM helminthic parasites make them resistant to
can prevent penetration of erythrocytes by   the cytotoxic effects of both neutrophils and  
 P la smod ium s p p. and  Babe sia s p p .,  but ar e
gener ally inef f ective against gastr ointestinal suar f fca r co ph
m e magoelesc. uTlehsisthmatay b bineddcuoemt po lethmeenlotssor of
helminths. In the presence of complement acquisition of host regulatory proteins such as
activity, these antibodies can mediate lysis of decay accelerating factor. Trypanolytic factors
trypomastigotes of Trypanosoma cruzi and, even such as apolipoprotein L-1 (APOL1) destroy
d estroy
in the absence of the complement, are involved non-human trypanosomes except Trypanosoma
in the rapid phagocytosis of the same parasites.  brucei which has evolved resistance through
Secretory IgA in the intestines protect against expression of serum resistance-associated
metacestodeandgastrointestinalinfections.IgM  protein. A frameshift
frameshi ft mutation
mutat ion in the
t he APOL1
with secretory IgA mediate ADCC in Giardia gene enables a non-human trypanosome ( T.
lamblia infection. Among immunocompetent evansi ) to infect a human, and addition of
individuals, Cryptosporidium infection is self- recombinant APOL1 restored trypanolytic
limited due to the combined action of IgA and activity. 
lgG with cell-medicated immunity, which helps B. Immune Suppression  
cleave the parasite from the enterocytes.  
In many infections, be it microbial or There are parasites that can reduce
 parasitic, the host can activate its non- specific, the immune function of macrophages that 
specific,  humoral, and cell-mediated defenses result in lower capacity of phagocytosis and
all at the same
s ame time.  defective processing of antigen, as in the case
of Plasmodium spp. infection. In Trypanosoma
Parasite Evasion Mechanisms 
brucei infection, the trypomastigotes can
Parasites have several characteristics that  produce large amounts of surface
surface glycoproteins.
glycoproteins.
make it difficult for the host to detect and This affects the processing of the proteins
eliminate them: parasite size, complicated   due to antigenic competition and at the 
 

12  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

same time impairs the B- and T-lymphocyte Malarial parasites, especially Plasm

 Plasmodium
odium
activities resulting in diminished production of arum , exhibit antigenic diversity. The
 falciparum
 falcip
lymphokines and immunoglobulins.  mechanism is through repeat variation of the
yticasuppresses
 Entamoebahistolytica
 Entamoebahistol macrophage encoded polypeptides, which contain tandem
t andem
respiratory burst and consequent nitric oxide sequences of amino acids, as observed in
 production,
 producti on, produces
prod uces a suppressor
suppr essor factor
fact or that merozoite surface antigen (MSA) and ring-

caninvasion
of inhibit movement
(monocyteoflocomotion
monocytes inhibitory
to the site   infected erythrocyte
These repeat surface
sequences antigen epitopes,
are antigenic (RESA). 
factor), and inhibits complement assembly. In which stimulate antibody production. With
la infection, there is down regulation of  
 Fasciola
 Fascio variation, therefore, antibodies fail to recognize 
Th1 lymphocytes. In filarial infections with the antigen.
Wuchereria bancrofti and Brugia malayi , there
D. Host Mimicry  
is polyclonal hypergammaglobulinemia where
antibodies lack specificity against these parasites. The larval stage of Echino
 Echinococcus
coccus granulosus
granulosus
This has also been observed in Plasmo diumspp.
 Plasmodium in the hydatid cyst has been found
fou nd to carry
infection.  P blood group antigen, and the tegument ofof
Blocking antibodies produced by several Schistosoma spp. adult can acquire antigenic
 parasites like Wuchereria bancrofti can also molecules from the host. Antibodies produced
dampen the effect of immune responses. In against the parasite then fail to recognize non-
america nus infection, the immune
 Necator americanus self from self-antigens.  
response is directed against the deeper layers   E. Intracellular Sequestration 
Sequestration 

odf ivietr stecdu tiocleth beur ta ptihdelyim
chmanugniengr es p
ur of n
acse oisf  its Amastigotes of Trypanosoma cruzi and
integument.    Leishmania spp. proliferate in macrophages
Immune complexes produced in cysticercus in various organs. Toxoplasma gondii multiply
cellulosae infection suppress inflammatory inside macrophages
macrophages as well as in other nucleated
response through inhibition of complement cells. Once intracellular, they are able to evade
activity. Infection with  Plasmodium spp. the host immune
immun e response. 
and Trypanosoma cruzi can also lead to The late intracellular stages of Plasm
 Plasmodium
odium
immunosuppression through the production arum are sequestered from the circulation
 falciparum
 falcip
of immune complexes. In Schistosoma spp. in deep vasculature beds. This is mediated by
infection, complement cannot participate in the the presence of knobs on infected erythrocytes
destruction of the parasite; it has been found that enable them to attach to endothelial
endoth elial cells of
that the complement is consumed by the soluble capillaries. This sequestration process excludes
antigens of the Schistosoma spp.  the parasitized red blood cells from splenic
 and the action of antibodies.  
filtration and
filtration
C.  Antigenic Variation 
Variation  
Adverse Effects of the Immune Response
In Trypanosoma brucei infection, the initial in the Host 
host response against the surface glycoproteins
glycoproteins
of the trypomastigotes is very effective. But in Under normal circumstances, orderly
the subsequent releases of trypomastigo
trypomastigotes,
tes, the  progression of host defenses through the
immune response is no longer effective profile
since different phases results in a well-controlled
the parasites have changed the antigenic immune and inflammatory response that
of their surface coat through variant surface  protects the host from the offending antigen.
glycoproteins
glycoproteins (VSG). Surface protein variation However, dysfunction of any of the host defense
defense
has also been observed in Giardia lamblia.  systems can result in damage to host tissue and 
 

CHAPTER 1: Introduction to Medical Parasitology   13 

 produce clinical
cli nical disease.
dis ease. The normal
nor mal immune
i mmune The main clinical manifestations of
response itself might contribute substantially to Schistosoma spp. infection are related to the
tissue damage as one of four types of reactions: host immune response to eggs that are trapped
Type 1 (Immediate type hypersensitivity), in various organs of the host. This usually
Type 2 (Immune complex formation), Type 3 results in hepatosplenomegaly, fibrosis, portal
(Cytotoxic reactions of antibody), and Type 4 hypertension, and esophageal varices. High
(Delayed-type hypersensitivity).
In acute infection   oma cru
with Trypanos
Trypanosoma cruzi
zi, levels
immune of Schistosoma
complexes spp.
can circulating
produce a antigen in 
condition
the intense immune response to the parasite is very similar to serum sickness. T-cell
T-cell mediated
accompanied by massive damage not only to the  delayed-typee of hypersensitivity
delayed-typ hypersensitivity lymphocytes,
lymphocytes, 
infected cells but also to the surrounding cells when stimulated such as in Schistosoma spp.
including nerve cells and myocytes.It is believed infection, can produce attractants and activators
that this is partially responsible for heart failure of other cells that form destructive granulomas
and meningoencephalitis. Moreover, it has around Schistosoma spp. eggs. In  Leishmania
 been postulated that antibodies to T.cruzi may spp. infections, more macrophages are damaged,
activate adrenergic and muscarinic receptors  be it the cutaneous,
cutaneou s, mucocutaneous,
mucocutane ous, or visceral
 because of similarities between these and parasite type of infection. 
antigens, leading to autonomic dysfunction and Practical Applications 
 predisposition to to arr
arrhythmias.
hythmias. In Wuchereria
bancrofti , there is an overproduction of IgM Understanding the host immune response to
(polyclonal hypergamma-globulinemia)
h ypergamma-globulinemia) due   parasitic invasion is useful in immunodiagnos
immuno diagnosis,
is,  
twohtihceh f eux p e -f sour  pm par teisosnor ocf eal la(r Tg8e)am
nclat ionns atlh  T deof eucntt, aCnudrr  per netdiccotnincge ptthseor nesuim
ltim noar tehgoulolagtyio. n  and
ngu p
of immune complexes in Tropical Pulmonary immunomodulation are products of intense
Eosinophilia (TPE).  and meticulous studies on these immune
i mmune
In recurrent  Plasmodium spp. infection, mechanisms. These insights may hold the key
immune complexes are associated with for potential control through vaccination and
a condition called hyperactive malarious development of novel anti-parasitic drugs.  
splenomegaly (HMS). There is a disturbance
References 
in the ability of T-lymphocytes to control the
humoral response resulting in polyclonal IgM Blum JA, Zellweger MJ, Burri C, Hatz C.
antibodies. Patients suffer from persistent Cardiac involvement in African and
splenomegaly and anemia. In patients with American trypanosomiasis. Lancet Infect
 Plasmodium
 Plasmodium malariae infection, these immune
malariae Dis. 2008;8(10):631 – 441.
1.
complexes may be deposited in the basement Garcia LS, editor. Diagnostic medical
membrane of the glomeruli leading to   parasitology.
 parasitolo gy. 5th ed.
ed . Washington
Washingt on DC:
kidney failure and nephrotic syndrome. This ASM Press; 2006. 
 phenomenon
 phenomenon may also occur
occur in schistosomiasis.  Kasper DL, Braunwald E, Fauci AS, Hauser SL,  
While the s equ est rat ion of l ate Longo DL, Jameson JL, editors. Harrison’s
intraerythrocytic  Plasmodium falciparum
falciparum  principles of internal medicine. 16th ed.
from the circulation and their attachment to  New York: McGraw-Hill;
McGraw -Hill; 2005. 
endothelial cells is protective
this is also believed to be theto t he cause
the
main parasite,
of
MacDonald AS, Araujo MI, Pearce EJ.
Immunology of parasitic helminth
manifestations of cerebral malaria. infections.InfectImmun.2002;70(2):427 –  
33.
 

14  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Maizels RM. Parasite immunomodulation and  Ndam NT, Deloron P. Molecular aspects
 polymorphisms
 polymor phisms of the immune system. J of  Plasmodium falciparum infection 
Biol. 2009;8(7):62.  during pregnancy. J Biomed Biotechnol.
Mandell GL, Bennett JE, Dolin R, editors. 2007;2(5):43785. 
Mandell, Douglas, and Bennett’s principles Rasmussen SB, Reinert LS, Paludan SR. Innate
and practice of infectious diseases. 7th ed. recognition of intracellular pathogens:

Philadelphia,
Elsevier; PA:
2010.   Churchill Livingstone   detection and activation
defense. APMIS. 2009; of the – first
117(5  line of   
6):323-37.
6):323-37.
Moncada DM, Kammanadiminiti SJ, Chadee   Sacks D, Sher A. Evasion of innate immunity  
K. Mucin and toll-like receptors in host  by parasitic
parasit ic protozoa.
protoz oa. Nat Immunol.
Imm unol. 2002;20 02;
defence against intestinal parasites. Trends 3(11):1041 – 7
7..
Parasitol. 2003;19(7):305 – 11.
11.  Takeda K, Akira S. TLR signaling pathways.  
Moreau E, Chauvin A. Immunity against Semin Immunol. 2004;16(1):3 – 9 9..
helminths: interactions with the host Vanhollebeke B, Truc P, Poelvoorde P, Pays
and the intercurrent infections. J Biomed A, Joshi PP, Katti R, et al. Human
Biotechnol. 2010;428593. Trypanosoma evansi infection linked to a
lack of apolipoprotein L-I. N Engl J Med.
2006;355(26): 2752 – 6
6..
 

CHAPTER 1: Introduction to Medical Parasitology   15 

Groups of Parasites with Medical and Public Health Importance

Winifreda U. de Leon, Vicente Y. Belizario, Jr.

ll parasites can be classified according to infective stages called cysts, which are relatively
the Linnaean
of decreasing hierarchical
generality. It startsscheme
generality. in order 
om, 
with Kingdom,
Kingd resistant
to to environmental
the vegetative changes
stages, called compared  
trophozoites.
Subkingdom, Phylum, Class, Order, Family, The parasitic species are capable of multiplying
Genus, and finally, Species. This  hierarchical  within the host and may be transmitted through  
classification is mainly based on morphological
morphological a biological vector within which they can also
characterization
characte rization found in the different stages of multiply (Table
(Tab le 1
1.1).
.1). 
 parasite development.  All protozoa fall under Kingdom Protista,
Currently, however, there are powerful which is a diverse group of eukaryotic
tools based on molecular studies which microorganisms. They have been divided
may provide elucidation of the taxonomic   into several phyla, but the major organisms
relationship of parasites at the subcellular level. causing disease in man belong to Phylum  
Molecular techniques such as DNA extraction
and sequencing, proteome analysis, RNA Table 1.1. Classification of protozoan parasites
interference, and polymerase chain reaction
interference,
are being used to show structural differences 
athmeoidnegn ptiafir acasitieosn. T e atir ce p
of hcer sy p  er oteocziaolalyn p
s p  usaer f ausiltiens
and their sibling
si bling species.Currently, there is a call
for parasitologists to integrate molecular and
morphological approaches in the identification
of parasites. This chapter will not elucidate on  Atrial flagellates Cho
De
l 
i mastx
imesni 
i ntamoebafrags
l 
l i 
il 
l  G iard iaa l mba
li 
these molecular advances, but the reader is Trc
i 
i homonashomn  i s
i Tr ichomonastenax 

enjoined to explore the included references at  

Trc
i 
i homonasvagn  i as i 
l 

the end of the chapter for further details.  

Les
i hman iadonovanL
i es
 ihmana
 i tropc
ia
Protozoa  
Balantidiumcoli
Parasitic infections are either due to the
unicellular protozoan or the multi-cellular Cryptospor idu
i mhom ins i Cyc o
l sporacayetanens s
i
metazoan. Generally, protozoan parasites are Cysto s
iosporabe lil Plasmodiumspp.
Toxoplasmagondii
 provided with
wit h a nucleus or nuclei, cytoplasm,
cytoplas m,
an outer limiting membrane, and cellular Vti aformacorneaTrach p
 i e
l s
i tophorahomn is
i 
elaborations called organelles. Among these Pleis  tophoraspp.

are locomotory apparatus, which include

in clude cilia,  
flagella, and pseudopodia. There is increasing
knowledge about the presence of an apical
complex found to aid the organism in the
 penetration of target cells. 
Many of these protozoa require a wet
environment for feeding, locomotion,
osmoregulation, and reproduction. They form  
 

16  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Sarcomastigophora, Phylum Ciliophora, varying stimuli from the gastrointestinal tract,

Phylum Apicomplexa, and Phylum Microspora.   extrudes, forming a polar tube that, in turn,
Under Phylum Sarcomastigophora are two  penetrates the host cell.
cel l. These parasites
par asites have
subphyla, namely, Subphylum Mastigophora, received more attention recently due to the
whose organelles of locomotion are whip-like increasing number of opportunistic infections
structures arising from the ectoplasm called associated with immunocompromised states,
flagella,
organellesand Subphylumare
of locomotion Sarcodina, whose  
hyaline foot-  particularly AIDS.
Nematodes 
like extrusions from the ectoplasm called
 pseudopodia.
 pseudopo dia. Subphylum
Sub phylum Mastigophora
Mastigo phora   Metazoan parasites are either helminths
includes the atrial flagellates and hemoflagellates, or arthropods which fall under the Kingdom
namely, Giardia , Chilomastix , Trichomonas , Animalia (Table 1.2). Helminths causing  
 Dientamoeba , Trypanosoma , and  Leishmania .
Subphylum Sarcodina includes the amebae,
Table 1.2. Classification of metazoan parasites  
namely,  Entamoeba ,  Endolimax ,  Iodamoeba ,
 Ac an th a mo eb a , and  Naegleria . Phylum
Ciliophora, whose species have organelles of Intestinal  Ascarislumbricoides
Cap a ill  r iaph
 p
 i 
l 
li pinenss
i Enterobu
 isvermc iua l rs
i 
i 
locomotion that are hair-like projections from Hookworm Strongyo  ld
i esstercora ls
i 
i Tr ichur is
the ectoplasm called cilia, which includes only trc
i 
i hu
i ra

one parasite of medical and public health

interest,  Balantidium coli. 
Extraintestinal

l ceom b pelr esxoaf tPtheylaunmter Ai por iceonmd pwlehxica hcaovensainsts
Parasrt ongy u
l scantonens isTr ichn
i ea
l sp iras
i 
l 
a picaM
of polar rings, subpellicular tubules, conoid  

 processes, rhoptries,
rh optries, and micronemes.
micron emes. These
structures are involved in the penetration and
invasion of target cells. All members are parasitic.
Very important groups of parasites fall under
Class Sporozoa, namely, Plasmodia , Babesia ,
Toxoplasma , Cystoisospora , Cryptosporidium ,
and Cyclospora . These organisms have been Heet rophy idsOp isthorchs ife ln
i 
i eusOp sithorch isvv
i ern
 ii 
Paragon mi uswese t rmanS i ch istosomahaemat obu i m
reported practically from all organ systems   Sch s
itosoma japonc  iumSch s itosomamanson i
of both humans and animals, specifically in  
the gastrointestinal tract, genitourinary tract,
central nervous system, respiratory tract,
reticuloendothelial system, blood and blood  
cells, eyes, skin, and even the oral cavity.
Phylum Microspora, which includes 
 Enterocytozoon and Encephalitozoon , consists
of spore-forming parasites of both vertebrates
and invertebrates. Though the phylum contains
more
in thatthan
they100 genera,
possess the members
a unique areapparatus
extrusion similar,
which enables them to insert infective material
into the host cell. The apparatus includes a
highly coiled polar filament,
filament, which,
 which, due to 
 

CHAPTER 1: Introduction to Medical Parasitology   17 

infections in man belong to three groups, Larvae of Trichinella are encysted in the host
namely, annelids, nematodes, and flatworms. muscles. 
Under the annelids, only the leeches are There are various ways by which
considered to be of medical importance. humans acquire these helminths. Ingestion
The nematodes are also known as of embryonated eggs is the mode of infection
roundworms because they are elongated and of  Ascaris , Trichuris , and  Enterobius . Skin

cylindrical in shape,
Generally, they have awith bilateral
complete symmetry.
digestive tract    penetration byhookworms
of infection of filariform larvae is the mode
and Strongyloides ,  
and a muscular pharynx
p harynx that
t hat ischaracteristically
ischaracteristically while the bite of mosquito vectors is the
triradiate. They are provided with separate  mode of transmission of Wuchereria and 
sexes, although some may be parthenogenetic.  Brugia . Ingestion of infective larvae is the
There are sensory organs in the anterior and mode of infection for Capillaria from fish,
 posterior ends of the worm called amphids Trichinella from pork, and Paras trongyluss from
 Parastrongylu
and phasmids, respectively. The latter are very snails. Autoinfection occurs in Capillaria ,
useful in the grouping of the nematodes. Those Strongyloides , and Enterobius . Transmission
roundworms with phasmids are described as through inhalation of embryonated eggs is
 phasmid nematodes, while those without them  possible for Enterobius and Ascaris. 
are described as aphasmid worms. Among
Cestodes 
the nematodes of medical and public health
importance, only three are aphasmid worms The two other groups of worms are
(Adenophorea). These are Trichuris, Trichinella,  tapeworms or cestodes, and flukesor trematodes.  

f or e, phas.mTihdenr em
athnedr eC  cear tnoednetsi a)r .e, 
staotof  dthese (nSem  bmeslo. nMg etm
o  bPelr astyohf elPmlaintytheelsmoir ntthhees,  in
a pill ar ia
flahtewsoe r 
T
The phasmid worms belong to several general, are dorso-ventrally flattened with
orders in the scientific taxonomic classification  bilateral symme
symmetry
try.. The cestodes
cestodes are segmented,
segmented,
of the worms.  Ascaris belongs to
 Ascaris t o Ascaridida,
Ascaridi da, with a ribbon-like appearance, while the
 Parastrong
 Paras ylus and the hookworms to
trongylus trematodes are leaf-like and unsegmented.  
Strongylida, Strongyloides to Rhabditida, Cestodes do not have a digestive tract, while
bius to Oxyurida, and the filarial worms
 Enterobius
 Entero trematodes have an incomplete one. Both
to Spirurida. A more extensive discussion of cestodes and trematodes do not have a
the taxonomic groupings of these worms can circulatory system. 
 be found in other references.   Adult tapeworms are hermaphroditic.
hermaphroditic. They
These nematodes can be grouped on the are found in the intestines of the definitive
 basis of the habitat of the adult worms. Most host, and the larval stage is encysted in the
of these nematodes are found in the small and tissues of the intermediate host. They have an
large intestines, while some are found outside   anterior structure called the scolex, which is
the intestines. the main organ of attachment of the worm to
Those typically found in the small the definitive host. After the scolex is the neck,
intestines are Ascaris, hookworms, Strongyloides, which is then followed by the
t he strobila. The neck
and Capillaria , while those usually located is considered the region of growth, because
in the colon are Trichuris and  Enterobius . segmentation or strobilization srcinates from
Extraintestinal nematodes like Wuchereria and it. Segments or proglottids that are nearest to
 Brugia have been recovered from the lymph the neck are the most immature, followed by
nodes and lymph vessels, whereas Parastr
 Parastrongyl
ongylus
us increasingly mature segments, and the most
has been reported from the eyes and meninges.   distal are gravid segments.
 

18  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

The cestodes are grouped together into various species of Taenia

Taenia produce the cysticercus
different orders, just like the nematodes.   type, while  Hymenolepis ,  Dipylidium , and
However,there are only two orders of tapeworms  Raillietina produce the cysticercoid type. A
with medical and public health significance, third type called the hydatid is produced by
namely, Order Pseudophyllidea and Order  Echinococcus
 Echinococc us spp.
Cyclophyllidea. These two orders differ in terms Infection with adult tapeworms is generally
of the morphology
eggs, as well as in of
thethenumber
nuscolex,
mber ofsegments, and  
intermediate acquired through
intermediate hosts.theThere
consumption
are cases,ofhowever,
infected 
hosts and the type of encysted larvae that where humans are infected with the larval stage
develop in the intermediate hosts.   of Taenia solium
solium, called cysticercosis, and of  
Pseudophyllidean tapeworms have a  Echinococcus spp., called hydatid cyst.  
spatulate scolex with sucking grooves, called Trematodes 
 bothria, while the Cyclophyllidean scolex
is globular with four muscular suckers.   The other group of flatworms is composed
Segments of both orders have genital
gen ital pores of the flukes or trematodes. Adult trematodes
 but Pseudophyll
Pseud ophyllidean
idean segments,
segm ents, in addition,
add ition, are equipped with an oral sucker, and a
have a uterine pore which allows release of eggs ventral sucker called an acetabulum. A third
from the gravid uterus. Since Cyclophyllidean sucker called a genital sucker or gonotyl is
segments do not have the uterine pore, they observed only among the heterophyids. They
undergo the process of apolysis whereby gravid are all hermaphroditic. All trematodes require
segments are detached from the main body   two intermediate hosts in their life cycle.  
oFf or thdeiawgonr omstican pdur e pgogseasr , einevCenytculoa pllhyyr lelildeaesaend. thlel  tinr ef emctaitvoedsetsagheavf oer  o p
A egagtos,deasnd
alle r tchuelsaetetdr em
infections, both eggs and segments are recovered is the encysted larva, the metacercaria, that
from the patients, while in Pseudophyllidean develops in the second intermediate host. These
infections, segments may not be found.   characteristics
characteristics are observed in all medically
 Non-operculated Cyclophyllidean
 Non-operculated Cyclophyllidean eggs
eggs are important trematodes, with the exception of
 passed out readily, containin
co ntainingg the hexacanth
hexacan th the schistosomes in which the infective stage is
embryo. On the other hand, Pseudophyllidean the cercaria. While the first intermediate  host
eggs, which are operculated and immature, is always a snail, the second intermediate host
require aquatic development of the embryo, may be a fish, crustacean, another snail, or fresh
called the coracidium.   water plants. 
Pseudophyllidean worms generally require Trematodes are generally grouped together
two intermediate hosts in their life cycle.    based on their habitat. Adult schistosomes
schistosom es are
In the first intermediate host, eggs encyst found in the mesenteric veins; hence they are
as procercoid larvae, then into plerocercoid  called blood flukes. Adult Parag onimuss worms
 Paragonimu
larvae in the second intermediate host. This are found in the lung parenchyma. There is
group of tapeworms is best represented by a group of flukes
flukes that
 that inhabits the liver and
 Diphyllobothrium , which utilizes humans as  bile passages. This group includes  Fasciola ,
definitive hosts, and Spirometra, which employs  Clonorchis , and Opisthorchis . Another group
humans as an intermediate host.   composed of  Fasciolopsis , Echinostoma , and
Cyclophyllidean worms require only one heterophyids inhabits the intestines. 
intermediate host, but different species of Mature eggs contain an embryo called the
Cyclophyllideans produce different types of miracidium. Eggs passed out by an infected host
encysted larvae in the intermediate hosts. The   may be mature, as in the case of Schistosoma , 
 

CHAPTER 1: Introduction to Medical Parasitology   19 

Clonorchis, Opistorchis, and heterophyids; while References 

immature eggs are associated with Paragonimus,
Beaver PC, Jung RC, Cupp EW. Clinical
 Fasciola, Fasciolopsis , and Echinostoma . The
miracidium of immature eggs develops in an  parasitology.
 parasitolo gy. 9th ed.
ed . Philadelphia:
Philadel phia: Lea &
Febiger; 1984. 
aquatic environment. 
Belding DL. Textbook of parasitology. 3rd
Arthropods  ed. New York: Appleton-Century Crofts; 
Phylum Arthropoda is composed of Borr 1o9r  6D5J. ,  Delong  DM,  Tr   p
iplehor n  CA.  An
 bilaterally symmetrical organisms with introduction to the study of insects. 4th ed.
segmented and jointed appendages. The USA: Holt, Rinehart and Winston; 1976. 
 body is covered with a chitinous
chitin ous exoskeleton.
exoskeleto n. Cavalier-Smith T, Chao EE. Phylogeny
This group includes insects, mites, ticks, and classification of phylum
p hylum Cecozoa 
spiders, scorpions, centipedes, millipedes, and (Protozoa). Protists. 2003;154(3-4):341 –  
crustaceans. Pentastomids or pentastomes may 58.
 be included under this group because they have Crofton HD. Nematodes. London: Hutchinson
the attributes of both arthropods and annelids.  & Co Ltd; 1966.
Arthropods affect human health in
Heinz M. Parasitology in focus: facts and trends.  
various ways, like envenomization through Berlin: Springer-Verlazg; 1988.  
 bites of spiders, flies,
flies, bugs,
 bugs, mites, and ticks.
Jahn FF, Jahn TL. The protozoa. Dubuque, 
Introduction of venom can also occur with
stings of scorpions, ants, wasps, and bees.  
Iowa: Wm. C. Brown Co. Publish
P ublishers;
ers; 1949.
1949.
Levine ND. A newly revised classification of  
enosr uer ceogtnoizaer dthar so pa ohdeaalltlher hgeanzasr dh.asThr eecr eenatly
 bEex p r e the protozoa. J Parasitol. 1980;27:37 – 558.
8.  
arthropods that feed on human blood, like Lydden P, Thompson RC. Parasite zoonosesand  
 biting flies
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shiftingchange: molecular
boundaries. toolsParasitol.
Trends for tracking
 
to become biological vectors to some disease
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91.
agents like Plasmodium, filaria,  trypanosomes,
 Plasmodium
 Babesia , and Leishmania . On the other hand,
Roberts LS, Janovy J. Foundations of
flies and cockroaches, which inhabit unsanitary
 parasitology.
 parasitolo gy. 5th ed. Dubuque, Iowa: Wm. 
C. Brown Publishers; 1996.
environments, can be mechanical vectors of Schmidt GD. The tapeworms. Dubuque, Iowa: 
microbes and parasites.  
Wm. C. Brown Co. Publishers; 1969.
Some arthropods, such as fleas
fleas and
 and lice,
de Leon GP, Nadler SA. What we
w e don’t 
can cause dermatologic manifestations due to recognize can hurt us: a plea for awareness
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human tissues, a condition known as myiasis. 
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e pR  MiolnoigsyP: T
a,mR uo blteidr tisco p na.r M
in lIiD lecr uolaacr h
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y a p
to understanding parasitic zoonoses. Int J
Parasitol. 2005;35(11 – 12):1295
12):1295 – 307.
307. 
 

20  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

CHAPTER 2 

Protozoan Infections 

Intestinal Ame bae
Pilar ita  T.  River a, Windell  L.  River a, Juan  A
Anto nio  A
A.  So lo n 

S  even species of amebae occur in humans.

These include the pathogenic Entamoeba  
histolytica, and the commensals  E. dispar , E. 
 E. 
reaction (PCR) restriction fragment length
 polymorphism (RFLP), and typing with
monoclonal antibodies, these three species are
moshkovskii ,  E. hartmanni ,  E. coli, Endolimax now differentiated.  E. hartmanni , formerly
nana , and Iodamoe ba butschlii . Entamoeba
 Iodamoeba referred to as “small
“small  race”
race”  of E. histolytica, is
 pole cki is an intestinal ameba of pigs and differentiated primarily on the basis of size. 
monkeys that has been occasionally detected
Parasite Biology 
in humans, and is a probable cause of diarrhea.
They are mainly differentiated on the basis of  Entamoeba histolytica is a pseudopod-
structure andsize. Trophozoites divide bybinary   forming non-flagellated protozoan parasite. It  
fission. Most cyst-forming amebae go through is the most invasive of the Entamoeba parasites
 Entamoeba
nuclear division, and then divide again after   (which includes E. dispar , E. moshkovskii , E.
excystation in a new host.  hartmanni , E.
 E. polecki , E.
 E. coli, and E. gingivalis ), 
Entamoeba histolytica 
and the only member of thefamily to cause colitis
and liver abscess. The life cycle of E. histolytica
histolytica
 Entamoeba
 Entamoeba histolyticais currently classified
histolytica consists of two stages: an infective cyst (Plate
within the subphylum Sarcodina, superclass 2.1) and an invasive trophozoite form. NoN o host
Rhizopoda, class Lobosea, order Amoebida, other than humans is implicated in the life cycle, 
family Entamoebidae, and genus  Entam oeba. 
 Entamoeba
The members of this genus are characterized
 by having a vesicular nucleus, a centrally
central ly (or naer
central) located small karyosome, and varying
numbers of chromatin granules adhering to
the nuclear membrane. These nuclear and  
r  emcioer  p
oththe es p longt iacmdoief f bear  enxce ps td E 
s ohf o E  is.tihnigt uoil  yshtica, 
 s

 E. dispar , and  E. moshkovskii (previously

known as the Laredo strain). The three said
species are morphologically identical and of
thehistolytica
 E. same size.species
It was only recently
complex was that this  
resolved. Plate  2.1.  E 
amoebahi 
nt  o
st  c 
t l y  ac yst (Co ur te sy
i t 
Through isoenzyme
isoenzyme analysis polymerase
polymerase chain  of the Department of Parasitology, UP-CPH)  

20 
 

CHAPTER 2: Protozoan Infections   21 

although natural infection of primates has been Infection with E. histolytica occurs when cysts
reported. The quadrinucleate cyst is resistant to are ingested from fecally-contaminated
fecally-contaminated material
gastric acidity and desiccation, and can survive (Figure 2.1). Other modes of transmission
in a moist environment for several weeks.   include venereal transmission through fecal-oral 
 

22  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

contact or direct colonic inoculation through

contaminated enema equipment. Excystation
occurs in the small or large bowel, where a cyst
undergoes nuclear followed by cytoplasmic
division to form eight trophozoites. The  E.
histolytica trophozoites are highly motile and

 possess
size frompseudopodia
pseudopodi
12 to a (Plate
t o 60 µm 2.2). They
in diameter
dia meter (aboutvary
(abou in 
t 20 µm
in average). Microscopic examination of fully-
 passed stool specimens reveals the characteristic 
 progressive and directional movement of
trophozoites, with pseudopodia as locomotory Plate 2.2. Entamoebahistolyticatrophozoite (Fro
(F rom
m
organelles. The hyaline pseudopodium is World Health Organization. Bench Aids for the
formed when the clear, glasslike ectoplasm, Diagnosis of Intestinal Parasites. 
or outer layer is extruded, and the granular Geneva: World Health Organization; 1994)
endoplasm flows
flows into
 into it. Ingested red blood
cells are observed as pale, greenish, refractile
 bodies in the cytoplasm
cytopla sm of the ameba. Cysts are
usually spherical, and the size may vary from 10
to 20 µm. They are characterized by a highly
refractile hyaline cyst wall, one to four nuclei, 
 banar ds.r oTdr -os phha poezdoi(toer s chiagvaer -tshea pa bedil)itcyhr to mcoaltonidizael
and/or invade the large bowel, while cysts are
never found within wit hin invaded tissues.  E. E.histolytica
histolytica
trophozoites multiply by binary fission. They
encyst producing uninucleate cysts, which
then undergo two successive nuclear divisions Plate 2.3. Entamoebahistolyticaquadrinucleate cyst
to form the characteristic quadrinucleate
quadrinucleate cysts (From World Health Organization. Bench Aids for
(Plate 2.3).  the Diagnosis of Intestinal Parasites. Geneva:
 E. histolytica is a eukaryotic organism but
histolytica World Health Organization; 1994) 
has several unusual features, including the lack
of organelles that morphologically resemble lack of glutathione metabolism, the use of
mitochondria. Because nuclear-encoded  pyrophosphate
 pyroph osphate instead of ATP at several steps
mitochondrial genes such as pyridi
 pyridine
ne nucleot
nucleotide
ide in glycolysis, and the inability to synthesize
transhydrogenase and hsp60 are present,  E.
 E.    purine nucleotides de novo. Glucose is actively  
histolytica , at one time may have contained transported into the cytoplasm, where the
mitochondria. There is no rough endoplasmic end products of carbohydrate metabolism are 
reticulum or Golgi apparatus, although cell ethanol, carbon dioxide, and under aerobic
surface and secreted proteins contain signal   conditions, acetate.
sequences, and tunicamycin inhibits protein Pathogenesis and Clinical Manifestations  
glycosylation. Ribosomes form aggregated The proposed mechanisms for virulence
crystalline arrays in the cytoplasm of the
trophozoite. Some differences in biochemical are: production of enzymes or other cytotoxic
 pathways from higher
hig her eukaryotes
eukary otes include
incl ude the   substances, contact-dependent cell killing, 
 

CHAPTER 2: Protozoan Infections   23 

and cytophagocytosis.  In vitro

vitro, amebic killing study involving 206 patients with probable
of target cultivated mammalian cells involve ALA as diagnosed by ultrasound, the two
receptor-mediated adherence of ameba to most frequent manifestations were fever in
target cells, amebic cytolysis of target cells, 77% and RUQ pain in 83%. Pain is either
and amebic phagocytosis of killed or viable localized in or referred to the right shoulder.
target cells. E. histolytica trophozoites adhere
histolytica The liver is tender, especially in acute cases,
to the colonic mucosa through a galactose-  and hepatomegaly
inhibitable adherence lectin (Gal lectin).
l ectin). Then, Chronic disease (>2is weeks
presentduration)
in 50% ofiscases.
found 
the amebae kill mucosal cells by activation of in older patients and it involves wasting with
their caspase-3, leading to their apoptotic death   significant weight loss rather than fever. Only  
engulfment. 30% of ALA cases have concurrent diarrhea.
Recent studies have shown thastusceptibility However, daily stool culture
culturess revealed that 72%
of humans to E. histolyticainfection is associated
histolytica harbored trophozoites even in asymptomatic
with specific
specific alleles
 alleles of the HLA complex.  infections. Mortality in uncomplicated ALA is
Majority of cases present as asymptomatic less than 1%.  
infections with cysts being passed out in   The onset of amebic colitis may be sudden
the stools (cyst carrier state). The recent after an incubation period of 8 to 10 days, or
differentiation of  E. dispar and E. histolytica after a long period of asymptomatic cyst carrier
 by PCR has confirmed
confirmed the  the high prevalence state. ALA may have all acute presentation of
of non-pathogenic E. dispar compared to the less than 2 weeks duration or a chronic one of
 pathogenicc E. histol
 pathogeni ytica. However,studies also  
histolytica more than 2 weeks duration. The recurrence 
r eenvdeam
ledic tchoamt muonstit E   s ica inf ec ons  in
ie.s har iet oal  ysyt m ptomatic. r oaf tAe LwAasif nouMnedxticoo b.e 0.29% in a five-year  study
Amebic colitis clinically presents as gradual  The most serious complication of amebic 
onset of abdominal pain and diarrhea with or colitis is perforation and secondary bacterial
without blood and mucus in the stools. Fever  peritonitis.
 peritoni tis. Colonic perforation occurs in 60%
is not common and it occurs only
o nly in one third   of fulminant colitis cases. 
of patients. Although some patients may only   In ALA, the most serious complications are
have intermittent diarrhea alternating with rupture into the pericardium with a mortality
constipation, children may develop fulminant rate of 70%, rupture into the pleura
p leura with
colitis with severe bloody diarrhea, fever, and mortality of 15 to 30%, and super infection.
abdominal pain. Intraperitoneal rupture, which occurs in 2 to
Ameboma occurs in le ss than 1% of 7.5% of cases, is the second most common
intestinal infections. It clinically presents as complication. However, it is not as serious as
a mass-like lesion with abdominal pain and colonic perforation because ALA is sterile.  
a history of dysentery. It can be mistaken for   Secondary amebic meningoencephalitis  
carcinoma. Asymptomatic ameboma may also occurs in 1 to 2%, and it should be considered
occur.  in cases of amebiasis with abnormal mental
Amebic liver abscess (ALA) is the most status. Renal involvement caused by extension
common extra-intestinal form of amebiasis. of ALA or retroperitoneal
retroperitoneal colonic perforation is 
The cardinal manifestations of ALA are fever rare. Genital involvement is caused by fistulae
and right upper quadrant (RUQ) pain. Several from ALA and colitis or primary infection
studies have shown these two as the most through sexual transmission.  
frequent complaints, particularly in acute  Natural or innate immunity
immunit y to E. histolytica
histolytica 
cases (<2 weeks duration). In a Philippine   in the intestines involves mucin inhibition of  
 

24  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

amebic attachment to the underlying mucosal Acute amebic colitis

coli tis should be differentiated
cells. In the systemic circulation, the mechanism from bacillary dysentery of the following
is that of complement-mediated killing of etiology: Shigella, Salmonella, Campylobacter ,
trophozoites. Acquired immunity primarily Yersinia, and enteroinvasive  Escherichia coli
involves cell-mediated responses, although (Table 2.1). Although stools may be
b e grossly
humoral responses may also contribute to   bloody or heme-positive in both conditions,

anti-amebic
 E. immunity.
tica by:
histolytica
histoly directlActivated
a) directly T-cells killtes
y lysing trophozoites
trophozoi
  fever
are less
significantly elevated leukocyte count 
andcommon in amebic colitis. Another
in a contact-dependent process; b) producing differential is inflammatory bowel disease.
cytokines which activate macrophages
macrophages and other   Amebic colitis should be ruled out before  
effector cells (neutrophils and eosinophils); and  steroid therapy for inflammatory bowel disease
c) providing helper effect for B-cell antibody is started because of the risk of developing toxic
 production. In vitro studies using activated megacolon. 
murine and human T-cells demonstrated The differential diagnoses of ALA include
significant killing of trophozoites in a contact-  pyogenicc liver abscess, tuberculosis
 pyogeni tuberculosis of the liver,
liver,
dependent and antibody independent manner. and hepatic carcinoma. On the other hand,
Cytokine studies revealed that interferon (IFN) genital amebiasis should be differentiated
and interleukin (IL-2) may have a role in from carcinoma, tuberculosis, chancroid, and
activating macrophages
macrophages for amebicidal activity. lymphogranuloma venereum. 
More recent studies demonstrated that
t hat activated
macrophages produce nitric oxide (NO) which   Table 2.1. Comparison of bacillary and amebic
dysentery 
w
(Ta N et)hwalatsosthr o ph
s lF s. uTulam
wnotzositeim r  nOec pr r osdisuf acctitonr .
teo N
Bacillary Dysentery Amebic Dysentery
Although it is known that antibodies are
 produced against amebic antigens, there has
 been no direct evidence of T-cell help for  
B-cells. Studies have revealed that the principal
antibody-dependent cell cytotoxicity (ADCC)
did not work against amebae. Antibodies which
were detected by seroepidemiologic studies and
secretory IgA isolated in the gut may merely
m erely
 be an indicator of current or
or recent invasive
amebiasis.
Amebic modulation of host immune
responses exists. For instance, infected human
subjects and animals have been shown to be in 
a state of immunosuppression during the acute
stage of amebiasis. This state, characterized
 by T-cell hyporesponsiveness, suppressed
 proliferationn and cytokine
 proliferatio cytokine production,
production, depressed
depressed 
delayed-type hypersensitivity (DTH), and
macrophage suppression, is favorable for amebic
macrophage
survival. It is the reversal of these modulatory
effects, which is the key in controlling amebiasis. 
 

CHAPTER 2: Protozoan Infections   25 

Diagnosis  following morphologic structures are noted:

size of the cyst, number of nuclei, location and
The standard method of parasitologic
appearanceofthekaryosome,the characteristic
characteristic
diagnosis is microscopic detection of the
appearance of chromatoid bodies, and presence
trophozoites and cysts in stool specimens.
of cytoplasmic structures such as glycogen
Ideally, a minimum of three stool specimens vacuole.  E. histolyticacan, thus, be differentiated
E. histolytica differentiated
collected on different days should be examined.  
Fs  ppoer cidmeetencstisohnouolf dt br o ph oiitnese,df rr we  sithhisnto3o0l from
colithe
, E.non-pathogenic species,
bütschlii. Stool,  
 E. hart
hartman
manni
ni  
e exoazm  E. nana, and Iodameba
minutes from defecation. Using the direct fecal culture using Robinson’s and Inoki medium is
smear (DFS) with saline solution alone, the
more sensitive than stool microscopy
microscopy,, but is not
routinely available. 
microscopist can
can observe trophozoite
trophozoite motility.  Differentiation between  E. histolytica and 
histolytica
Unidirectional movement is characteristic  
 E. dispar is not possible by microscopy. This
of E. histolytica. Using saline and methylene
can only be done by PCR, enzyme-linked
 blue, Entamoeba species will stain blue, thus,
differentiating them from white blood cells.
immunosorbent
immunosorbent assay (ELISA), and isoenzyme
analysis. The last is primarily a research
Using saline and iodine, the nucleus and
karyosome can be observed to differentiate E. technique. On the other hand, an ELISA-based
assay for stool is now commercially available
histolytica from the non-pathogenic amebae
and studies have demonstrated a sensitivity of
( E. hartmanni ,  E. coli ,  Endolimax nana ).
80% and specificity
specificity of
 of 99%. The use of PCR
The detection of  E. histolytica trophozoites
with ingested red blood cells is diagnostic of  
is limited by the requirement of sophisticated 
amebiasis. Charcot-Leyden
Charcot-Leyden crystals (Plate 2.4) esaqm ese)nlto.oAkedPhiinl p
uiplm ito pitnhe  sr teulida by il(inty=4o9f 7stsotool  l
can also be seen in the stool.  
ELISA with PCR as gold standard (Plate 2.5).
Sensitivity and specificity were 91% and 97%,
respectively. 
Detection of antibodies in the serum is
still the key in the diagnosis of ALA.
ALA . It must
 be noted that
t hat in ALA,
AL A, microscopic
microsco pic detection
detecti on
cannot be done because aspiration is an invasive
 procedure, and trophozoites
trophozoites are missed
missed because
because
they are located in the periphery of the abscess. 

Plate 2.4. Charcot-Leyden crystal observed

in stool specimen of a patient suffering from
amebiasis (Courtesy of the Department of
Parasitology, UP-CPH) 

Concentration
Ether/Ethyl methods
Acetate such as Formalin
Concentration Test
Plate 2.5. Agarose gel showing the 100bp PCR
(FECT) and Merthiolate Iodine Formalin products of Entamoebahistolytica-posititv
ve
ie s
sttool
Concentration
Concentr ation Test(MIFC)
(MIF C) are more sensitive specimens (lanes 2-15) 
than the DFS for detection of cysts. The (Courtesy of Dr. Windell Rivera)
 

26  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

To date, serological tests for amebic disease Treatment and Prognosis 

include indirect hemagglutination (IHAT),
The treatment of amebiasis has two
counter immunoelectrophoresis (CIE), agar gel
diffusion (AGD), indirect fluorescent antibody objectives: a) to cure invasive disease at both
intestinal and extraintestinal sites; and b) to
test (IFAT),
(IFAT), and ELISA. The IHAT
IHA T can detect
antibodies of a past infection even as long as 10 eliminate the passage of cysts from the intestinal
lumen. Metronidazole is the drug of choice  
years ago.AGD,
In contrast,
CIthe antibodies
of shortdetected
duration,by
 
f 5o-r  r eiadtamzoelnet doef r iivnavtaivsievsesaum
ELISA, and CIE E are nitthr eoitm che baisastins.idOatzhoeler
lasting for a few months. Antibodies have
 been demonstrated in asymptomatic
asympto matic intestinal   and secnidazole are also effective. Diloxanide
infections so that serology can be used in the
furoate is the drug of choice for asymptomatic
cyst passers. It is also given after a course of
monitoring of a cyst carrier.  
metronidazole for invasive amebiasis. 
Ultrasound, computerized tomography
(CT scan), and magnetic resonance imaging Percutaneous drainage of liver abscess is
indicated for patients who do not respond
(MRI) are non-invasive and sensitive methods
to metronidazole and who need prompt
in early detection of ALA. Ultrasound (Plate
2.6) typically shows a round or oval hypoechoic symptomatic relief of severe pain. It is also done
area with wall echoes. In 80% of cases, this
for those who have left lobe abscess that may
finding is
finding  is seen in the right lobe of the liver.
rupture into the pericardium, large abscesses in
Multiple lesions occur in 50% of acute cases, danger of rupture, and multiple abscesses with
a probable associated pyogenic etiology.  
and aspiration may be required to differentiate 
amete bhoicdf sr (oIm AyToganendicIFa b
H p sc)eas s. gUoslidnsgtasenr doalr 
AT odg,icaal Epidemiology 

Philippine study has shown that the sensitivity For a long time, the species-complex
and specificity of ultrasound were 95% and referred to as  E. histolytica was believed to
40%, respectively. However, as the results of infect 500 million people, or 10% of the
the study still revealed some limitations in the world’s population. However, with the recent
use of ultrasound in the diagnosis of ALA, redescription into three different species: the
additional diagnostic ultrasound findings have  pathogen ic E. histol
 pathogenic histolytica, and the commensals,
ytica commensals ,  E.
E.
dispar and E. moshko vskiii, the true prevalence of
moshkovski
yet to be identified.  
amebiasis is approximately 1 to 5% worldwide.
There are 50 million  E. histolytica infection
cases, and 40,000 to 100,000 deaths due to
amebiasis in the world per year. Thus, amebiasis
is the third most important parasitic disease,
after malaria and schistosomiasis, and second  
asailtaicr  p
toar m
 p ia r aosttohzeoatno ps. cause of  mor tality among
Humans are the major reservoirs of
infection with E. histolytica
histolytica. Ingestion of food
and drink contaminated with  E. histolytica
histolytica  

cysts from human

oral contact are thefeces, and direct
most common fecal-of
means
Plate 2.6. Ultrasound showing a solitary infection. Amebic infection is prevalent in the
hypoechoic mass at the right lobe of the liver Indian subcontinent, Africa, East Asia, and
suggesting ALA (Courtesy of Dr. Pilarita Rivera) South and Central America. In developing  
 

CHAPTER 2: Protozoan Infections   27 

countries, prevalence depends on the level of cases should be done. Food handlers should be
sanitation, crowding, socio-economic status, screened for cyst carriage, and asymptomatic
cultural habits, and age. In developed countries, cyst carriers should be treated. 
infection is usually caused by  E. dispar , and Vaccines can be a cost-effective and
is prevalent in certain groups: immigrants,  potent strategy for amebiasis prevention
travelers from endemic countries, homosexual and eradication. Unlike in other protozoan

malesinstitutionalized
and (men having sex with men), HIV patients, 
people. infections, amebic
fewer problems. Thevaccine development
ameba life has  
cycle is simple,
A microscopic study of diarrheic stools in   and no intermediate hosts are involved. Amebae
Australia (n=5,921) revealed 177 (3%) positive are extracellularly located, and do not undergo
un dergo 
samples. PCR detected 5 E. histolytica, 63 E. antigenic variation. All these characteristics are
dispar , and 55 E. moshkovskii
moshkovs kii infections. The supportive of an achievable amebic vaccine. 
latter two species, which are both commensals, Studies have also demonstrated the
are 10 times more prevalent than E. histol
histolytica.
ytica. acquisition of protective immunity to amebae,
A stool survey done in Iran (n=16,592) showed  particul arly that of mucosal immune response.
 particularly
226 positive samples. Only 101 isolates were Trials with recombinant amebic antigens as
successfully cultured in Robinson’s  medium. vaccines have proven to be more advantageous
Of these isolates, 93 (92.1%) were E. dispar , than inactivated/attenuated amebae. The
and only 8 (7.9%) were E. histolytica or mixed candidate vaccine molecules which have been
infections by PCR- RFLP. most intensely studied are the serine-rich  E.
A field study in Northern Philippines   histolytica  protein (SREHP), the adherence 

(1n8=(10,.89762%)  )s E 
ho. w
 s
13ti7ca( b7.y3P%C)R 
hiedt ol  y
 E . d i par ,  a d
 s
. A study in  a lceycstienin(eG-r aicl/hGamlNe bAic laenctinge),n.anHdow
  N theve2r 9, m
kD
osat
mental institution (n=113) showed E. histolytica histolytica of these studies have utilized animal models
or E. dispar in 43 subjects (38.1%), while PCR and artificial infection during challenge.  
detected 74 (65.5%)  E. histolytica
h istolytica -positive Testing these candidate vaccines in humans
samples, and 6 (5.3%) E. dispar / E.
 E. histolytica and developing them as food-based vaccines
mixed samples. will be in the forefront of future directions of
amebiasis control. 
Prevention and Control 
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WevACJr l.inR eLca b
entSacdi.v1a9n9c6es;3in3(a1m):e1 b7 – 
ias2i3s . Cr it Star kenDteJr , iFc p
otr eodtaor zoR a,  ivnanHH l SoJs.itPivr evanlednH
IVa- p ceIoVf -
Ravdin JI. Amebiasis: series on tropical   negative men who have sex with men from
medicine: science and practice. London: Sydney, Australia. Am J Trop Med
M ed Hyg.
Imperial College Press; 2000. p. 65 – 159.
159.  2007;76:549 – 5 52.
2. 
Rivera PT, Rivera WL, Escueta AS, Villacorte Van Hal SJ, Stark DJ, Fotedar R, Marriott
EA, Limlingan ET, Lazaro CM, et al. D, Ellis JT, Harkness JL. Amoebiasis:
Prevalence of serologically positive amebic current status in Australia. Med J Aust.
liver abscess cases in the Philippines. Acta 2007;186(8):412 – 6 6..
Med Philipp. 2007;41(2):31 – 6.
6 .  Walshh JA, Ravdin JI. Prevalence of Entam
Wals  Entamoeba
oeba
Rivera WL, Kanbara H. Detection of histolytica infection. Amebiasis . Human
 Entamoeba dispar DNA in macaque feces Infection by Entamoeba histolytica
histolytic a. New
 by polymerase
polymerase chain reaction.
reaction. Parasitol
Parasitol Res. York:: Wiley; 1988. p. 93 – 105.
York 105.
1999;85:493 – 5.
5. World Health Organization.  Entamoeba
Rivera WL, Tachibana H, Kanbara H. Field taxonomy. Bull World Health Organ.
Study on the distribution of  Entameba  1997;75:291 – 22..
 

CHAPTER 2: Protozoan Infections   29 

Commensal Amebae  
Pilarita T. Rivera, Vicente Y. Belizario, Jr., Juan Antonio A. Solon

he presence of commensal amebae in the   (Figure 2.2). These amebae are non-invasive
non -invasive
stools significant two  and do not cause disease.  
reasons: (a)oftheanamebae
individual
mayisbe mistaken for
for the Reproduction is by binary fission
fission of
 of the
T 
 pathogenic Entamoeba histolytica; and (b) it is
an indication of fecal contamination of food
trophozoites. Encystation occurs as amebae pass
trophozoites.
through the lower colon where colonic contents
or water. Accurate identification of  commensal
 commensal  are more dehydrated.  
amebae is therefore crucial.  
Entamoeba dispar  
Parasite Biology 
Entamoebamoshkovskii  
Commensal amebae must be differentiated  Entamoeba dispar is morphologically
from pathogenic  E. histolytica to avoid similar to  E. histolytica , but their DNA and
unnecessary treatment of patients infected ribosomal RNA are different. The former’s
with non-pathogenic species. The three genera isoenzyme pattern is different from that of E.
of intestinal amebae can be differentiated histolytica . 
through the morphological features of their  Entamoeba
 Entamoeba m
moshkovskii isolates, although
oshkovskii
nuclei. The genus Entamoeba has a spherical  first detected in sewage, have been reported  
first detected
linuecle
n s iw
d uw thithchar odm anedm br 
isatitninctgnr aunculelaer s  m a sam
neall in some areas, such as North America, Italy,
I taly,
karyosome found near the center of the nucleus. South Africa, Bangladesh, India, Iran, and
Trophozoitesusually haveonly
haveo nly one nucleus. The Australia. It is a non-patho genic speci es  
that is morphologically indistinguishable
genus Endolimax has a vesicular nucleus with
from  E. histolytica and E. dispar , but differs
a relatively large, irregularly-shaped karyosome
karyosome from them biochemically and genetically. E.
anchored to the nucleus by achromatic fibrils.
moshkovskii is also physiologically unique — it it
The genus Iodamoebais characterized
 Iodamoeba characterized by a large,  being osmotolerant, able to grow at room
chromatin-rich karyosome surrounded by a temperature (25-30°C optimum), able to
layer of achromatic globules and anchored to survive at temperatures
temp eratures ranging from 0 to 41°C.
41°C .
the nuclear membrane by achromatic fibrils.  It has limited pathogenicity in experimental
All species have the following stages: trials in animals, but is non-pathogenic to
trophozoite, precyst, cyst, and metacystic humans. All human isolates have been found
trophozoite; with the exception of Entamoeba to belong to one group “ribodeme
“ribodeme  2.” 
alis, which has no cyst stage, and does not
 gingivalis
 gingiv
inhabit the intestines. Humans are infected by Entamoebahartmanni  
commensal intestinal amebae through ingestion The appearance of  E. hartmanni
hartmanniis relatively
of viable cysts in food or water. Cysts pass similar to that of E. histolytica apart from its
through the acidic stomach and remain viable smaller size. Trophozoites
Trophozoites of the former
former measure
 because of protective
pr otective cyst
c yst walls.
wall s. Excystation
Excystati on
occurs in the alkaline environment of the from 3 to 12
histolytica µm in diameter
measuring (compared
12-60 µm). to E.
Mature cysts
lower small intestines. Metacystic trophozoites measure 4 to 10 µm, are quadrinucleated like 
colonize the large intestines and live on the histolytica, and have rod-shaped chromatoid
 E. histolytica
mucus coat covering the intestinal mucosa   material with rounded or squared ends. Unlike  
 

30  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

elt lisc.a,  E 
 E l.ohoidt ocl  y
 b  s tmanni does not ingest r ed 
E . har tm  bor y tghr aenf uollaor weindgo p r esw: 1it)ha bmacotr er ivacaunodlated
f ealatsum
debris, but no red blood cells; 2) a narrower,
Entamoebacoli  
less-differentiated
less-differentiated ectoplasm; 3) broader and
 Entamoeba coli
c oli is cosmopolitan in  blunter pseudopodia used more for feeding

distribution,
than and isamebae.
other human considerably more common
Trophozoites of E. than locomotion;
movements; and 5)4)thicker,
more sluggish,
irregularundirected
peripheral
coli measure 15 to 50 µm in diameter. It can chromatin with a large, eccentric karyosome in
 be differentiated
different iated from E. histolytica trophozoite 
histolytica the nucleus (Plate 2.7). 
 

CHAPTER 2: Protozoan Infections   31 

 Entamoeba
 Entam oeba cha
chattoni, which is found in apes
ttoni
and monkeys, is morphologically identical to 
polecki. More recently, it has been detected
 E. polecki
in eight human infections. Identification of E.
chattoni was done via isoenzyme analysis. 
Entamoeba gingivalis 
gingivalis 

gingivalis can be found in

 Entamoeba gingivalis
the mouth. The trophozoite measures 10 to
20 µm. It moves quickly, and has numerous
 blunt pseudopodia.
pseudop odia. Food vacuoles that contain  
cellular debris (mostly leukocytes, which is
characteristic
character istic of this species) and bacteria are
numerous. E. gingiva lis lives on the surface of
gingivalis
Plate  2.7.  E  oli i tr o pho zo ite  (Co ur te sy
amoebac 
nt  gum and teeth, in gum pockets, and sometimes
of Department of Parasitology, UP-CPH)
in the tonsillar crypts. They are abundant in
cases of oral disease. This species has no cyst
An E. coli cyst may be differentiated from   stage. Transmission is most probably direct:
 E. histolytica by: 1) its larger size (10 to 35 µm through kissing, droplet spray, or by sharing
sh aring
in diameter), 2) more nuclei (eight versus four utensils. 
in E. histolytica ), 3) more granular cytoplasm,
and 4) splinter-like chromatoidal bodies. Iodine Endolimax nana 
nana 

staining reveals dark-staining, perinuclear  Endolimax nana occurs with the same
masses, which are actually glycogen. Its location, frequency as  Entamoeba coli
co li . Trophozoites
surrounding the nucleus, is more characteristic are small, with a diameter of 5 to 12 µm, and
of E. coli compared to E. histolytica.  exhibit sluggish movement. They have blunt,
Entamoeba polecki   hyaline pseudopodia, and the nucleus has a
large, irregular karyosome. Foodvacuoles found
Entamoebachattoni  
in the cytoplasm may contain bacteria. Cysts
polec ki is a parasite found in
 Entamoeba polecki measure about the same size as trophozoites,
the intestines of pigs and monkeys. Rarely,
R arely, it and are quadrinucleated when mature.  
can infect humans, though a high prevalence Iodamoeba bütschlii  
(19%) was reported in some parts of Papua
 New Guinea (n=184 children).
childr en). In these areas, The trophozoite averages 9 to 14 µm
 both pig-to-human and human-to-human in diameter (ranging from 4-20 µm). It is  
transmission may exist. Like E. coli, motility identified by its characteristic
characteristic large, vesicular  
of trophozoites of  E. polecki is sluggish. A nucleus with a large, central karyosome,
small karyosome is centrally located in the surrounded by achromatic granules. There
nucleus.  E.
E. polecki can be distinguished from E. are no peripheral chromatin granules on the
histolytica in that the former’s cyst is consistently nuclear membrane. The cyst is about 9 to 10  
uninucleated, and chromatoidal bars are µm in diameter (ranging from 6-16 µm), is
frequently angular or pointed. In stained fecal uninucleated, and has a large glycogen body
smears, the nuclear membrane and karyosome which stains dark brown with iodine (Plate 2.8). 
are very prominent.
 

32  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

1998. A study on intestinal parasitic infections

among food service workers in a tertiary
hospital in Manila revealed that 20.3% were
infected with Endolimax nana and 13.6% with
 Entamoeba
 Entam coli. Another study of food handlers
oeba coli
in selected school canteens in Manila showed
infection rates of 22.8% for Endolimax nana, 
17.9% for Entamoeba coli, and 0.8% each for  
 Entamoeba
 Entam oeba hartm anniand  Iodamo
hartmanni  Iodamoeba
eba bütschlii. 
bütschlii
Prevention and Control 

Contraction of the organism may be

 prevented through
throug h proper disposal
d isposal of human
Plate 2.8. Iodamoebabütschli cyst (Courtesy waste and good personal hygiene.
of the D epartment of Parasitology,
Parasitology, UP-CPH) 
References 

Diagnosis  Ali IK, Clark CG, Petri WA. Molecular

Diagnosis is done through stool
Epidemiology of Amebiasis. Infect Genet
Evol. 2008;8(5):698 – 707.
707.
examination. Formalin ether/ethyl acetate
concentration technique (FECT) and and iodine  Antonio R. Conservative management of two
cases of hepato-pulmonary
hepato-pulmonary amebiasis. Bull 
stain are useful to differentiate the species. For  
 E. gin
gingivaliss, a swab between the gums and teeth  
givali Quezon Inst. 1954;2:263 – 74. 
Avila MS, Gar cia MR ,  Nar celle s MV,  Serr a
is examined for trophozoites. Cysts arerecovered
arerecovered
from formed stools, while trophozoites are FB, TejidaandGM.
helminth Prevalence
protozoan of intestinal
infections among
recovered from watery or semi-formed stools.
Trophozoites are best demonstrated by direct foodhandlers in selected school canteens
canteens
fecal smear. In recovering cysts, the use of
in Manila [undergraduate special study].
concentration techniques like FECT and zinc 2003. Located at: College of Public Health
Library, University of the Philippines
sulfate flotation is useful.  
Manila. 
Treatment  Beaver PC, Jung RC, Cupp EW. Clinical
 parasitology.
 parasitolo gy. 9th ed.
ed . Philadelphia:
Philadel phia: Lea &
 No treatment
treatmen t is necessary
necessar y because these
t hese Febiger; 1984. 
amebae do not cause disease.  
Belding DL. Textbook of parasitology, 3rd
Epidemiology  ed. New York: Appleton-Century Crofts;
1965. 
In single stool examinations of over
Clark CA, Diamond LS. Pathogenicity,
30,000 Filipinos, the prevalence of  Entam
 Entamoeba
oeba
virulence and  Entamoeba histolytica .
coli was about 21%,  Endolimax nana , about
Parasitol Today. 1994;11(2):46 – 77..
9%, and  Iodamoeba bütschlii
bütsc hlii , 1%. Intestinal
Cross JH, Basaca-Sevilla V. Biomedical
Biomedical surveys
 protozoan cysts were observed in 13.5% of
in the Philippines. Manila (Philippines): 
overseas Filipinoofworkers
the Department (OFWs)UP
Parasitology, screened
Manilabyin   U.S. Naval Medical Research Unit No.
2; 1984. 
 

CHAPTER 2: Protozoan Infections   33 

Diamond LS, Clark CG. A redescription of  Neva FA, Brown HW

HW. Basic ClinicalPa
ClinicalParasi
rasitolo
tology.
gy.
histolytic a Schaudinn, 1903
 Entamoeba histolytica 6th ed. Connecticut: Appleton & Lange;
(Emended Walker, 1911) separating it 1994. 
from Entamoeba dispar Brumpt, 1925. J Phillips SC, Mildvan MD, William DC, Gelb
Eukaryot Microbiol. 1993;40(3):340 – 4.
4.  AM, White MC. Sexual transmission
Esparar DG, Belizario VY, Relos JR. Prevalence of enteric protozoa and helminths in a

of aparasitic infectionofamong food-handlers J venereal disease clinic population.

6.. N Engl
   
in dietary service a tertiary hospital in Med. 1981; 305(11):603  – 6
Manila. Phil J Microbiol Infect Dis. 2004; Roberts LS, Janovy J. Foundations of  
33(3):99 – 103.
103.   parasitology. 5th ed. Dubuque: Wm. C.
Imperato PJ. A historical overview of amebiasis. Brown Publishers; 1996.
Bull N Y Acad Med. 1981;57(3):175-87.  Salazar NP, Pasay CJ, Avenido AO, Macapasir
John DT, Petri WA.
WA. Markell and Voge’s medical SR, Lena MJ, Maguinsay VM, et al.
 parasitology.
 parasitolo gy. 9th ed. St. Louis: Elsevier Detection of Entamoeba histolytica
histolytica in
Saunders; 2006. p. 36 – 48.
48.  routine stool examination. Phil J Microbiol
Mahmoud AA. Tropical and geographical Infect Dis. 1990;19(2):57 – 60.
60.
medicine companion handbook. 2nd ed. Van Hal SJ, Stark DJ, Fotedar R, Marriott
Singapore: McGraw-Hill Book Co.; 1993.   D, Ellis JT, Harkness JL. Amoebiasis:
Martinez-Palomo A, Espinosa-Castellano M. current status in Australia. Med J Aust.
Amoebiasis: new understanding and new 2007;186(8):412 – 6 6..
goals. Parasitol Today. 1998;14(1):1 – 4.
4.  World Health Organization. Amebiasis. Wkly
Epidemiol Rec. 1997;72(14):97 – 100.
100. 
 

34  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Free-living Pathogenic Amebae 

Edsel Maurice T. Salvana

 Acanthamo
 Acant eba spp. 
hamoeba

Parasite Biology 

canthamoeba is a ubiquitous, free-living

ameba that is the etiologic agent of
 Ac
 Acan
antha
thamoebakeratitis (AK) and granulomatous
moeba
amebic encephalitis (GAE). Acanthamoeba is
characterized by an active trophozoite stage
with characteristic prominent “thorn-
“thorn -like”
appendages (acanthopodia); and a highly
resilient cyst stage into which it transforms when
environmental conditions are not favorable.  
It is an aquatic organism that is found in a
myriad of natural and artifi cial environments,
and can survive even in contact lens cleaning
solutions. Motile trophozoites feed on gram-  Plate 2.9. Acanthamoebatrophozoite exhibiting 
negative bacteria, blue-green algae, or yeasts and characteristic
characteri stic acanthopodia (Accessed from
www.dpd.cdc.gov/dpdx) 
reproduce by binary fission, but can also adapt
to feedthrough
tissue on corneal epithelial cells
phagocytosis andand neurologic
secretion of
  The presence of naturally-occurring
lytic enzymes.   bacterial endosymbionts in  Acanthamoeba
Morphologically,  A c a n t ha mo e b a spp. has been reported. Although the presence
trophozoites exhibit a characteristic single of bacterial symbionts is widespread among
large nucleus with a centrally-located, densely small, free-living amebae, the significance  
staining nucleolus; a large endosome; finely of this association is not known. Recently,
granulated cytoplasm; and a large contractile  Acanthamoeba spp. have been implicated as
vacuole. Small, spiny filaments for locomotion  possible reservoir hosts for
for medically
medically important
known as acanthapodia are evident on phase-  bacteria such as Legion ella spp., mycobacteria
 Legionella my cobacteria,,
contrast microscopy (Plate 2.9).   and gram-negative bacilli such as E. coli . 
 Ac
 Acan
antha
thamoebahas only two stages, cysts and  
moeba Pathogenesis and Clinical Manifestations  

ter xoi p oiater st,oinf  tihtselliif f e cyclele. N
sths oazs p . Tohfle atgr oel plahtoezdositaege
s  A.  Acanthamoeba Keratitis 
Keratitis 

replicate by mitosis (nuclear membrane does  Acanthamoeba was first described as an

not remain intact). The trophozoites are   opportunistic ocular surface pathogen causing
the infective stage, although both cysts and keratitis in 1974. AK is associated with the
trophozoites
various means. gainEntry
entrycan
intooccur
the body through
through the use of improperly disinfected soft contact
lenses, particularly those which are rinsed with
eye, the nasal passages to the lower
lo wer respiratory tap water or contaminated lens solution. An
tract, or ulcerated or broken skin (Figure 2.3).  immunocompromised state contributes to  
 

CHAPTER 2: Protozoan Infections   35 

increased susceptibility
susceptibility to infection, and may fluorescence microscopy. GAE usually occurs
lead to disseminated disease in the lungs and in immunocompromised hosts including  
 brain (GAE).   the chronically ill and debilitated, and
Symptoms of AK include severe ocular those on immunosuppressive agents such as  
 pain and blurring
blurrin g of vision. Corneal ulceration chemotherapy and anti-rejection medications.
with progressive corneal infiltration may occur. The acquired immune deficiency syndrome
Primary amebic infection or secondary bacterial (AIDS) epidemic in the 1980’s dramatically
infection may lead to hypopyon formation.   increased the numbers of person with GAE,  
Progression of infection may cause scleritis and  but these numbers have since fallen with the
iritis, and may ultimately lead to vision loss.  advent of highly effective antiretroviral therapy. 
Major differentials which need to be ruled out Signs and symptoms of GAE
GA E are generally
include fungal and herpetic keratitis.   related to destruction of brain tissue and the
associated meningeal irritation. Systemic
B. Granulomatous Amebic Encephalitis 
Encephalitis 
manifestations early in the course include fever,
 Acanthamoe
 Acanth ba was documented as the
amoeba malaise, and anorexia. Neurologic symptoms
causative agent of human GAE by Stamm in may include increased sleeping time, severe
1972. Amebae were demonstrated in brain headache, mental status changes, epilepsy, and
sections of a GAE patient using indirect coma. Neurologic findings depending on the  
 

36  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

location of the lesions include hemiparesis, Diagnosis of GAE is usually made post-
 blurring of vision, diplopia, cranial nerve mortem in most cases. The rarity of the
deficits, ataxia, and increased intracranial disease and unfamiliarity of most physicians
 pressure.  with the pathogen contribute to frequently
Entry of  Acanthamoeba into the central missed diagnosis. Signs and symptoms of
nervous system is still incompletely understood.  disease are usually attributed to more common
From a primary site of infection in the   differentials.
cerebrospinalMoreover,
Moreover , recovery ofrare,
amebaandfrom
 
skin or lungs, the likely route of invasion is fluid is exceedingly
hematogenous. Direct infection through the imaging results are generally nonspecific.
nonspecific.  
olfactory valves has also been proposed, but   Immunocompromised patients such such 
not conclusively demonstrated. Recent reviews as those with AIDS are at the highest risk
have focused on blood-borne invasion, with for acquiring GAE. While opportunistic
a combination of host factors, elucidation of infections of the central nervous system such
serine proteases, and parasite adhesion using as Cryptococcus meningitis and toxoplasmosis
a mannose-binding protein all contributing to are much more common than GAE, the lack of
 brain endothelial
endotheli al cell damage and subsequent
subsequen t response despite appropriate treatment should
 breakdown of
of the
the blood-brain barrier.   prompt a more thorough evaluation for more
Gross examination of neural tissue post- esoteric organisms. 
mortem reveals cerebral hemispheres that are Specific diagnosis depends on demonstrating
edematous and soft, with areas of hemorrhage the trophozoites or cysts in tissues using
and focal abscesses. The most affected areas  histopathologic stains and microscopy. The  
e  bur sa, inanadr eththe e b pr aoisntestr eiomr . f oInssathsetr uaf cf teucr tesd,
othf atlham or r gea bnr iosm
ce  psincalnflr 
s p  boencsutr latuter dedinf or the
delayn bdecadnem
uair 
areas, the leptomeninges are opaque and exhibit  
 purulent exudates and vascular congestion.  further studies.
Treatment 
The incubation period from initial
inoculation is approximately 10 days, with a Medical treatment of AK has been met
subacute and chronic clinical course of infection with increasing success in recent years. While
that lasts for several weeks to several months. historically, only surgical excision of the infected
The clinical manifestations of disease include cornea with subsequent corneal transplantation
decreased sensorium, altered mental status, was curative, early recognition of AK coupled
meningitis, and neurologic deficits. The natural with aggressive combination anti-amebic
course of the disease eventually results in coma agents can preclude the need for extensive
and death.  surgery. D’Aversa and his colleagues have
Diagnosis 
achieved acceptable results with clotrimazole
combined with pentamidine, isethionate,  
 Acanthamoeba keratitis is diagnosed by and neosporin. Other agents that have been
epithelial biopsy or corneal scrapings for used include polyhexamethylene biguanide,
recoverable ameba with characteristic staining  propamidine, dibromopropamidine
 propamidine, dibromopropamidine isethionate,
isethionate,
 patterns on histologic analysis. Amebae have neomycin, paromomycin, polymyxin B,
also been isolated from the contact lens and lens ketoconazole, miconazole, and itraconazole.
solution of patients. Species-specific identification Topical corticosteroids should be avoided, as
can be made from culture and molecularanalysis
molecularan alysis this retards the immune response. Advanced
through PCR. Known species that have caused AK usually requires debridement, but complete
AK include  A. castellani , A. culbert soni ,  A.
cu lbertsoni excision of the cornea can be avoided if the
hutchetti , A. polyphaga, and A. rhysoides.  infection is confined to more superficial areas. 
 

CHAPTER 2: Protozoan Infections   37 

Deep lamellar keratectomy is the procedure of of the risk of infection, and physicians treating
choice.  these patients should maintain a high index
Clinically apparent neurologic disease in of suspicion in the presence of compatible
GAE usually heralds a fatal outcome within signs and symptoms of infection which do not
3 to 40 days. A few patients have shown good respond to conventional
conventional antimicrobial
antimicrobial therapy. 
responses to combinations of amphotericin
References 
B, pentamidine isethionate, sulfadiazine, 
flucytosine, fluconazole or itraconazole.   D’Aversa G, Stern GA, Driebe
Drie be WTJr.
WTJr. Diagnosis
One liver transplant patient survived after and successful medical treatment of
decompressive frontal lobectomy and treatment  Acanthamoe
 Acanth ba keratitis. Arch Ophthalmol.
amoeba
with amphotericin, cotrimoxazole, and 1995;113(9):1120 – 3
3..
rifampin. Poor prognostic factors include severe De Jonckheere JF. Ecology of  Acantha
 Acanthamoeb
moebaa.
immunosuppression and advanced disease.   Rev Infect Dis. 1991;13(Suppl 5):S3857.
Epidemiology 
Enriquez GL, Lagmay
L agmay J, Natividad
Nativi dad FF,Matias  
GA. Pathogenicity of two human isolates of
 Acanthamoe ba spp. have a protean
 Acanthamoeba  Acanthamoe
 Acanthamoebaba keratitis in mice. Proc. IXth
distribution, having been isolated from a International Congress of Protozoology;
multitude of natural and artificial aquatic 1993. Berlin, Germany.  
environments including fresh and salt water, Fung KT, Dhillon AP, McLaughlin JE, Lucas
sewage, hospital equipment, and contact lenses SB, Davidson B, Rolles K, et al. Cure of
and lens solution.  Acanthamoeba cerebral abscess in a liver  

r eafitir esnt tdiiangn1o9s9e A
GAEDienJoanlcivkihnege p 1d.caPnr t ehvaimo ba
ousely, t1r 4a(n3s p  p1a2t.ient.  Liver   Tr ans  p
):l3a0n8t –  pl.  2008;

diagnosis ofearlier
recognized GAE was post-mortem.
in the AKbeen
1970s and has was Khan NA.
 brain  Acanth
 Aca nthamoe
barrier: amoe
the ba and the blood-
breakthrough. J Med  
reported in the United States, Europe, South Microbiol. 2008;57:1051 – 7 7..
America, and Asia. The first
first case
 case of AK was Matias R, Schottelius
Schotteli us J, Raddatz CF, Michel R.
recognized in the Philippines in the 1990s Species identification and characterization
from a patient from the Philippine General of an  Acanthamoeb
 Acanthamoeba a strain from human
Hospital, and samples obtained from the patient cornea. Parasitol Res. 1991;77(6):469
1991;77(6):469 – 774.
4. 
was shown to cause GAE in mice. Multiple Salvana EM, Matias RR. Histopathology of
environmental
environmental isolates have likewise been well- mouse brain infected with  Acanth
 Acanthamoeb
amoeba
a
characterized from all over the Philippines, isolate IB-17 [undergraduate thesis].  
including a few containing endosymbionts.  Quezon City, Philippines: University of
the Philippines Diliman; 1996.  
Prevention and Control 
Visvesvara GS, Moura H, Schuster FL.
The ubiquitious nature of Acanthamoeba Pathogenic and opportunistic free-living
spp. makes exposure unavoidable. A robust amoebae: Acanth
 Acanthamoeb
amoeba a spp., Balam
 Balamuthia
uthia
immune system is able to prevent infection, mandrillaris, Naegler
 Naegleria
ia fo
fowler ,iand Sappinia
wler 
except in relatively immunocompromised diploidea. FEMS Immunol Med Microbiol.
sites such as the cornea. Meticulous contact 2007;50:1 – 226.
6.
lens hygiene is essential in avoiding infection, Yagita K, Matias RR, Yasuda T, Natividad FF,
and rinsing contact lenses in tap water should Enriquez GL, Endo T.  Acantham oeba sp.
 Acanthamoeba
 be avoided. Prolonged heating and boiling from the Philippines: electron microscopy
kill amebic trophozoites and cyst forms.  studies on naturally occurring bacterial
Immunocompromised persons should be aware   symbionts. Parasitol Res. 1995;81(2):98
1995;81(2):98 – 102.
102. 
 

38  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Naegleriaspp. 

Parasite Biology  10 to 35 µm but when

wh en rounded are usually 10
to 15 µm in diameter. In culture, trophozoites 
  f -olr ivmins:g a pnr oatmoze bo ans
with two vegeatr aetivf rr eee
p p. may get over 40 µm. The cytoplasm is granular
ae g l er ia  s  p
(trophozoite form), and a flagellate (swimming and contains many vacuoles. The single
s ingle nucleus
form). A dormant cyst form is produced when is large and has a large, dense karyosome and
lacks peripheral chromatin.  
conditions are not favorable. Transformation Transformation ia spp. are thermophilic organisms
 Naegleria
 Naegler
from the trophozoite to the flagellate form
which thrive best in hot springs and other warm
may facilitate more rapid movement toward aquatic environments. Both nonpathogenic and
food sources. 
 pathogenicc forms exist.
 pathogeni exi st. Only  Naegler
 Naegleria
ia fow
fowleri
leri
There are two forms of trophozoites of
has been reported to consistently cause disease
 Naegleria
 Naegleria fowleri: ameboid and ameboflagellate,
fowleri
in humans, although some non- fowleri
 fowleri species
only the former of which is found in humans
may cause opportunistic infections.
(Plate 2.10). The ameboid trophozoites measure 

(Accessed from www.dpd.cdc.gov/dpdx)
from www.dpd.cdc.gov/dpdx) 

 Naegleria fowleri has three stages, cysts,  by penetrating

penetrati ng the nasal mucosa and migrating
trophozoites, and flagellated
flagellated forms,
 forms, in its life to the brain via the olfactory nerves. N. fowleri
cycle. The trophozoites replicate by promitosis trophozoites are found in cerebrospinal fluid
(nuclear membrane remains intact) and can turn (CSF) and tissue, while flagellated forms are
into temporary non-feeding flagellated forms, occasionally found in CSF. Cysts are not seen
which usually revert back to the trophozoite in brain tissue (Figure 2.4). 
stage. Trophozoites infect humans or animals
animals 
 

CHAPTER 2: Protozoan Infections   39 

 

40  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Pathogenesis and Clinical Manifestations   shows a fibrinopurulent exudate consisting

mostly of neutrophils in the leptomeninges
 N. fowleri is the causative agent
and brain tissue, and pockets of amebae with
of a rare but rapidly destructive and fatal 
scant inflammatory exudates in necrotic
n ecrotic areas.
meningoencephalitis termed primary amebic Death usually occurs as a result of cerebral or
meningoencephalitis (PAM). In contrast to
cerebellar herniation as a result of increased
GAE which is predominantly an opportunistic  
intracranial pressure. 
ihnef aelctthiyona,dPuAltsMwuitshuaallyhiostcocr uyr soif n s pwr iemvimouinslgy. Diagnosis 
Therefore, in contrast to Acanth  Acanthamoeb amoeba a which
is largely an opportunistic organism, N. fowler fowlerii
Diagnosis of PAM is usually suspected in
is considered a true pathogen. 
 persons with a compatible history of exposure
 N. fowleri is able to survive in elevated
and a rapidly progressive meningoencephalitis.
In the past, definitive
definitive diagnosis
 diagnosis of PAM was
temperatures and reproduces rapidly in
 based on demonstration of characteristic
temperaturess above 30°C. Aside from naturally
temperature
trophozoites in the brain and cerebrospinal
occurring hot springs, warm geothermal plant
fluid. Aspirates from suspected inf ections,
ections, when
effluent into lakes and streams can lead to
introduced into bacteria-seeded agar culture
 proliferation of amebae.  
Most cases of PAM have occurred in young, medium, will exhibit active trophozoites within
24 hours. 
healthy persons who swim in contaminated
ia trophozoites can be identified b
 Naegleria
 Naegler byy
water. The route of entry is through invasion
the presence of blunt, lobose pseudopodia and  
of organisms through the olfactory bulb after
accidental inhalation of water containing seinr escittiivointyalf omr oitdielintyti.fiFclaatgioelnlastiinocnetaem
d stse bhaaevew phoicohr
the organisms. The sustentacular cells of the 
olfactory neuroepithelium are thought to test negative
as Naegler haveand
iaspp.
 Naegleria been subsequently
 Naegleriafowle
 Naegler identified
ri with
iafowleri more
 phagocyt ose the amebae
 phagocytose ameb ae and transport
trans port these
thes e sensitive and specific molecular techniques such
through the cribriform plate and into the brain.
Multiple mechanisms then come into play,
as PCR andimmunostaining. Serology utilizing
ELISA is less useful in diagnosing active
 producin g a cytopathic effect on host tissues.
 producing ti ssues.
These mechanisms include secretion of lytic infection since healthy individuals especially in
enzymes, membrane pore-forming proteins, endemic areas have been shown to have positive
factors which induce apoptosis, and direct antibody titers. 
feeding on cells by the amebae. Treatment 
In humans, PAM presents as fever, nausea,
vomitin g, headache, nuchal
vomiting, nuchal rigidity,
rigidi ty, and mental Most persons infected with  Naegleria die
 Naegleria
status changes, with rapid progression to coma    prior to institution of effective treatment.
Symptoms of PAM are indistinguishable from
afinnddidnegastihn.clCuhdaer ealcetvear tiestdicwcheir te b
 br loso pdinceall  flcouuidnt  bacterial meningitis. Initial CSF results
results are
with neutrophilic predominance, high protein, suggestive of a bacterial etiology,and so patients
and low glucose.  are typically treated with antibiotics which have
no activity against Naegleria . 
Post-mortem
Post-mor tem examination
examinat ion of infected
infectedbrain
Amphotericin B in combination wit with
h
shows hemorrhagic
the olfactory necrosis, particularly
bulbs, congestion and edemaofof clotrimazole is synergistic, and has been
neural tissue. Leptomeninges are inflamed and successfully used to treat PAM. Amphotericin
congested as well. Microscopic examination  B produces deleterious changes in the nucleus
n ucleus 
 

CHAPTER 2: Protozoan Infections   41 

and mitochondria of the ameba, decreases Prevention and Control 

the number of food vacuoles, and increases
The ubiquitous nature of  Naegleria, in
the formation of autophagic vacuoles. Ameba
contrast to the rarity of infection seems to
exposed to amphotericin B exhibit decreased
 pseudopod formation and form blebs on
indicate that incidental exposure is unlikely to
the plasma membrane. Newer agents such
lead to disease. Most instances of infection
i nfection are
related to invasion of the ameba through the 
as azithromycin and voriconazole have been  
shown to be active against N. fowleri
vitro and in vivo.
fowleri, both in
of lf athcteohr yea bdual b
 nbsd,  aacncdidseontavl oinidhianlgatiiomnmoef r swioanter
should be practiced in endemic areas and in hot
Epidemiology  springs. No known cases of PAM have resulted
from drinking ameba-infected water.  
Distribution of  Naegleria in freshwater
 Naegleria fowleri is easily killed by
lakes and ponds has been correlated with
chlorination of water at 1 ppm or higher.
 physical, chemical, and biological
biolog ical parameters. Infection has been reported from swimming
Strains have been frequently isolated from
in contaminated water with inadequate
thermal effluents,
effluents,  hot springs, and water with
chlorination, and so recommendations for
naturally or artificially elevated temperatures.
appropriate decontamination of swimming
Fecal coliform contamination provides a ready water should be followed, especially in areas of
food source for ameba, and may increase the risk high prevalence.
of infection due to higher density of organisms. 
Studies on local Naegle ria have identified
 Naegleria identified   References 

aindnieswtins p is iomcohr  p
gueicsiheas bwleh bicuht  b emhioclaollgyicadlilsytinct Behets
Beh ets J, Seghi F,
F,Declerck
Decl erck P,Verelst L, Duvivier
L, Van Damme A, et al. Detection of
from other
thermally- knownstream,
 polluted
 polluted strspecies. Isolates from
eam, an artificially a
-heated  Naegleria spp. and  Naegleria fowleri : a
comparison of flagellation tests, ELISA and
swimming pool, and from the brain aspirate of
a young patient have all yielded a single species,  PCR. Water Sci Techno
Technol.l. 2003;47(3):117
2003;47(3): 117 –  
22. 
 N. philippinensis. This has been extensively
Enriquez GL. Studies on  Naegleria isolate
studied by Castro et al., and Matias et al. Only
O nly
from a reported case of PAM from the
one case of PAM has been reported locally, in
a young male with a history of swimming in
Philippines. 1989. Located at: College of
fresh water. He responded well to amphotericin Public Health Library, University of the
Philippines Manila. 
B infusion.
Two Philippine isolates of  Naegleria
Matias RR, Enriquez GL, Schotellius J. Surface
(NSzu and RITM strains) have been evaluated lectin receptors on a Naegleria species from
 Naegleria
for pathogenicity. Massive doses of amebae the Philippines. Lectins Biol Biochem Clin 
successfully established
established infection in the brain mS. ,19M9o0u;7r :a32H9 – 
and caused death in some mice within two to
VisveBsivoacr haeG , S3c3h. uster  FL.
six days post-inoculation. Clinical features of Pathogenic and opportunistic free-living
infection and histopathology were compatible amoebae: Acanth  Acanthamoeb
amoeba a spp., Balam
 Balamuthia
uthia
mandrillaris, Naegler
 Naegleria ia fo
fowle
wler  r ,iand Sappinia
with PAM. 
diploidea. FEMS Immunol Med Microbiol.
2007;50:1 – 26.
26.
 

42  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Ciliates and Flagellates

Vicente Y. Belizario, Jr., Francis Isidore G. Totañes

Balantidiumcoli   Human infection results from ingestion

of food and/or water contaminated with  B.   B.  
nitially identified as  Paramecium coli
c oli by coli cysts. The incubation period is normally
I  Malmsten in 1857,  Balantidium coli was 
later described and placed under a separate
from 4 to 5 days. Ingested cysts excyst in the
small intestines and become trophozoites.  
genus in 1863. B. coli is the causative agent Trophozoites inhabit the lumen, mucosa, and
of the zoonotic disease called balantidiasis, submucosa of the large intestines,
i ntestines, primarily
 balantidiosis, or balantidial dysentery. It is the cecal region. They cause pathologic
considered as the largest protozoan parasite changes in the colonic wall and mucosa.  
affecting humans and is the only ciliate Parasite reproduction occurs asexually through
known to cause human disease. It is capable of asymmetric binary fission, although sexual
attacking the intestinal epithelium, resulting in reproduction through conjugation has been
ulcer formation which, in turn, causes bloody reported. Cysts are formed principally as
diarrhea similar to that of amebic dysentery.  protection for survival outside the host. The
This organism is primarily associated with pigs,  parasites encyst
en cyst during
duri ng intestinal
intesti nal transport
trans port or
its normal host.  after evacuation of semi-formed stools. Cysts  
Parasite Biology  avr iae btlhe ef oir nsf evcteir vael wsteaegkes, (aFnidgutr hee2y.5m).ay  r emain 

 Balantidium coli trophozoite measures Pathogenesis and Clinical Manifestations 

30 to 150 µm long and 25 to 120 µm µ m wide.
For locomotion, trophozoites are covered tidium colitrophozoites are capable of
 Balantidium
 Balan
with cilia arranged in a longitudinal pattern attacking the intestinal epithelium and creating
extending from the oral to the caudal
caud al region.  a characteristic ulcer with a rounded base and
It has a cytostome, an oral apparatus at wide neck, in contrast to the flask-shaped,
the tapered anterior end, through which it  narrow necked ulcers of amebiasis. Ulceration is
acquires food, and a cytopyge at the rounded caused by the lytic enzyme hyaluronidase which
 posterior end through which it excretes waste. is secreted by the trophozoite. The trophozoites
It has two dissimilar nuclei. The macronucleus are abundant in exudates on mucosal surfaces;
surfaces;
is usually bean-shaped and can easily be while inflammatory cells and trophozoites
trop hozoites are
identified in stained specimens, while the numerous in the base of the ulcers. Trophozoites
Trophozoites
micronucleus is round and lies in the concavity also invade the submucosa and the muscular
of the macronucleus. B.
 B. coli has two contractile coat, including blood vessels and lymphatics.  
vacuoles that act as osmoregulatory organelles. Intrinsic host factors including nutritional 
The parasite also contains extrusive organelles status, intestinal bacteria flora, achlorhydria,
called mucocysts which are located beneath the alcoholism, and presence of chronic disease
cell membrane.  contribute to host susceptibility to and severity
 B. coli cysts are spherical to slightly ovoid of B. coli infection. It has been suggested by
in shape and measure 40 to 60 µm in diameter. some investigators that B. coli mucocysts might
They are covered with thick cell walls (double- have a function in the adhesion of parasitic
walled). Unlike amebae, encystation does not ciliates that may contribute to
t o parasite virulence,
result in an increase in number of nuclei.   although no definitive study has proven this. In 
 

CHAPTER 2: Protozoan Infections   43 

 

44  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

one study, it was shown that mucocysts

mu cocysts in B. Diagnosis 
coli trophozoites obtained from symptomatic
Diagnosis is made by microscopic
 pigs were more numerous compared with
demonstration of trophozoites and cysts in
trophozoites
trophozoites obtained from asymptomatic
asymptomatic hosts.
In addition, co-infection with other organisms feces using direct examination or concentration
(sedimentation or flotation) techniques.  
may also contribute to severity o  BBf .coli infection.
Repeated stool examinations may be done to  
The presence of Salmonella in the intestines  
has been shown to aggravate balantidiasis by ashe oseznoistietisviinty b. D
ionf ctr r eo p nsetcr iam
syos p
io pem tin mr elesseinocnes
engstf hr eo p
invading the ulcers caused by the protozoan.   obtained through sigmoidoscopy is likewise
Balantidiasis has three forms of clinical diagnostic. Bronchoalveolar washings may  
manifestations. Asymptomatic carriers are also contain B. coli trophozoites in the case of
those who do not present with diarrhea or
 pulmonary infection.
dysentery, but may serve as parasite reservoir
in the community. Fulminant balantidiasis, Treatment 
or balantidial dysentery involves diarrhea with
 bloody and mucoid stools, which is sometimes The treatment of choice for balantidiasis
indistinguishable from amebic dysentery. Acute is tetracycline or metronidazole. Treatment in
cases may have 6 to 15 episodes of diarrhea per adults and older children is with tetracycline
day accompanied by abdominal pain, nausea, 500 mg or 40 mg/kg/dose divided in four doses
for 10 days. Tetracycline is contraindicated
and vomiting. This form of balantidiasis is
in children less than eight years of age and in
often associated with immunocompromised  
 pregnant women. Metronidazole
Metroni dazole 750 mg three
 banaldanmtiadlinaosius r is htehde scthar toesn.icTf hoer m r dhef r oer im
thiw n  of
times daily, or 35 to 50 mg/kg body weight/
day in three divided doses, may be given for
diarrhea
may may alternate
be accompanied bywith constipation,
nonspecific and
symptoms 5 days. Iodoquinol may also be given at 650
mg, or 40 mg/kg/dose, divided in three doses
such as abdominal pain or cramping, anemia,
for 20 days. Other alternative treatments
and cachexia. 
for balantidiasis include doxycycline and
 B. coli can spread to extraintestinal sites
including the mesenteric nodes, appendix, liver, nitazoxanide. Currently there are no reports of  
 B. coli exhibiting drug resistance . 
genitourinary sites, pleura, and lungs. One
case report involved the detection of a cavitary Epidemiology 
lesion in the right upper lobe of the lung on
chest radiograph in a patient who presented The distribution of B. coli is cosmopolitan
with hemoptysis. The patient had a history of and is more prevalent in areas with poor
insulin-dependentdiabetes andorganic farming sanitation, close contact with pigs or pig feces
using pig manure as fertilizer. Bronchoalveolar 
Bronchoalveolar   (e.g., farms, abattoirs), and in overcrowded  
lavage revealed B. coli trophozoites.
trophozoites. Another case institutions (e.g., asylum, orphanages, prisons).
Warm and humid climates in tropical and  
 presented with pulmonary
pulmon ary hemorrhage
hemorrh age and iron subtropical countries can also contribute to
deficiency anemia, and revealed numerous
nu merous  B.
coli trophozo
trophozoites
ites by bronchial biopsy and lavage.  the survival of cysts. High prevalence levels
Complications of balantidiasis include in pigs have been reported in regions in Latin
intestinal perforation and acute appendicitis. America andPapua
Philippines, the Middle East, as well
New Guinea, as in
and the the
West
Cases of mortality related to balantidiasis
were reported to be associated with intestinal Irian province of Indonesia. 
hemorrhage and shock, intestinal perforation, There is an estimated 1% worldwide
or sepsis.   prevalence of human  B. coli infection. Pigs 
 

CHAPTER 2: Protozoan Infections   45 

are the major host of balantidiasis, although Dodd LG.  Balantidium coli infestation as a
 primates have been reported to harbor infection. cause of acute appendicitis. J Infect Dis.
Prevalence studies in the United States and in 1991; 163:13 – 992.
2. 
Europe have reported infection rates ranging Goldberg JE, Parasitic colitides. Clin Colon
from 5% to as high as 100% in some areas. In Rectal Surg. 2007;20:38 – 4
46.
6. 
a study done in two (northern and southern) Karanis P, Kourenti C, Smith H. Waterborne
Water borne
sites in the Philippines, an examination of pigs  transmission of protozoan parasites: a 
revealed 66.1% prevalence of B. coli infection. worldwide review of outbreaks and lessons
There has been a single report of an outbreak learnt. J Wat Health. 2007;5:1 – 3
38.
8. 
of balantidiasis that occurred in the Truk island  Koopowitz A, Smith P, van Rensburg N,
in Micronesia in 1971. RudmanA.  Balantidium colicoli -induced
 pulmonary haemorrhage with iron
Prevention and Control 
deficiency. S Afr Med J. 2010;100:534 – 66..  
Control measures for balantidiasis include Ladas SD, Savva S, Frydas A, Kaloviduris  
 proper sanitation, safe water supply, good A, Hatzioannou J, Raptis S. Invasive
 personal hygiene, and protection
protecti on of food from  balantidiasis
 balantidi asis presented
present ed as chronic
chroni c colitis
coliti s
contamination. Measures to limit contact of and lung involvement. Dig Dis Sci.  
 pigs with water sources and food crops may 1989;34(10):1621 – 3
3..
also contribute to reducing transmission La Via MV. Parasitic gastroenteritis. Pediatr
and infection. Use of pig feces as fertilizer Ann. 1994;23(70):556 – 6
60.
0. 
should also be avoided. Though cysts may   Lee JL, Lanada EB, More SJ, Cotiw-an  
 bmeayr essuisr tvainvte  tf or elnovnigr o pnemr ieondtsalof cotinmdeit,iothnesyaanr de of S,gr Toawvienr go p
B s .r aAiseldon bgyitusm
s iAgA dianlalhl osltduedr y

easily inactivated
hypochlorite. by heat
Ordinary and by 1%of
chlorination sodium
water farmers in the Philippines.
2005;70:75-93.   Prev Vet Med.
is not effective against B. coli cysts.   Nakauchi K.The prevalence
prevalen ce of Balantidium
Balantid ium coli
infection in fifty-six mammalian species. J
References 
Vet Med Sci. 1999;61(1):63 – 5
5.. 
Beaver PC, Jung RC, Cupp EW. Clinical  Nilles-Bije ML,
ML, Rivera WL. Ultrastructural
Ultrastructural and
 parasito
 parasitology
logy.. Philadelphia:
Philadelphia: Lea and
and Febiger; molecular characterization of Balan
 Balantidium
tidium
1984.  coli isolated in the Philippines. Parasitol
Belding DL. Textbook of parasitology. 3rd Res. 2010;106:387 – 94. 94.
ed. New York: Appleton-Century Crofts; Shar ma S, Har ding G.  NNecr otizing lung inf eecction
1965.  caused by the protozoan  Balantidium coli .
Borda CE, Rea MJ, Rosa JR, Maidana C. Can J Infect Dis. 2003;14(3):163 – 6 6..
Intestinal parasitism in San Cayetano, Schuster FL, Ramirez-Avila L. Current world  
Corrientes, Argentina. Bull of Pan Am status of Balantidium coli . Clin Microbiol
Health Organ. 1996;30(3):227 – 33.
33.  Rev. 2008;21(4):626 – 38. 38.
Farthing MJ. Treatment options for the Skotarczak B. Cytochemical identification of
eradication of intestinal protozoa. Nat mucocysts in Balan
 Balantidiumcoli trophozoites.
tidiumcoli
Clin Pract Gastroenterol Hepatol. Folia Biol. 1999;47(1-2):61 – 5
5..
2006;3(8):436 – 45.
45. The Medical Letter. Drugs for parasitic
infections [Internet]. Available from www.
from www.
medicalletter.org. 
 

46  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Gi 
ard iaduodena lii 
s 
Juan Antonio A. Solon  

iardia duodenalis is an intestinal parasitic Cysts are ovoid and measure 8 to 12 µm

flagellate of worldwide distribution. It  is  long by 7 to 10 µm
µ m wide. The young cysts have 
known to cause epidemic and endemic diarrhea. two nuclei, while the mature cysts have four.
This protozoan is also known as Giardia Cysts are characterized by flagella retracted into
intestinalis or G. lamblia. It wasfirst
was first  discovered axonemes, the median or parabasal body, and
in 1681 by Antoine van Leeuwenhoek in his   deeply stained curved fibrils surrounded by a 
own stools and was first described by Lambl in tough hyaline cyst wall secreted from condensed
condensed
1859 who called itCercomonas intestinalis. It was cytoplasm.  
later renamed Giardia lamblia by Stiles in 1915. Cysts from animals or human feces are
The disease caused by this parasite is called transferred to the mouth via contaminated
giardiasis, and this manifests as a significant hands, food, or water. Once mature cysts
 but not
not life-threatening
life-threatening gastrointestinal
gastrointestinal disease.  (infective stage) are ingested, they pass safely
through the stomach and excyst in the
Parasite Biology 
duodenum (in about 30 minutes) developing
Giardia duodenalis is a flagellate that lives into trophozoites which rapidly multiply and
in the duodenum, jejunum, and upper ileum   attach to the intestinal villi causing pathologic 
othf aht uinmclaundse. sIttr o p
hahs oazosiitm
e p le asexual lif e cycle
s and quadr inucleated cinhatnhgee jse.  jT tr .o pAhs otzhoeitf eescm
unhuem es aeyntther esn b
thee  f coouln
ond
infective
shows thatcystthose
stages. Molecular
which typing
parasitize of isolates
humans can and dehydrates,
encystment, the parasite
mature then
cysts are encysts.
passed After
out in the
 be classified as belonging to either assemblage feces and are infectious (Figure 2.6). 
A or B genotypes based on specific sequences Pathogenesis and Clinical Manifestations  
in the small subunit of their ribosomal RNA. 
The trophozoites measure 9 to 12 µm Infection with G. duodenalis occurs when
long by 5 to l5 µm wide. They are pyriform the host ingests food or water contaminated
or teardrop shaped, pointed posteriorly, with with the mature cysts. Depending on the strain
a pair of ovoidal nuclei, one on each side of involved, infection can occur with one ingesting
the midline. The dorsal side of the
t he organism is as few as 10 cysts. The
Th e ability of the parasite to
convex, while the ventral side is concave with cause disease can be traced to its ability to alter
a large adhesive disc used for attachment. It is mucosal intestinal cells once it has attached to
 bilaterally
 bilateral ly symmetrical, with a distinct
distin ct medial the apical portion
port ion of the enterocyte.
enterocyte. The parasite
line called the axostyle. The parasite is propelled attaches to the intestinal cells via an adhesive
into an erratic tumbling motion by four pairs sucking disc located on its ventral side, causing
of flagella arising from superficial organelles in mechanical irritation in the affected tissues.
the ventral side of the body. Trophozoites
Trophozoitesdivide Several studies have investigated this mechanism
 by longitudinal binary fission and are found in of attachment. In monolayer studies, it was
diarrheic stools. Antigenic variation results in noted that attachment was influenced by certain
the entire surface of the parasite being covered  physical factors such as temperature and pH.
with variant-specific surface proteins (VSPs).   Attachment was observed to be maximal at 
 

CHAPTER 2: Protozoan Infections   47 

 

48  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 body temperature and stable at a pH of 7.8  be asymptomatic. Fo

Forr aacute
cute cases, patients
to 8.2. The parasite may also produce a lectin experience abdominal pain, described as
which, when activated by duodenal secretions, cramping, associated with diarrhea. There is
is able to facilitate attachment. Once attached, also excessive flatus
flatus with
 with an odor of “rotten
the organism is able to avoid peristalsis by eggs” due to hydrogen sulfide. Other clinical
trapping itself in between the villi or within the features include abdominal bloating, nausea,
intestinal mucus. and anorexia. Diarrhea is the most common  
Upon attachment to the intestinal cells,   symptom, occurring in 89% of cases. It is
G. duodenalis is able to cause alterations in   followed by malaise and flatulence. Spontaneous
the villi such as villous flattening
flattening and
 and crypt recovery occurs within 6 weeks in mild to  
hypertrophy.These alterations lead to decreased moderate cases. In untreated cases, patients may
electrolyte, glucose, and fluid absorption, and experience diarrhea with varying intensities, for
cause deficiencies in disaccharidases. Studies on weeks or months. 
Giardiamuris-infectedmice showeddiffuse loss Chronic infection is characterized by
of microvillous surface area which investigators steatorrhea, or the passage of greasy, frothy
also correlated to decreased maltase and stools. In some cases, periods of diarrhea have
sucrase activities. The physiologic disturbances
disturbances  been observed to alternate with normal or even
subsequently result in malabsorption and constipated bowel periods. There may be weight
maldigestion, which in turn cause the signs and loss, profound malaise, and low-grade fever. In
symptoms experienced
experienced by the patient. Bacterial developing countries, it has been described as a
colonization of the area may further worsen the  cause of the failure-to-thrive syndrome.  
adstyucdaiues,edG b. yd uthod 
damaIngeoatlhr er  e par asite.
enal i s was shown
Diagnosis 

to
andrearrange
duodenalthemonolayers.
cytoskeleton in human colonic
Cytoskeleton is Diagnosis
duodenalis is made(Plate
trophozoites by demonstration of G.
2.11)and/or cysts
essential for proper cell attachment to the (Plate 2.12) in stool specimens. Trophozoites
extracellularr matrix and the other neighboring
extracellula in direct fecal smears may be characterized as
cells. Changes observed in apoptotic cells having a floating leaf -like
-like motility. To detect 
include disruption of the cytoskeleton that leads
to structural disintegration and detachment
from the substrate. Hence, the parasite has
 been suggested
sugg ested to cause
caus e enterocyte
enterocyt e apoptosis.
apoptosi s.
This finding was strengthened
strengthened by another study,
stu dy,
which showed the ability of the parasite not
only to disrupt cellular tight junctions but also
toincreaseepithelialpermeability,thus,leading  
to the loss of epithelial barrier function. With
this loss of barrier function, luminal contents
contents
may penetrate the submucosal layers causing
causing
more damage in the intestinal tissue.  
From ingestion of the cysts, it takes about
1 to 4 weeks (average of 9 days) for the disease Plate 2.11. Giardiaduodenalistrophozoite
(Courtesy of the Department of Parasitology,
to manifest. Half of the infected patients may  UP-CPH)
 

CHAPTER 2: Protozoan Infections   49 

the highest combination of sensitivity and

specificity. 
Treatment 

Giardiasis may be treated with

metronidazole 250 mg three times a day for 5
to 7 days (pediatric dose: 15 mg/kg/day in three  
divided doses). Metronidazole is usually well- 
tolerated in adults and has a cure rate of 90%.  
Alternative drugs include tinidazole (single 
dose of 2 g for adults; 50 mg/kg in children) 
and furazolidone (100 mg four times daily
Plate 2.12. Giardiaduodenaliscysts for 10 days for adults; 6 mg/kg/day in four
(Courtesy of the Depa rtment of Parasitology,
Parasitology, divided doses for 7 to 10 days). Albendazole
UP-CPH)  is an alternative at 400 mg/day for 5 days in
adults and 10 mg/kg/day for 5 days in children.
cysts in stools, concentration techniques are A meta-analysis has shown that albendazole is
recommended. At least three stool examinations
recommended. equally effective as metronidazole at the above 
on alternate days are recommended because of doses. Although not available in the Philippines,
spotty shedding of cysts. If the parasite is not nitazoxanide has likewise been used effectively
found in the feces, duodeno-jejunal aspiration  in drug-resistant cases.  

coanyte bnetsdf oonr et.r oE pxham
m ozioniatetisongivoef s tahehidguhoedr  enal indivPidr oumls tr etdr euactemceynstt  p
a p of asassaygme p
  atnodm patoiscsi b
 ble
 percentage of positiv
positivee findings
finding s compared
compare d to
examination of feces. In a patient with chronic transmission
such especiallyinstitutionalized
as foodhandlers, among high riskpatients,
groups
diarrhea, giardiasis should be considered as a children attending day-care, and day-care
 possible cause.  workers. 
Aside from duodenal aspiration, the
Epidemiology 
Enterotest® (HDC Mountain View,
View, CA) may
demonstrate Giardia trophozoites. The patient Giardia has a worldwide distribution. In
swallows a gelatin capsule attached to a nylon the Philippines, the prevalence of giardiasis
string, with one end of the string attached to ranges from 1.6 to 22.0% depending on the
the patient’s
the patient’s cheek.
 cheek. After about 4 to 6 hours,  population
 populat ion group being studied. From the local
the string is removed, and any adherent fluid is data, it can be clearly seen that the groups in
 placed on the
the slide for microscopic
microscopic examination.
examination.  areas with poor sanitation and hygiene practices
Presently, antigen detection tests and have a higher prevalence of giardiasis.  
immunofluorescent tests are already available  Notably, Giardia is not commonly found
as commercial kits. Immunochromatographic in patients with diarrhea. In this symptomatic
assays detect the presence of Giardia antigen  population,, the prevalence
 population prevalence was similar between
in stool. Cyst wall protein 1 (CWP1) is one children (<18 years old) and adults. However,
of the antigens used for these diagnostic tests.
Direct fluorescent antibody assays have  been the prevalence
higher of giardiasis
in male adults was significantly
than females, a trend also
considered by many laboratories as the gold seen in other countries (Tabl
(Tablee 2.2).
standard in diagnosis as such assays have 
 

50  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Table 2.2. Selected Philippine data on giardiasis  

Reference  Po pulation
(n)  Prevalence 
CrossandBasaca-Sevilla(1986)  Community(n=30,000)   6.0%  

 Auer (1990)  Urbanpoor,8months –15years(n=238) 20.0%

Bustos, et al. (1991)   Mentallyillpatients(n=176) 17.0%

Lee
eee
e t l(.1999) 
, a Childr en(LegazpC
i  ityn
)  64  
=
7.8%  

Belizario, et al.(2000)   Community(Brgy.

Community(Brgy. S an Isidro, Compostela Valley) (n=242)  7.4%  
 Avila, et al. (2003)  Food handlers, school canteen (n=123)   3.3%  

Esparar,etal.(2003)  Foodhandlers,tertiaryhospital(n=59)  3.4%  

Kim ,t((l2
ea l. 003)  C ommunit(yn 301) 
= 0.0% 

Baldo,etal.(2004)  Institutionalizedchildren(Metro
Institutionalizedchildren(MetroManila)(n=172
Manila)(n=172))   11.6%  

Belizario,etal.(2005)  Mallemployees(Cebucity)(n=256)   0.8% 

Natividad,etal.(2008)   Diarrheicpatients(n=3,456)   2.0%  

The first published study on Giardia or by infected food handlers. Normal water  
genotypes in the Philippines showed that the chlorination will not affect cysts, but usual
majority (86%) of the isolated genotypes
geno types belong  water treatmentmodalities should be adequate. 
to assemblage B.   References 
Direct oral-anal sexual contact among men
who have sex with men may increase the risk Adam RD. Biology of Giardia lamblia. Clin
of giardiasis and infection with other intestinal Microbiol Rev. 2001;14(3):447 – 7 75.
5. 
 protozoans.  Adam RD, Nigam A, Seshadri V, Martens  
Outbreaks of giardiasis are more frequently CA, Farneth GA, Morrison HG, H G, et al. 
reported outside the Philippines. Most of these The Giardia lamblia vsp gene repertoire: 
are water-borne (recreationalwater or drinking characteristics, genomic
genomic organization,
organization, and  
water). Foodborne outbreaks have also been evolution. BMC Genomics. 2010;11:424. 
reported. The low infective dose, prolonged Auer C. Health status of children living in
communicability, and relative resistance to a squatter area of Manila, Philippines,
chlorine facilitate the transmission of Giardia with particular emphasis on intestinal  
through drinking and recreational
recreational water, food,
and person-to-person contact.    p r asH
Pau b itoeaseltsh. .S1o9u9th0;e2a1st(2A):s2iiaa8n9 – J3T00r ro . p
    Med
 p 
Avila MS, Garcia MR, M R, Narcelles MV, Serra 
Prevention and Control 
FB, Tejida BM. Prevalence of intestinal
Methods of prevention and control include helminth and protozoan infections among
 proper or sanitary
to prevent disposalof
contamination of food
human excreta
and water food-handlers
in in selected school
Manila [undergraduate specialcanteens
study].
supply. The former can be contaminated 2003. Located at: College of Public Health,
 by the use of night soil as fertilizer, by flies,  University of the Philippines Manila.  
 

CHAPTER 2: Protozoan Infections   51 

Baldo ET, Belizario VY, de Leon WU, Kong Esparar DG, Belizario VY, Jr., Relos JR.
HH, Chung DI. Infection status of Prevalence of intestinal parasitic infections
infections
intestinal parasites in children living in among food handlers of a tertiary hospital
residential institutions in Metro Manila, in Manila using direct fecal smear and
the Philippines. Korean
K orean J Parasitol.  formalin ether concentration technique.
2004;42(2):67 – 70.
70. Phil J Microbiol Infect Dis. 2004;33(3):1 –  
Beaver PC, Jung RC, Cupp EW. Clinical   6.
 parasitology.
 parasitology. 3rd ed. Philadelphia:
Philadelphia: Lea and
and Faubert G. Immune Response to Giardia
Febiger; 1984.  duodenalis . Clin Microbiol Rev.
Belding DL. Textbook of parasitology. New 2000;13(1):35 – 54.
54.
York: Appleton-Century Crofts; 1965.   Gardner TB, Hill DR. Treatment of Giardiasis.
Giardi asis.
Belizario VY, Jr., de Leon WU, Esparar Clin Microbiol Rev.
Rev. 2001;14(1):114 – 228.
8.  
DG, Galang JM, Fantone J, Verdadero  Jones JE. String test for diagnosing Giardiasis.
C. Compostela Valley: a new endemic Am Fam Physician. 1986;34(2):123 – 66.. 
focus for Capillariasis philippinensis. Kim BJ, Ock MS, Chung DI, Yong TS, Lee
Southeast Asian J Trop Med Pub Health. KJ. The intestinal parasite infection
2000;31(3):478 – 81.
81.  status of inhabitants in the Roxas City,
Belizario VY, Jr., Bersabe MJ, de Leon WU, the Philippines. Korean
K orean J Pa
Parasitol.
rasitol. 
Bugayong MG, de Guzman AD, et al. A 2003;41:113 – 5 5..
new look at heterophyidiasis (intestinal Korman SH, Hais E, Spira DT. Routine in
fluke infection): a food-borne parasitic  vitro cultivation of Giardia lamblia by
noesailsthinr tehseaPr hchil p
zoof  oH  ipc pin pese.nIdni:uDme p1a9r 9tm
om 3 – ent usi9n0g;2th8e(2s)t:r 
19 3i6n8g – t9e.st.  J  Clin  Micr o biol. 
2001. Manila
of Health; (Philippines):
2001. 1. Department
p. 60 – 1. Kuntz RE. Intestinal
republic parasites JofPhilipp
of the Philippines. man inMed
the
Belizario VY, Diaz AB, Esparar DG, Bugayong Assoc. 1963;39(7):590 – 600.
600.
MG. Parasitologic screening of mall Lee KJ, Ahn YK, Yong TS. A small-scale
employees applying for health certificates survey of intestinal parasite infections
at a local health office in Cebu City: among children and adolescents in Legaspi
implications for policy and practice. Phil J City, the Philippines. Korean J Parasitol.
Microbiol Infect Dis. 2005;34(2):65 – 70.70.   2000;38:183 – 5 5.. 
Bustos MD, Salazar N, Espino FE, Montalban  Nash TE. Antigenic variation in Giardia
CS, Sabordo D, Laurente M. Ornidazole in lamblia and the host’s immune respon se.
the treatment of giardiasis in an institution Philos Trans R Soc Lond B Biol Sci.  
for the mentally retarded. Phil J Microbiol 1997;352(1359):1369 – 7 75.
5.
Infect Dis. 1991;20(1):13 – 6.
6.  Nash TE, Herrington DA, Losonsky GA,
Cross JH, Sevilla VB. Biomedical surveys in Levine MM. Experimental human
the Philippines. Manila (Philippines): US infections with Giardia lamblia. J Infect
 NAMRU Unit
Un it No. 2; 1984.  Dis. 1987;156(6):974 – 8 84.
4.
Dib HH, Lu SQ, Wen
W en SF
SF.Prevalence of Giardia
Giardia  Natividad FF, Buerano CC, Lago CB,
lamblia with or without diarrhea in South Mapua CA, de Guzman BB, Seraspe
East, South East Asia and the Far East. EB, et al. Prevalence rates of Giardia and
Parasitol Res. 2008;103(2):239 – 51.
51. Cryptosporidium among diarrheic patients 
 

52  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

in the Philippines. Southeast Asian J Trop Yasonn JA, Rivera WL. Genotyping of Giardia
Yaso
Med Public Health. 2008;39(6):991 – 9.
9 .  duodenalis isolates among residents of slum
Oberhuber G, Stolte M. Giardiasis: analysis of area in Manila, Philippines. Parasitol Res.
histological changes
changes in biopsy specimens of 2007;101(3):681 – 7 7..
80 patients. JClin Pathol. 1990;43(8):641 –   Yoder JS, Harral C, Beach MJ. Giardiasis
3. surveillance — United
United States, 2006-2008.
Upcroft P, Upcroft JA. Drug targets and MMWR Surveill Summ. 2010;59(6):15 –  
mechanisms of resistance in the 25.
anaerobic protozoa. Clin Microbiol Rev.
2001;14(1):150 – 64.
64. 
 

CHAPTER 2: Protozoan Infections   53 

Tr ic ho mo nas vaginalis 
 vag
Juan Antonio A. Solon  

richomonas vaginalis causes a sexually of the tissue layer. The trophozoites infect the
transmitted disease called trichomoniasis  surface but do not appear to invade the mucosa. 
which has a worldwide distribution. Its The acute inflammation caused by the parasite
incidence correlates strongly with the number results in the characteristic liquid vaginal
of sexual partners. It was first observed by secretions, greenish or yellow in color, that
Donne in 1836 in purulent secretions of male   cover the mucosa down to the urethral orifice,
orifice,  
and female urogenital tracts. It is now often vestibular glands, and clitoris. The vaginal
described as the most prevalent non-viral secretions are very irritating and may cause
sexually transmitted infection.  intense itchiness and burning sensation. As the
Parasite Biology 
acute condition changes to the chronic stage, the
secretion loses its purulent appearance due to a
Trichomonas vaginalis exists only in the decrease in the trichomonads and leukocytes, an
trophozoite stage. It has a pyriform shape,
shap e, increase in epithelialcells, and the establishment
measuring 7 to 23 µm with four free anterior of a mixed bacterial flora. Aside from the
flagella that appear to arise from a simple common symptoms of vaginal discharge,
stalk, and a fifth
fifth  flagellum
flagellum embedded
 embedded in the  vulvitis, and dysuria, trichomonads appear to 

tonad buolauttinhgalm
u e e  bor r gaannei.sTmhsilsem
f  thm ’ ngetm br ane exten s
h. The par asitde  beosat p
 p  p tedenwdiothmaentr iitnisc.r C
ssaor ctiuam eaosemd pilniccaitdieonncseinof
has a median axostyle and a single nucleus.   women include secondary
The parasite is found in the urogenital
urog enital of the urogenital tract.   bacterial infection
tract. In women, it is found in the vagina but Speculum examination reveals punctate
may ascend as far as therenal pelvis.
pelv is. The parasite
parasit e hemorrhages of the cervix, the so-called
can be isolated from the urethra, prostate, and strawberry cervix, which is observed in only
less frequently, in the epididymis in men. The 2% of cases. 
trophozoites multiply by binary fission
fission in
 in the Trichomonas infection in males may be
host and are transferred passively from person latent and essentially asymptomatic. In some
to person (Figure 2.7). The usual mode of cases, it is responsible for an irritating persistent
transmission is by sexual intercourse.   and recurring urethritis. Prostatitis is the most
common complication.  
Pathogenesis and Clinical Manifestations  
Diagnosis 
Inflammation of the vaginal mucosa occurs
several days after the inoculation of T.vaginalis
vagina lis Saline preparation of vaginal fluid is
trophozoites. T. vaginalis cannot live without the quickest and most inexpensive way to
close association with the vaginal, urethral,  diagnose trichomoniasis, but the sensitivity
or prostatic tissues. Four to 28 days after of this technique is low at 60 to 70%. The

introduction
introdu ction ofcolonies
 proliferating vi
viab
able
leT. vaginalis into the vagina,
of the flagellate cause accepted
takes 2 togold standard
5 days. is culturewet
The unstained which
drop
degeneration and desquamation of the vaginal
v aginal  preparations may be fixed and stained by
epithelium followed by leukocytic inflammation   Giemsa, Papanicolau, Romanowsky, and  
 

54  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

acridine orange stains. Trichomonas can also be detection tests and polymerase chain reaction
cultured using Diamond’s modified medium,
and Feinberg and Whittington culture medium.   (PCR) assays
not widely arelocally.
used commercially available,
PCR among but
females
The Pap smear may also showtrichomonads
showtrichomonads does not seem to offer an added diagnostic
(sensitivity 60%; specificity  95%). Antigen 
specificity 95%). advantage. Among males, however, diagnosis is  
 

CHAPTER 2: Protozoan Infections   55 

more difficult. For culture, the best results are Epidemiology 

seen with a combination of cultures of urethral
Trichomonasinfection occurs worldwide. It
swabs and urine sediment. PCR appears to
is estimated that there are 170 to 190 million
detect more cases than culture among males. 
The InPouchTM TV Testis a novel transport
tran sport individuals with trichomoniasis. Prevalence is
higher among women of child-bearing age.
and culture test system which allows the
specimen to be inoculated into a sealed pouch  About 5 to 20% of women and 2 to 12% of
with culture media. Growth can be monitored mr envailnendceeveislo p
 p r ieitshar ger einatf er ctf er deq. H
asseodcciaotuendtw ueingchyer
microscopically directly through the pouch. of sexual intercourse with multiple partners and
This test has a comparable sensitivity to  
Diamond’s modified medium culture.  
with commercial
co mmercial sex workers. Trichomoniasis
Trichomoniasisis
often associated with other sexually transmitted
Treatment  infections. In a study in the United States, 70%
of male partners of women with trichomoniasis
Trichomoniasis can be treated with
were likewise infected and the majority of the
metronidazole or tinidazole 2 g as a single
infected male partners were asymptomatic
dose. The reported cure rates of these drugs
(77%). 
range from 86 to 100%. Sexual partners must
In the Philippines, the prevalence of
 be treated concomitantly to prevent reinfection.
reinfection . trichomoniasis among commercial sex workers
If metronidazole treatment failure occurs and varies with the method of diagnosis used,
reinfection is ruled out, a seven-day regimen of from 15% in studies using only microscopic
500 mg metronidazole three times a day may 
examination of vaginal swabs to 37% in studies  
 bgedcaoilny sdidoesr eef do.r I5f  ediatyhser of theiisthr eer gimmeetnr of naiidlsa,zaol2e using culture. One study surveyed 421 male
sex workers and there were no positive cases
cases
or tinidazole can
metronidazole be used.
remains In pregnancy,
the drug of choice for among them based on microscopy (Table
2.3). Local isolates of T. vaginalis have been 
trichomoniasis. 

Table 2.3. Selected Philippine studies on trichomoniasis

Population(n)
 Amongwaitresses/hostesses:15.0%
 

56  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

characterizedd molecularly showing low genetic

characterize Gumbo FZ, Duri K, Kandawasvika GQ,
 polymorphism.   Kurewa NE, Mapingure MP, Munjoma
It is relevant to discuss trichomoniasis in the MW, et al. Risk factors of HIV vertical
context of HIV.In Zimbabwe
Zimbab we and South Africa, transmission in a cohort of women
trial participants diagnosed with trichomoniasis under a PMTCT program at three peri-
were more likely to test positive for HIV in their urban clinics in a resource-poor setting. J
next visit. Perinatal transmission of HIV was   Perinatol. 2010;30(11):717 – 2
23.
3.
likewise more likely if the mother had vaginal Jueco NL, Araneta CA, Tadina EG.
infections.  Epidemiology of Trichomonas vaginitis
Prevention and Control 
among selected group of women in Manila.
Acta Med Phili
Philipp.
pp. 1988;24(3):85 – 6
6.. 
Prevention is best achieved by reducing Mavedzenge S N, Pol BV
, Cheng H, Montgomer y
the risk of exposure. Limiting the number of ET, Blanchard K, de Bruyn G, et al.
sexual partners, and proper use of protective Epidemiological synergy of Trichomonas
devices such as condoms and spermicidal foams vaginalis and HIV in Zimbabwean and
may help prevent infection. To prevent “ping- South African women. Sex Transm Dis.
 pong” or
 pong”  or recurrent infections, there should 2010;37(7):460 – 6
6..
 be simultaneous
simultaneo us treatment of sexual partners.
partn ers.  Monzon OT, Santana RT, Paladin FJ, Bautista
Prompt follow-up of patients and their contacts, A, FajutaganaL, Eugenio S. The Prevalence
Prevalen ce
as well as health and sex education about of sexually transmitted diseases (STDs) and
venereal disease are also important.   human immunodeficiency virus (HIV)  
References  iJnM ecictir o bn iaom
f ec li  ppisin. o19se9x1;w2o0r :k4e1 – 
l Ionf gecFt iD r s4. P. hil

Arambulo
JC. APV,
PV, Cabrera BD,
comparative Osteria
OsteriofaTrichomonas
study TS, Baltazar Riveracharacte
WL, Ong
O ng VA, Masalun
characterizationMasa
rization lunga
ga MC.
MC. Molecular
of Trichomonas vaginalis  

vaginalis prevalence in Filipino women. isolates from the Philippines. Parasitol Res.  

Southeast Asian J Tro
Tropp Med Public Health.
Heal th. 2009;106(1):105 – 10.
10.
1977;8:298.  Schwebke JR, Burgess D. Trichomoniasis. Clin
Basaca-Sevilla V, Cross JH, Alquiza L, Lacap T. Microbiol Rev. 2004;17(4):794 – 803.
803. 
Prevalence of Trichomonas
Trichomonas vaginalii  ssn some Spence MR, Harwell TS, Davies MC, Smith
S mith JL.
Filipino women. Southeast Asian J Trop The minimum single oral metronidazole
Med Public Health. 1986;17(2):194 – 6
6..  for treating trichomoniasis: a randomized,
Beaver PC, Jung RC, Cupp EW. Clinical  blinded study
study.. Obstet Gynecol. 1997;89(5):
1997; 89(5):
 parasitology.
 parasitology. 9th ed. Philadelphia:
Philadelphia: Lea and 699 – 703.
703. 
Febiger; 1984.  Van der Pol B. Trichomonasvaginalis infection:
Belding DL. Textbook of parasitology. New the most prevalent nonviral sexually
York: Appleton-Century Crofts; 1965.   transmitted infection receives the least
Cudmore SL, Delgaty KL, Hayward-McClelland
Hayward-McClelland  public health attention. Clin Infect Dis.
SF, Petrin DP, Garber GE. Treatment   2007;44(1):23 – 55..
of infections caused by metronidazole- Wendel KA, Workowski
Workowski KA. Trichomoniasis:
Trichomoniasi s:
challenges to appropriate management.
resistant Trichomonas
Microbiol vaginalis . Clin
Rev. 2004;17(4):783  – 9
93.
3.  Clin Infect Dis. 2007;44(Suppl 3):123 – 99.. 
Gerbase AC, Rowley JT, Mertens TE. Global
epidemiology of sexually transmitted
diseases.. Lancet. 1998;351(Suppl 3):2 – 4.
diseases 4. 
 

CHAPTER 2: Protozoan Infections   57 

Non-Pathogenic Flagellates 
Juan Antonio A. Solon  

Trichomonashominis Diagnosis is made by swabbing the tartar

 between the teeth, the gingival margin, or
s with other Trichomonas
Trichomonasspecies, T. hominis tonsillar crypts.  
A 
 

occurs only as a trophozoite which has a   Pulmonary trichomoniasis has been  

 pyriform
 pyrifor m shape and measures
measures 7 to 13 µm. It has  reported among those with underlying
un derlying chronic
five  anterior flagella and a posterior flagellum
flagellum    pulmonary disease, entering the lungs most
 projectingg from an undulating
 projectin undulat ing membrane. The  probabl y by aspiration.
 probably aspirati on. The parasite is probabl
probablyy
cytostome and the nucleus are situated at the unable to cause disease on its own. The presence
anterior end. An axostyle extends from anterior of bacteria most probably allows it to proliferate
to posterior along the mid-axis. Transmission  profusely.
 profusel y. In most ofthese cases, treatment
treatment with
occurs rapidly through fecal contamination of metronidazole results in rapid improvement.
imp rovement. 
food and drinks.
Its habitat is the cecal area of the large Cho
i 
l mas
 x
t i mesnil 
i 
intestine of human and other primates. It is non-
invasive. Trophozoites pass out with diarrheic This organism inhabits the cecal region
stools. The prevalence in the Philippines is less  of the large intestine. It has well-defined
trophic and cystic stages. The trophozoite is
than 1%. asymmetrically pear-shaped as a result of a
spiral groove extending through the middle half
  Trc
i 
i homonastenax  of the body. Its size ranges from 6 to 10 µm.
Trichomonas tenax is a pyriform flagellate The characteristic boring and spiral forward
which has been observed only in the trophozoite movement is made possible by the three anterior
stage. It measures 5 to 12 µm ,and is smaller and free flagella and a more delicate one within the
more slender than T. vaginalis. It has four free  prominent cytostome. 
equal flagella
flagella and
 and a fifth
fifth one
 one on the margin of The cyst is pear- or lemon-shaped, broadly-
an undulating membrane which does
do es not reach rounded at one end and somewhat bluntly-
the posterior end of the body, and lacks a free conical at the other end which has a knob-like
 posterior extension.
extensi on. It has a single nucleus and  protruberance that is visible occasionally. 
a cytostome. The organism multiplies by binary Internally, hematoxylin and eosin stained films
fission and thrives on the microorganisms found clearly demonstrate the single large vestibular
in its environment.   nucleus and the cytostome, which is almost 

r omEtx p
f r 
osur oeur thes,ukltisssf inr ogm
he m ,  odr   r co p onr auyse  of
letms p
om as long as the encysted or ganism. Good
 pr e par ations r eveal a fi br il on either side of   the
contaminated dishes and drinking glasses.   cytostome.
Trichomonas tenax is a harmless commensal of Transmission occurs through ingestion
the human mouth, living in the tartar around of cysts in food and drinks. Prevalence in
the teeth, in cavities of carious teeth, and in the Philippines is less than 1%. This is a
necrotic mucosal
mucos al cells in the gingival
gingiv al margin.sIt
margin.sIt harmless commensal diagnosed by microscop
microscopic
ic
is quite resistant to changes in temperature and examination of feces and demonstration of
will survive for several hours in drinking water.  either trophozoites or cysts. No treatment is 
 

58  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

indicated. Preventive and control measures Southeast Asian

A sian J Trop
Trop Med Public
Publi c Health.
include improved sanitation and personal
p ersonal 1981;12(1):12 – 8
8..
hygiene.  Carney WP, de Veyra VU, Cala EM, Cross
JH. Intestinal parasites of man in
References 
Bukidnon, Philippines, with emphasis on
Beaver PC, Jung RC, Cupp EW. Clinical schistosomiasis. Southeast
Southeast Asian J Trop
 parasitology.
 parasitolo gy. 9th ed. Philadelpha:
Philadel pha: Lea and Med Public Health. 1981;12(1):24 – 9 9.. 
Febiger; 1984.  Cross JH, Banzon T, Wheeling CH, Cometa
Carney WP, Banzon T, de Veyra VU, Dana E,  H, Lien JC, Clarke R, et al. Biomedical
Cross JH. Intestinal parasites of man in survey in North Samar
Sa mar Province,
Province,Philippine
Philipp ine  
 NorthernBohol, Philippines,
Philippines, with emphasis Islands. Southeast
Sout heast Asian J TropMed Public
Publi c
on schistosomiasis. Southeast Asian J Trop Health. 1977;8(4):464 – 75.
75.
Med Public Health. 1980;11(4):473 – 9
9..  Hersh SM. Pulmonary trichomoniasis and
Carney WP, Banzon T, de Veyra VU, Papasin Trichomonas tenax . J Med Microbiol.
MC, Cross JH. Intestinal parasites of 1985;20(1):1 – 10.
10.
man in Oriental Mindoro, Philippines, Lewis KL, Doherty DE, Ribes J, Seabolt JP,
with emphasis on schistosomiasis.   Bensadoun ES. Empyema caused by
Trichomonas. Chest. 2003;123(1):291 – 2
2.. 
 

CHAPTER 2: Protozoan Infections   59 

Coccidians 
Winifreda U. de Leon  

he coccidian parasites are the largest group reported that the only species that infect
of apicomplexan protozoa falling under   mammals was C. parvum and was believed 
Class Conoidasida. Coccidia is a subclass of to be the species infecting humans. However,
T 
microscopic, spore-forming, single-celled
obligate intracellular protozoan. Members
molecular tools, especially DNA analysis,
described the existence of another species,
of Phylum Apicomplexa are provided with  ium hominis found mainly in
Cryptosporidium
Cryptosporid
a cluster of secretory organelles made up of humans.
rhoptries, micronemes, and polar rings with
Parasite Biology 
microtubules. In some species, a conoid may
 be found within the polar rings as well. The All stages of development
development are completed in
secretion allows the parasite to enter the host the gastrointestinal tract of the host. Oocysts
cell.  when passed out are already infective. Oocysts
Coccidians infect the intestinal tract of  produced by C. hominis are found in the feces
most phyla of invertebrates and all classes of of humans and other animals. The oocysts are
vertebrates including humans. They fall under round and measure 4 to 5 µm in diameter.
Order Eucoccidiorida Suborder Eimeriorina.  Each oocyst contains four sporozoites, which  
onhee odf istehaesemcaa jloler d pcr o bccleidmios siins iasnr iemcoalgnf aizr m
T edinags aTr he p
e or eosceynstt aist itnhf eectitm
ioeusof a p sahgeninintogetshteedf e, ctehse.
ndasw
and in zoo management. Among humans, sporozoites attach to the surface of epithelial
they are considered to be opportunistic in cells of the gastrointestinal tract. The sporozoit
s porozoites
es
immunocompromised and immunodeficient develop into small trophozoites and become
individuals.. Species
individuals Speci es with medical and
a nd evterin
evterinary
ary intracellular but extracytoplasmic, and attach
significance includeCryptosporidium, Cyclospora, to the brush borders. The trophozoites divide
Cystoisospora , Sarcocystis , and Toxoplasma.   by schizogony
schizogo ny producing
produci ng merozoites
merozoit es that infect
In the coccidian life cycle, there is an other cells. Macro- and microgametocytes
microgametocytes are
alternation of sexual and asexual multiplication. eventually produced, and the macrogamete  
It is typically characterized by three sequential is fertilized by the microgamete to produce
stages, namely: sexual cycle or sporogony a zygote. There are two types of oocysts
 producin g oocysts, asexual cycle or schizogony
 producing schizogo ny resulting from the zygote: the thin-walled
(merogony) producing merozoites (meronts), and the thick-walled oocysts. The thin-walled
and gametogony resulting in the development
d evelopment  oocysts infect other enterocytes thus resulting
of male (micro) and female (macro) gametocytes
gametocytes in autoinfection, which is possibly responsible
(gamonts). The complexity in the life cycles of for the chronicity of the infection among the
coccidians is a challenge in terms of taxonomy.  immunocompromised. On the other hand, the
thick-walled oocysts are passed out with the
Cryptospord
 i u
i mhom n
i i 
s
  feces
whichthat may contaminate
are ingested food
by the same and water,
or another host
There are several species of Cryptosporidium
Cryptosporidium
(Figure 2.8).
that are currently recognized. It was initially  
 

60  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

CHAPTER 2: Protozoan Infections   61 

Pathogenesis and Clinical Manifestations   Treatment 

Cryptosporidiosis hominis was not well There is presently no acceptable treatment

recognized prior to the occurrence of acquired for cryptosporidiosis. Nitazoxanide, however,
immune deficiency syndrome (AIDS). In   has been reported effective in preliminar
preliminaryy trials.
the immunocompetent host, the disease
di sease may Bovine colostrum as well as paromomycin and
 present as a self-li
sel f-limiting
miting diarrhea
di arrhea lasting
last ing for   clarithromycin have shown promise in treating 
 pain, anor exia, f ever , nausea,  and w b
2 t o 3 wee ks , a nd less com m o ly, aeidghom
t  lionsasl. sveavluer 
ee. Idniaar dr dhietai.o nAtzoithchr oemyocthiner m  baolsdoy bfleuiodf
a payy,  b
In immunocompromised persons, the diarrhea replacement and symptomatic treatment are
 becomes more severe, progressive, and may recommended for both the immunocompetent
 become life-threatening.
life-threatenin g. The bile duct and gall and immunosuppressed patients.
 bladder may become heavily infected and lead to Epidemiology 
acute and gangrenous cholecystitis. Respiratory
infections lead to chronic coughing, dyspnea, Cryptosporidiosis hominis has a universal
 bronchiolitis, and pneumonia.
pneumonia.   distribution with infections reported worldwide.
The villi of the intestines become blunted Epidemics are unusual in North America,
and there is infiltration
infiltration  of inflammatory
inflammatory cells
 cells although there was a report of an epidemic
into the lamina propria and elongated crypts. involving over 400,000 cases in the state  
There may be varying degrees of malabsorption of Wisconsin in the United States. This
and excessive fluid loss in immunocompromised epidemic was attributed to the use of a faulty
 patients. Death may occur in disseminated water purification system. Most epidemics
infections.  are associated with water, and in many cases,
the water was contaminated with calf feces.
Diagnosis  Cryptosporidium parvum of calves has been
There are several methods of stool reported to cause infection among veterinary
examination that will reveal C. hominis oocyst. attendants and visitors in dairy farms and
an d
Sheather’s sugar flotation and the formalin
Sheather’s sugar  petting zoos. 
ether/ethyl acetate concentration technique Swimming in contaminated recreation
are commonly used. Kinyoun’s modified
modified acid- water may result in accidental ingestion of
fast stain is routinely used with the oocysts   infective oocysts. Swimming pool disinfection
appearing as red-pink doughnut-shaped
doughnut-shaped circular with 3 to 5 mg/L of chlorine does not kill
organisms in a blue background. Intestinal the oocysts. The most common mode of
 biopsy material may also be examined under a transmission is from one person to another.
light microscope and stages of the parasite can Infected food handlers may likewise transmit
 be seen at the microvillus
microvil lus region of the infected   oocysts during handling of beverages, raw  
ethnet p r eodnf ar or yminthvoels p
er aor caystiete.  Imnacya bsees r oef c pouvlem veumtuenmt, vr aew a bnle
ge.tU s, an ot er   oo that may  be  eaten
 pasteudr izedh mif lk, df r 
r eshly pr essed a p ple
although transbronchial and broncheo-alveolar broncheo-alveolar cider, potato salad, and sausages were found
lavage can yield a better result.  sources of infection. Nosocomial infections have
Indirect fluorescent antibody, enzyme also been reported among health workers caring
immunoassay, and DNA probes specific for C. for AIDS patients. 
hominis have been developed. Acid-fast staining In developing countries, prevalence
is probably the quickest and cheapest method ranged from 3 to 20%. The prevalence in the
of diagnosis.  Philippines has been reported to be low at 2.6%. 
 

62  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

A study done in San Lazaro Hospital attempted gametes. The microgametes fertilize the
to describe Cryptosporidium among diarrheic macrogametes to produce oocysts, which are
 patients and reported a prevalence of 8.5%,  passed out with feces when the host cells are
while a study done in the Philippine General sloughed off from the intestinal wall. The
Hospital on diarrheic patients had a much lower oocysts undergo complete sporulation within
 prevalence at 1.7%. 7 to 12 days in a warm environment. 
It is assumed that the oocyst is the infective  
Prevention and Control  stage and when ingested, the sporozoites are
Water-borne transmission is the most released and enter intestinal cells to go through
common source of cryptosporidiosis.   schizogony and gametogony. The different  
Chlorination does not affect the parasite. The developmental stages of the parasite may be
synergistic effect of multiple disinfectants and found in the intestinal tissue (Figure 2.9).  
combined water treatment processes may reduce  Pathogenesis and Clinical Manifestations  
C. hominis oocysts in drinking water. Natural
water and swimming pool water should not be Initial symptoms include malaise and low
swallowed. Contamination of drinking water by grade fever, which may occur 12 to 24 hours
human and animal feces should be prevented.  after exposure. Chronic and intermittent watery
diarrhea occurs early in the infection and may
Cyco
l sporacayetanenss
i alternate with constipation. The diarrhea
 
may continue for 6 to 7 weeks with six or
When firs t associated with diarrhea,
more stools per day. Other symptoms such as  
this organism was thought to be a  
member of cyanobacteria because it f a b r eaxiina, wf leaitguhlet nlocses,,  b
atdigoume,inanalo p nalouasteian, gv,om
anidting,
showed photosynthesizing organelles and  
autofluorescing particles characteristic of   the
the dyspnea
has beenmay develop.
found D-xylose
to develop in malabsorption
malabsorptio
some of then
 blue green algae.   patients. Infections
Infection s are usually
usuall y self-limiti
self -limiting
ng
Parasite Biology  and immunity may result with repeated
infections. No death has been associated with
Cyclospora cayetanensis was srcinally cyclosporidiosis. 
called a cyanobacterium-like body (CLB)
 but upon careful study, it was found to be Diagnosis 
a coccidian parasite. Similar to the other Direct microscopic examination of fecal
intestinal coccidians, the life cycle begins with smears under high magnification (400x)  
the ingestion of sporulated oocyst, which is recommended. Various concentration
contains two sporocysts with two sporozoites techniques and acid-fast staining (Kinyoun’s
each. The released sporozoites invade the  stain) are also useful. Oocysts are auto-
epithelial cells of the small intestines, although fluorescent and under fluorescent microscopy,
the site of predilection was found to be the   they appear as blue or green circles depending
 jejunum. Multiple fissions of these sporozoites on the filter  (365-450
 (365-450 DM). This technique
take place inside the cells to produce meronts, is useful for screening. Safranin staining
which contain 8 to 12 merozoites during the
first generation,
first generation, and only four merozoites in and microwave
 polymerase chain heating
reaction are
(PCR)
(PCR)also helpful.has
technique hA
as
the second generation. Some of the merozoites  been developed
developed to differentiate
differentiate Cyclospora from
develop into male (micro) and female (macro)   closely related  Eimeria species. 
 

CHAPTER 2: Protozoan Infections   63 

 

64  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Treatment  followed to prevent the infection. Only water

that has been subjected to adequate treatment
The disease is self-limiting and treatment  procedures should be consumed. In most
is not necessary if the symptoms are mild. If
endemic areas, boiling water seems to be the best
 pharmacol ogic treatment is warranted,
 pharmacologic warrant ed, the only method since chlorination is not effective. Fruits
effective drug is trimethoprim-sulfamethoxa
trimethoprim-sulfamethoxazole
zole and vegetables should be washed with clean
160/800 mg twice daily for 7 days. There is   water, but it would be prudent to avoid eating 
toolear latteer nsautlef atm
n tieonctysstasr eduisna pa b
r eeatthmoexnatzoif le p. aO to
 pleear  fruits and vegetables that have been exposed
from the stools a few days after treatment. to natural untreated water. In Guatemala, it
was believed that raspberries were exposed to  
However, recurrence of symptoms was noted oocysts in places where creek water was used
in about 40% of patients within 1 to 3 months
to dilute insecticides sprayed on the plants.
 post treatment. 
Similarly, in Nepal it is believed that cabbage
Epidemiology   became contaminated
cont aminated when watered
water ed with raw
ra w
irrigation water.
Cyclosporidiosis has been described in
many countries, with epidemics reported in Cystoisosporabelli
 Nepal, Peru, Haiti, and the United States.
Infections were reported to appear in Nepal in This is the causative agent of a medical
late May and June and continued until October condition affecting the small bowel called
to November, the rainy season. Most cases in cystoisosporiasis. The other known species
 Nepal were reported in expatriates
expatriat es and tourists,
touris ts,  Isospora
 Isospora hominisis now taxonomically grouped
hominis
and more recently in Nepali children and adults. under the genus Sarcocystis . 
In Peru, infections are commonly reported in
children, while in Haiti, infections affect more Parasite Biology 
homosexual males. Epidemics involving over The sporulated oocyst contains two
1,000 persons were reported in the United sporocysts each containing four sporozoites
States in 1996 and 1997. Raspberries imported (infective stage). When ingested via contaminated
from Guatemala were incriminated in the water or food, the sporozoites excyst in the small
infections in the United States. Leafy vegetables intestine releasing sporozoites, which penetrate
have been found to contain oocysts in Peru and the epithelial cells, thus starting the asexual
 Nepal, while
whi le lettuce and
an d basil-pesto
basil -pesto salad has stage or the schizogonic phase of the life cycle
 been incriminated in other cases in the United (Figure 2.10). The sporozoites develop in the
States. Contaminated water is thought to be the epithelial cell to form a schizont, which ruptures
main source of infection. No animal reservoirs the host epithelial cell liberating merozoites into
have been found and, therefore, cyclosporidiosis  the lumen. These merozoites will then infect 

ser 
idsi p ier  pedinems,aainsltyudasy  oa f hduiamrr ahneic
aessee. nIntlythceoPnshiidl p new epithelialincells
reproduction the and the process
intestine of asexual
continues.
continue s. This 
stools from children in 2005 at the College of  process may continue for weeks or months.
Public Health, University of the Philippines Some of the merozoites undergo gametogony
Manila, revealed a prevalence of 3.1% using to produce macrogametes and microgametes
safranin staining heated in a microwave.   (sexual stages), which fuse to form a zygote that
eventually matures to form an unsporulated
Prevention and Control 
oocyst. Sporulation usually occurs within 48
Since the direct source of C. cayetanensis  hours after passage with the stool. 
is unknown, good sanitary practices should be  
 

CHAPTER 2: Protozoan Infections   65 

 

66  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Pathogenesis and Clinical Manifestations   Other concentration techniques that can also
 be used include zinc sulfate and sugar flotation.
Amongthe immunocompetent,infection
infectionis Oocysts are thin walled, transparent, and ovoid
generally asymptomatic or may presentas a self- in shape. They appear as translucent, oval
limiting gastroenteritis.However,
gastroenteritis.However, in more severe structures measuring 20 to 33 µm by 10 to
infections, severe diarrhea and fat malabsorption 19 µm. Alternatively, oocysts can be seen in a
can occur. Symptoms include low-grade fever,  fecal smear stained by a modified Ziehl-Neelsen 
anor exia, vwoem cea.laSitsoe,ols
igihtitnlgo,ssg,enaner dalfl batoudlyenm method, where they stain granular red color
usually contain undigested food, mucus, and against a green background. Phenol-auramine,
as well as iodine staining of the specimen  
Charcot-Leyden crystals.  
can help visualize the organism. Acid-fast
Infection in immunocompromised
stain, such as Kinyoun’s stain or an auramine-
individuals ranges from a self-limiting enteritis
individuals rhodamine stain, is also useful. A considerable
to severe diarrheal illness resembling that of amount of stool may have to be examined
cryptosporidiosis,, giardiasis or cyclosporiasis.
cryptosporidiosis cyclosporiasis.  because oocysts in the samples are often few in
Mucosal bowel biopsy may reveal flattened
number. Charcot-Leyden crystals may be seen
mucosa and damaged villi. Infiltration of the
in the stool specimen. In blood examination,
lamina propria with lymphocytes, plasma cells,  peripheral eosinophilia is common. String
and eosinophils has been reported. However, capsule (Enterotest®) and duodenal aspirate
the mechanism by which the parasite produces examinationss may be of value. Molecular based
examination
these lesions is still not clear.  
techniques may prove useful as an additional 
Diagnosis  diagnostic tool.
C. belli Treatment 
in theThe oocysts
feces of microscopy
by direct may orbeformalin-
detected
Asympto matic in fections may be
ether/ethyl acetate concentration (Plate 2.13).   managed with bed rest and a bland diet,
while symptomatic infections, such as those
t hose
occurring in AIDS patients, can be treated with
trimethoprim-sulfamethoxazole
trimethoprim-sulfamethoxaz ole 160/800 mg
four times per day for 10 days, then two times
 per day for 3 weeks. Combination
Combin ation therapy with
 pyrimethamine
 pyrimetham ine and sulfadiazine for 7 w
weeks
eeks has
also been
b een used successfully. 
Epidemiology 

Unlike the other coccidians, humans are

the only known hosts of C. belli , which has
a worldwide distribution. It is however more
common in tropical and subtropical countries
with poor sanitary conditions. The actual

incidence
C.   belli hasofbeen
cystoisosporiasis
tagged as theiscausative
not known but 
agent
Plate 2.13. Immature oocyst of Cystoisospora of diarrheal episodes in day care centers and
belli recovered
recovered from stool sample,  
showing a single sporoblast
mental institutions. The disease is common
(Accessed from www.dpd.cdc.gov/dpdx)
from www.dpd.cdc.gov/dpdx)  among patients with AIDS. In Africa, 2 to 3%  
 

CHAPTER 2: Protozoan Infections   67 

of those with AIDS were infected; in South Microsporidia, Isospora

 Isospora and Cyclospora . Ann
America, 10%, and in Haiti and Africa, a range Intern Med. 1996;124:429 – 441.
441.
of 7 to 20% was observed. The disease has also Heyworth MF. Parasitic diseases in
 been reported
report ed among those with
wi th lymphoma,
lymp homa, immunocompromised hosts,
leukemia, and organ transplants. Considered cryptosporidiosis, isosporiasis and
endemic are the following: Africa, Australia, strongyloidiasis.
strongyloidiasis. Gastroenterol Clin
C lin North
the Caribbean Islands, Latin America, and   Am. 1996;25:691 – 707.
707. 
Southeast Asia. Cystoisosporiasis has been Hoepelman IM. Human cryptosporidiosis. Int
reported in both adults and children, but severe J STD AIDS. 1996;7(suppl)l:28 – 3
33.3. 
diarrhea is common among infants. Both sexes  Jueco NL, Belizario VY, Jr., de Leon WU,
were found susceptible to infection. Tan-Liu N, Bravo LC, Gregorio GV.
Cryptosporidiosis among selected patients
Cryptosporidiosis
Prevention and Control 
in the Philippine General Hospital. Acta
Cystoisosporiasis can be prevented by Med Philipp. 1991;27:244 – 247.
247. 
following good sanitary practices, thorough Lindsay DS, Dubey JP, Blagburn BL. Biology
washing and cooking food, and drinking safe of Isospora spp. from humans, non human
 Isospora
water.   primates and domestic animals. Clin
Microbiol Rev. 1997;10:19 – 34.
34.
References 
MacKenzie WR, Hoxie NJ, Proctor ME,
Ackers JP. Gut Coccidia
Coccidia — 
 —    Isospora ,  Gradus MS, Blair KA, Peterson DE, et
Cryptosporidium , Cyclospora and Sarcocystis.  al. A massive outbreak in Milwaukee of  

n  inMG
Br enSneam r oaincPtehsetr Dsoins.  1D9W
K a,stM 97,;8P(a1l)m:3e3r  – J4, 4. tr alyn. N
thr ough the Pu blicinwf aetcetr iosnup p
C r  y pt o s po
 por id ium smiEttnegdl J

Keystone
diarrhea. JS. Cyclosporiasis:
CMAJ. a new cause
1996;155(9):1293 of  Marshall
 – 1296.
1296.
Med. 1994;331:161.
MM, Naumovitz D, Ortega, Sterling
Cross JH, Serchand JB, Sharma P, Escheverria   CR. Waterborne protozoan pathogens.
P. Cyclosporiasis at the Kanti Children’s Clin Microbiol Rev. 1997;10:67 – 8
85.
5. 
hospital in Kathmandu, Nepal: a cursory Millard PS, Gensheimer KF, Addis DG, Sosin
survey. J Trop Med Parasitol. 1997;20:30 –   DM, Beckett GA, Houck-Jankoski A, 
32.  et al. An outbreak of cryptosporidiosis
Duszynski D, Upton S, Couch L. The coccidia from fresh-pressed apple cider. JAMA.
of the world 1995, a compilation of the 1994;272:1592. 
national science foundation a database Orenstein JM. Isosporiasis. In: Connor D.
of known species of coccidian [Internet]. et al, editors. Pathology of Infectious
 New Mexico and Kansas: University of Diseases. Connecticut: Appleton and
 New Mexico and Kansas State University;
Universi ty; Lange, Norwalk; 1997. p. 1185 – 9
90.
0. 
1995 [cited 2009 Mar 1]. Available from Ortega YR. Cyclospora species a new protozoan
protozoan
http://www.k-state.edu/parasitology/  pathogen of humans. N Eng J Med. 1993;
worldcoccidia/. 328:1308 – 1312.
1312.
Fayer R.Cryptosporidium and cryptosporidiosis.
cryptosporidiosis. Ortega YR, Sanchez R. Updates on Cyclospora
Florida:
 p. 251.  CRR Press, Boca Raton; 1997.
cayetanensis
Clin - a food
Microbiol and
Rev. water-borne parasite.
2010;23(1):218  – 234.
234. 
Goodgame RW. Understanding intestinal Rose JB. Environmental ecology of  
spore forming protozoa: Cryptosporidia ,  Cryptosporidium and Public Health
 

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Implications. Annu Rev Public Smith HV, Rose JB. Water borne
Health.1997;18:135 – 161.
161. cryptosporidiosis:
cryptosporidiosis: current status. Parasitol
Serchand JB, Cross JH, Jimba M, Serchand M, Today. 1998; 14:14 – 2
22.
2. 
Shresta MP. Study of Cyclosporacayetanensis
Cyclosporacayetanensis Soave R.Cyclospora an overview. Clin Infect Dis.  
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1999;30:58 – 63.
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261. 
 

CHAPTER 2: Protozoan Infections   69 

Toxop a
l smagond ii  

oxoplasma gondii is a coccidian that belongs into a tachyzoite (Plate 2.14). Tachyzoites are
to the Phylum Apicomplexa. It is a parasite   found during the initial and acute stage of the  
that has a worldwide distribution and that infection, but as host immunity to the parasite
infects humans and many species of animals.  is developed, the fast multiplying tachyzoites
Parasite Biology 
give rise to slow multiplying bradyzoites that
form cysts. Only these two stages are present 
The infective stages include the tachyzoite, in humans and other animal intermediate
the bradyzoite, and the oocyst. The complete hosts. Asexual multiplication is by a variation
life cycle occurs only in the members of the cat of binary fission
fis sion call
called
ed endodyogeny.
endody ogeny. Th is  is
This
family (Felidae), which serve as definitive hosts. characterized
character ized by the formation of the plasma
It follows a typical coccidian life cycle consisting membrane by the two new daughter parasites,
of schizogony, gametogony, and sporogony in even before the division of the nucleus. Cells
Cells
the intestinal epithelium. The extraintestinal in which endodyogeny occur eventually burst,
stages are the asexual stages: tachyzoites and thus liberating trophozoites that invade other
 bradyzoites.  cells. It is possible that tachyzoites can be
be
In the intestinal epithelium of the cat, transferred from one person to another by  

dif ef r eor zeonittieastemin
m lyic(r sochgaizmogeotoncyy)teasnadntdhen
ipm
ultto  p gcar ann buelotcr yatnes bf elr or oed  f tr oanmsf uthsieo n.ewTlaychinyf zeocitteeds
macrogam
macrogametocytes
etocytes (gametogony).
(gametogo ny). Fertilization mother to the fetus during the first
first trimester
 trimester
of the macrogamete by the microgamete gives of pregnancy by passing through the placental
rise to an oocyst. The oocyst is ovoidal in shape,  barrier. Tachyzoites and bradyzoites can be
has a thin wall, and measures 10 to 13 µm by transferred by organ transplant especially bone
9 to 11 µm.  marrow, and bradyzoites can be acquired by
These oocysts are passed out with the feces eating meat of infected animals.  
of the cat in the unsporulated stage. These can The trophozoite measures 4 to 8 µm
 be ingested
ingeste d together with contaminated
contamin ated food in length, 2 to 3 µm width. It is crescent-
or water by another host. The oocysts complete shaped with a pointed anterior and a rounded
sporulation within three to four days. Inside  posterior end. Organelles, such as rhoptries
the mature oocyst, two sporocysts are formed, and micronemes, which are associated with
each having four sporozoites. When the mature cell penetration, are found in a short conoid
oocyst reaches the intestine of the new host, it on the anterior end. A spherical nucleus is 
excysts and releases four sporozoites which can found in the posterior end. In the
th e infected
 penetrate the lamina propria. The parasites macrophage, the parasites prevent the fusion of
gain entry to the lymphatics
ly mphatics then spread to the the parasitophorous vacuole that contains the
different organs, tissues, and fluids of the body  parasites, with the lysosome and are, thus, not
(Figure 2.11). is an intracellular parasite,
Toxoplasma killed by the lysozyme.
 proliferating Pseudocysts
tachyzoites are seencontaining
in tissue
which infects different kinds of nucleated cells sections taken from patients suffering from
including macrophages. Following the entry acute infection. These do nothave well-formed 
of the sporozoite into a new cell, it transforms   walls unlike cysts containing many bradyzoites 
 

70  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Figure 2.11. Life cycle of Toxoplasmagondii  

(Accessed from www.dpd.cdc.gov/dpdx)
from www.dpd.cdc.gov/dpdx) 

that are seen during chronic infections. Cysts

C ysts
are found in muscles and in the central nervous
system. 
Pathogenesis and Clinical Manifestations  

Toxoplasmosis
Toxoplasmosis is commonly
commonly asymptomatic
as long as the immune system of
o f the patient is
functioning well. Many surveys have shown
the presence of antibodies in a large portion
of the population, although the proportion of
 patients exhibiting characteristic symptoms of
Plate 2.14. Toxoplasmatachyzoites
toxoplasmosis is very low. Once stimulated,
(Courtesy of the Department of Parasitology,
Parasitology, the immune system quickly responds to the
UP-CPH)   parasites, which, in turn, adapt by transforming
transfor ming  
 

CHAPTER 2: Protozoan Infections   71 

into bradyzoites that are protected by a cyst antibodies against T. gondii. A seroconversion
wall and proliferate at a slower rate. Cysts to a positive titer or a four-fold increase in titers
can be found in the brain, skeletal and heart is indicative
indicati ve of an infection.
infection.The Sabin-
Sabin-Feldman
Feldman
muscles, and retina. Clinical manifestations methylene blue dye test is very sensitive and
 become apparent when the immune system specific but it requires the maintenance of
is suppressed as in old age, drug-induced   live organisms in the laboratory. High titers
immunosuppressionafterorgan transplantation,  (>1,024), although usually indicating an acute 
or in the case of AIDS. More often, symptoms infection, may also be seen in chronic cases,
appear when there is relapse of chronic hence the need for IgM antibody detection
infections as a result of a suppressed immune   through either the IgM indirect fluorescent 
system rather than as a response to an acute antibody technique or through a double
infection. Among the immunocompromised sandwich IgM enzyme immunoa say. Handlin
Handlingg
 patients, the most common manifestation is of live trophozoites may result in accidental
encephalitis. Myocarditis and focal pneumonia
pneumonia infection of the laboratory personnel. Other tests
have also been reported. It is also possible are the indirect hemagglutination test, indirect
that the immunosuppressed patient acquires fluorescent antibody test, and enzyme -linked
the infection from blood transfusion or immunosorbent assay. Latex agglutination test
organ transplantation. Clinical manifestations is also available. Differentiating pre-existing
include retinochoroiditis, lymphoreticular antibody from passively transferred antibody
hyperplasia with enlargement of the posterior from the mother or antibody related to illness
cervical lymph node, hepatitis,
hepatitis, splenomegaly,
splenomegaly,  is important in the assessment of serological  

f anileur m
 p ighedt.ullar y hemato poiesis, and
e tonig a,ienxtwr aem test r Beesuttletsr .diagnostic assays are being developed
Stillbirth and abortion may result when    because tox oplasmosis
toxoplasmos is has been recognized
recognize d  
mothers acquire the infection during the first as an important disease associated with
trimester of pregnancy. Babies may exhibit AIDS. Polymerase chain reaction (PCR) has
clinical manifestations like chorioretinitis,  been successfully used in the diagnosis of
epileptic seizures, jaundice, hydrocephaly, and toxoplasmosis using samples taken from the
microcephaly. Death of the infected newborn  patient, which
w hich include
incl ude serum, amniotic
amnioti c fluid,
 babies is usually due to anemia with pneumonia.
pneumoni a. cerebrospinal fluid, and broncheoalveolar
There are cases when clinical manifestations lavage, especially
especially in cases where there is
i s very
may not be apparent during the neonatal little amount of specimen available.  
 period, but will appear later in childhood. Most
Treatment 
 babies will harbor the ininfection
fection aand
nd grow up
without any clinical manifestation until such Treatment consists of pyrimethamine
time later in life when their immune system is   (25-100 mg daily) and sulfadiazine (1-1.5 g
suppressed and there is reactivation of chronic four times daily) used in combination for one
toxoplasmosis.  month. These drugs keep the Toxoplasmaunder
Diagnosis 
control but do not kill it. Since pyrimethamine
can lower blood counts in most people, it
Identification
through of of
examination thetissue
parasite can be
imprints  done
stained shouldSulfadiazine
acid). be given together
may with
causeleucovorin (folic
serious allergic
with Giemsa. Tissue sections can be processed reactions like fever and rash, but it can be
and stained with hematoxylin and eosin.
eosin.  substituted with clindamycin. Spiramycin,
Serodiagnostic methods are used to detect   azithromycin, clarithromycin,
clarithromycin, dapsone, and 
 

72  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

atovaquone may also be used. Corticosteroids References 

are sometimes given to prevent occurrence of
hypersensitivity reactions. Prophylaxis with Cross JH, Basaca-Sevilla V. Biomedical surveys
in the Philippines. Manila (Philippines):
trimethoprim-sulfamethoxazole may be given
US Naval Medical Research Unit No. 2;
for the immunocompromised.  
1984. 
Epidemiology  Eduardo SL. Food-borne zoonoses in the
Toxoplasmosis is endemic worldwide in Phu bil p
ili p
cHineeasl.thS.o1ut9h9e1a;s2t2A:1s6ia – n22J .Tr o p
 p  Med
humans and in domestic and wild animals as Frenkel JK, Hassanein KM. Transmission of  
well. Disease due to
t o this parasitic
parasiti c infectionsinot Toxoplasma gondii in Panama: a five -year
manifested except in cases of immune deficiency  prospectivee cohort. Study
 prospectiv cats, 
Study of children, cats,
or suppression. Determination of the t he prevalence rodents and soil. Am J Trop Med Hyg.  
of infection is based on serodiagnostic tests,
1995;53:458.
although these tests are not readily available  
Jackson MH, Hutchison WM. The prevalence
in the Philippines due perhaps to a lack of
and source of Toxoplasma infection in the
demand since clinical toxoplasmosis is not
environment. Adv Parasitol. 1989;28:55 –  
common. According to surveys by Cross and 105.
Basaca-Sevilla,, only 2.4% of the population is
Basaca-Sevilla  Nantulya VM. TrypTect CIATT
CI ATT — a card
seropositive for Toxoplasmagondii
Toxoplasmagondii. Pigs and rats,
indirect agglutination trypanosomiasis test
however, have a higher prevalence of positive for diagnosis of Trypanosomagambiense
Trypanosomagambiense and 
titers for Toxoplasma antibodies at 19% and  
T. rhodesiense infection
infections.
s. Trans R Soc Trop
8.1%, respectively.  Med Hyg. 1997;91:55l  – 
– 553.
553.
Prevention and Control 
 Neva6th
FA,
ed.Brown HW. Basic
Connecticut:BAppleton
asic clinical parasitology. 
& Lange;
Food should be protected from
1944.
contamination with cat feces. Meat and eggs Roberts LS, Janovy J. Foundations of
should be well cooked. Unpasteurized milk
 parasitology. 5th ed. Dubuque: Wm. C.
should be avoided. Pregnant women should
Brown Publishers; 1996.  
avoid contact with cats. Laboratory workers
w orkers World Health Organization. WHO Fact
should be very careful in handling the parasite.  Sheet no. 116. Geneva: World Health
Organization; 1996.
 

CHAPTER 2: Protozoan Infections   73 

Sarcocystisspp.
 Alice Alma C. Bungay, Raezelle
Raezelle Nadine T. Ciro

arcocystis is a genus of intracellular protozoa environment suitable for parasite growth and
reported to infect humans and animals   development. 
worldwide. Infection with this parasite is known Sporulated oocysts and individual
as sarcosporidiosis or sarcocystosis. Species sporocysts can be passed out in the feces of an
 belonging
 belongi ng to this genus infect a wide variety of   infected definitive host. The sporulated oocyst 
animals such as birds, reptiles, and mammals. undergoes sporogony creating two sporocysts.
While majority of the species infect mammals, Once sporogony is complete, the oocyst itself
about a dozen are known to infect snakes.   undergoes lysis, releasing the sporocysts into
This parasite wasfirst
was first  reported in 1843 by the environment. Sporocysts of most species
Miescher as white threadlike cysts in striated measure 15 to 19 µm by 8 to 10µm, and contain
muscles of a house mouse. It was simply referred four sporozoites and a discrete refractile residual
to as Miescher’s
Miescher’s tubules
 tubules until 1899, when the  body. Sporocysts are capable of surviving on
name Sarcocystis miescheriana was proposed to the ground and infecting intermediate hosts
identify the said parasite. Since its discovery, it (Figure 2.12).
has been debated whether Sarcocystis spp. were After oocysts and/or sporocysts are ingested
 protozoa or fungi. The debate was resolved   by a susceptible intermediate host
host (usually 
ownelr ye isntu1d9i6e7d w er  btr haedeylzeocitr eosninmthicer osascr c p
unhden oceyastnsd cinotwestionr e p. T
ighs)e, p s f oromcyinstgs p
 tlhaete p thaes p cyestsm
s tor oth wall
were seen to possess organelles found in other separate, releasing the four sporozoites into
apicomplexan protozoa such as Toxoplasma and the intermediate host’s body. The sporozoites
 Eimeria .  migrate through the gut epithelium and
There are about 130 recognized species eventually enter the endothelial cells in small
under Sarcocystis including S. hominis and S. arteries where they undergo the first two
inis. Humans serve as definitive hosts for
 suihominis
 suihom generations of asexual reproduction (called
the two species, but occasionally, humans can schizogony or merogony). These cycles result
act as intermediate hosts. There is an ongoing in the development of meronts. This stage lasts
revision of the taxonomy of this genus, and it is about 15 to 16 days after ingestion of sporocysts.
 possible that all the currently
currently recognized species Merozoites emerge from the second generation
may be fewer or may in fact be a single species meronts and enter the mononucleate cells
that can infect multiple hosts.  where they develop. Subsequent generations of
merozoites develop in the direction of blood  
Parasite Biology  flow to arterioles, capillaries, venules, and
Sarcocystis can take several forms. The veins throughout the body. The third asexual
simplest form is called a zoite. It is a banana- generation appears as multinucleate schizonts
shaped cell, with a pointed anterior end, also in capillaries throughout the body. Merozoites
Merozoites 
known as the apical
micronemes, complex,and
micropores, which possesses
rhoptries,  from
in thethis generation
muscles, form sarcocyst
initiating metrocytesformation.
and encyst 
and believed to be associated with host cell Sarcocysts begin as unicellular bodies
 penetration and creation of an intracellular   containing a single metrocyte. Through  
 

74  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

CHAPTER 2: Protozoan Infections   75 

repeated asexual multiplication, numerous anorexia, nausea, abdominal pain, distension,

metrocytes accumulate and the sarcocyst diarrhea, vomiting, dyspnea, and tachycardia.
increases in size. As sarcocysts mature, the All symptoms were transient and lasted about
small, rounded, non-infectious metrocytes give 36 hours. 
rise to infectious, crescent-shaped bodies called Sarcocystosis has also been associated with
 bradyzoites.
 bradyzoit es. About two and a half months after acute fever, myalgias, bronchospasm, pruritic
infection, sarcocysts are already mature and are  rashes, lymphadenopathy, subcutaneous 
able to infect the definitive host.   nodules with concurrent eosinophilia, elevated
Humans, as well as other definitive
definitive  hosts,  erythrocyte sedimentation rate, and elevated
are infected by consumption of uncooked or creatine kinase levels. Symptoms may last as  
undercooked meat of intermediate host that long as 5 years. Segmental necrotizing enteritis
contains sarcocysts. Once the intermediate has also been reported in one study.  
host is eaten by a definitive
definitive host
 host such as dog
Diagnosis 
or human, the parasite undergoes sexual
reproduction within the intestines. After Presumptive diagnosis of human intestinal
sarcocysts are ingested and the wall is digested, sarcocystosis is based on symptoms manifested
 bradyzoitess become motile.
 bradyzoite motile. Active bradyzoites
bradyzoites  by infected individuals
indivi duals and a history of recent
enter intestinal cells and change into the consumption of raw or undercooked meat.  
male and female forms, microgamonts and Identification of sporocysts in feces may
macrogamonts, respectively. Fusion of a require several stool examinations done on
macrogamont and a microgamont creates a   separate days during the infection. Sporocysts 
f iner ttoiliaznedocoeclyl scta(llceodnta  iznyignogtet,ww ichor odceyvsetlso p
o hs p ).  s oaf f teS r . ihnogmesitnini ga br eefif ,r satndextchr eotseedo1f  4S . toui1h8omdianyis
 s
 s  s

The oocyst is passed through the feces of

o f the are excreted 11 to 13 days after ingesting
definitive host. Most definitive
definitive host. definitive hosts
 hosts do not  pork. A fecal flotation
flotation wet
 wet mount is usually
show any clinical signs or symptoms.   done to visualize sporocysts using bright- field
More recently, a second life cycle has been microscopy. Flotation methods based on
described whereby carnivores and omnivores high-density solutions incorporating sodium
 pass the infectious stages in their feces.
feces. Ingestion
Ingestion chloride, cesium chloride, zinc sulfate, sucrose,
of this contaminated material may lead to Percoll, Ficoll-Hypaque, and other density
successful infection. gradient media are preferred over formalin-
ether/ethyl acetate and other sedimentation
Pathology and Clinical Manifestations 
methods. Species cannot be distinguished
The pathology is of two types: a rare from one another solely by microscopy because
invasive form that presents with vasculitis and sporocysts of different species overlap in size
myositis, and an intestinal form that presents and shape. 
with nausea, abdominal pain, and diarrhea. Definitive diagnosis can be made through
While normally mild and lasting under 48  biopsy of
o f an infected
infect ed muscle. Sarcocysts
Sar cocysts of
S.
hours, the intestinal form may occasionally be hominis are microscopic in muscles of cattle,
severe or even life threatening. The invasive whereas those of S. suihominis are macroscopic
form maylymph
including involve a wide
nodes, variety
muscles, andofthetissues
tiss ues  
larynx. in muscles
with of swine.
hematoxylin andSarcocysts
eosin stain.areConfirmatory
identifiable
In studies where volunteers ingested staining with the periodic acid-Schiff (PAS) can
infected beef, symptoms appeared 3 to 6  be performed as the walls stain positively. The
hours after eating. These symptoms included   walls of the sarcocyst may be used in species 
 

76  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

diagnosis. Currently, 24 wall types have been America, China, India, Tibet, and Southeast
identified in 62 species. S. hominis and S. Asia.
 suihominis both have walls of type 10. The wall
 suihominis Of fecal specimens examined from children
of S. hominis is up to 6 µm thick and appears in Poland and Germany, 10.4% and 7.3% were
radially striated from villar protrusions that are found positive, respectively. In Tibet,Sarcocystis
up to 7 µm long. The wall of S. suihominis is was detected in 42.9% of beef specimens
4 to 9 µm thick, with villar protrusions up to  examined from the marketplace,
marketplace, and S. hominis 
13 µm long. and S. suihominis were found in stool samples
Recently, polymerase chain reaction   of 21.8% and 7% of 926 persons, respectively.
r espectively.
(PCR) amplification of the 18S rRNA was Stool examination among Thai laborers showed  
demonstrated to be useful in distinguishing S. that Sarcocystis infection had a prevalence of
hominis , S. fusiformis, and S. cruzi sarcocysts about 23%; all cases were asymptomatic which
and oocysts. The technique makes possible  probablyy explained
 probabl explain ed the lack of recognition.
recogni tion. A
amplification and identification of species- study of 100 human tongues obtained post
specific gene sequences based on DNA extracted mortem in Malaysia revealed an infection
i nfection rate
from as few as seven excreted sporocysts (the of 21%. There was no sex difference and the age
equivalent of 3 ½ oocysts) from freshly prepared range was 16 to 57 years (mean 37.7 years). A
material, or as few as 50 sporocysts from fecal seroepidemiological survey in West Malaysia
seroepidemiological
samples that had been stored in potassium found that 19.7% of 243 persons had antibodies
dichromate (K 2Cr 2O7) for as long as 6 years.   for Sarcocystis . 
In the Philippines, studies involving  
Treatment 

Because infection is often asymptomatic, ho emexw

f trr  atienr a btiuof nf aolof em
am ssiugess,  oa b
s, ucsactltelet,i p ndtaignoeadts
treatment is rarely required. There have been revealed the presence of S. cruzi in backyard
no published trials so treatment remains cattle ( Bos tauruss) possessing a type 7 sarcocyst
 Bos tauru
empirical. Agents that have been used include wall, S. levinei in water buffaloes (  Bubalus
albendazole,
albendazo le, metronidazole,
metronidazole, and co-trimoxazole bubalis ) possessing a type 7 sarcocyst wall
for myositis. Corticosteroids have also been used with similarities to S. cruzi, S. miescheriana in
for symptomatic relief.   domestic pigs (Sus scrofa domestica) with a type
10 sarcocyst wall, and S. capracanisin domestic
Epidemiology 
goats (Capra hircus) with a type 14 sarcocyst
There are very few large-scale
l arge-scale population wall. There is a lack of local studies on human
surveys that have been conducted for Sarcocystis sarcocystosis. 
in humans. Prevalence data for Sarcocystis Prevention and Control 
infections often come from case reports and
findings of physicians, public health workers, Intestinal sarcocystosis can be prevented
and scientists with specific  interests. 
specific interests.  by thoroughly cooking or freezing meat to kill
Human infection is considered rare with  bradyzoites
 bradyzoi tes in the sarcocysts.
sar cocysts. Alternativ
Al ternatively,
ely,
less than 100 published cases of invasive freezing the meat at – 
at – 5°C
5°C for several days
disease (approximately 46 cases reported by will kill the sporocysts. Where contaminated
1990). These figures may represent a gross drinking water is suspected, boiling  should be
underestimate of the human burden of disease. considered to ensure disinfection.
Sarcocystosis has been reported in Africa, The administration of anticoccidial
Europe (Germany, Spain, and Poland), the drugs, amprolium and salinomycin, as
United States (California), Central and South  chemoprophylactic
chemopro phylactic agents was effective 
 

CHAPTER 2: Protozoan Infections   77 

in preventing severe illness and death in Research@DLSU-Manila:_Continu

Research@DLSU-Manila:_Continuing_
ing_
experimentally
experimentally infected calves and lambs.  the_Cycle. 2007;100.
The risk of foodborne zoonoses warrants Croft JC. Nonamebic
Non amebic protozoal enteridities.
 prevention and control in food animals. To In: Hoeprich D, Jordan MC, Ronald AR.
avoid infection of food animals, they must be Infectious processes. 5th ed. Philadelphia,
 prevented from
f rom ingesting
ing esting the
t he sporocyst
sporocy st stage Pa: Lippincott; 1994. p. 769 – 74.
74.
from human feces in contaminated water, feeds,  Dubey JP, Speer CA, Fayer R. Sarcocystis of  
and bedding. If such measures cannot be a sured animals and man. Boca Raton, Fla.: CRC
and meat is suspected to harbor cysts, the extent Press, Inc.; 1989.  
of infestation must be considered. In heavy and   Herenda D, Chambers PG, Ettriqui A,
widespread infestations with visible cysts, the Seneviratn a P,da Silva
Seneviratna Silv a TJ. Manual on meat
whole carcass must be condemned. In lighter inspection for developing countries. Rome,
R ome,
infestations, those parts of the carcass which are Italy: FAO;
FAO ; 2000. 
not affected are passed for human consumption.   Leek RG, Fayer R. Experimental Sarcocystis
 No vaccines are currently available. ovicanis infection in lambs: salinomycin
Experimentally inoculated pigs appear to chemoprophylaxis and protective
develop a persistent immunity, hence, vaccine immunity. J Parasitol. 1983;69:271 – 6
6.. 
development may be explored.  Ohio State University.Sarcocystis spp [Internet].
References 
2010 [cited 2010 Mar 1]. Available from
http://www.biosci.ohiostate.edu/parasite/
Bruckner DA, Garcia LS. Diagnostic medical  sarcocystis.html

r asair ttomloegnyt.oU
Dae p
 p f   PCaL ogeyd: iEclaslevCieer nStecr ie, nce
thAolM PayeC in. S 
r  lR  ar coc y t i s  p
 s  s
Micr o biol  R  ti9o0n2s.
pe pv. 2in00h4u;1m7a(n4)i:8n9f e4c – 
Publishing Co., Inc; 1988.   Xiang Z, Chen X, Yang L, He Y, Jiang R,  
Charleston WAG, Pomroy WE. Sarcocystis Rosenthal BM, et al.Non-invasive methods
species: self-teaching manual for veterinary for identifying oocysts of Sarcocystis spp.
 parasitology.
 parasitolo gy. Massey University:
Universit y: VPPH from definitive hosts. Parasitol Int. 2009;
Publication; 1995.  58(3):293 – 6.
6 . 
Claveria FG. Survey of Sarcocystis spp. infection Yu S. [Field
[Field survey of Sarcocystis infection in the
in Philippine livestock animals: light Tibet autonomous region]. Zhongguo Yi
microscopic and ultrastructural studies.   Xue Ke Xue Yuan Xue Bao. 1991;13:29 –  
32. Chinese.
 

78  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Other Intestinal Protozoans

Winifreda U. de Leon  

Blastocystishominis Parasite biology 

lastocystis hominis is an intestinal protozoan  

osheed ltihf eatctyhcelelif ies cuyncclele baer g. iInts hwaisth bienegnestion
 pr o pT
found in a vast array of animals, including  of cysts from contaminate
co ntaminatedd food or water.
water.Upon
humans. The classification of  Blastocystis has 
 Blastocystis
 been a long-standin
long-s tandingg problem
proble m for taxonomists.
taxono mists. ingestion, the cyst possibly develops into other
forms, which may in turn re-develop into cyst
It was previously classified as yeast under
forms. When excreted with stools, the cysts
the genus Schizosaccharomyces , while other
taxonomists suggested that it was related
r elated to
contaminate the environment and are eventually
transmitted to humans and other animals
omyces based on its glistening appearance
 Blastomyces
 Blast
in a wet mount and the absence of any organelle through the fecal-oral route, repeating the cycle.
Because the life cycle is not fully understood,
of locomotion. 
validation of this proposed life cycle and the
Correlative light electron microscopy has mode of transmission needs experimental
since shown that
th at the organism lacks
lack s a cell wal.lI
wal.lItt
confirmation. Multiplication of  B. hominis is
 possesses nuclei, endoplasmic reticulum, Golgi
 by binary fission. 
complex, and mitochondrion-like organelles 
 B. hominis is known to occur in four
tIht aits acr ae pcao bmle  b plesewuidthopor odtiaolzoeaxntemnosir  p
 paotf i b onhoalnodgy. morphological
morphological forms: (a) vacuolated, (b) ameba-
retraction. Moreover, the organism does not
grow on fungal culture media. It responds to
like, (c) granular,
recently, andcyst
additional (d) multiple
and avacuolar  More
fission.forms

anti-protozoal drugs. Studies with cultured have been recognized. 

organisms have shown that reproduction 
Vacuolated forms arethe most predominant
is asexual, either through binary fission or forms in fecal specimens. These are spherical in
shape, measuring 5 to 10 µm in diameter. A
sporulation under strict anaerobic conditions.
Optimal growth is at 37°C in the presence of large central vacuole pushes the cytoplasm and
the four nuclei to the periphery of the cell.
 bacteria. All the above findings supported the
Sometimes, a very thick capsule surrounds
reclassification of B. homin
hominisis from a yeast to an
emerging human protozoan parasite. 
the vacuolated forms. The prominent central
vacuole has been found to be a reproductive
There are new research findings  on the
findings on
taxonomic classification of  B. hominis . In
organelle. The vacuolar forms are considered
to be the main type of Blastocystis that cause 
1996, Silberman et al. completed a study of  
the small subunit rRNA (SSUrRNA) gene ea.e b a- li ke  f o r m s,  us ua lly  me as ur in g
diarr Ahm
of the organism, and the results showed
that it belongs to an informal group
g roup called
 between 2.5 to 8 µm, are occasion
occasionally
ally observed
Stramenophiles,
Stramenoph iles, which is a recently recognized  in stool samples. They exhibit active extension
and retraction of pseudopodia. The nuclear
group of microscopic
heterogenous
heterogen parasites.
parasites
ous protists like brown. algae,
This includes
diatoms, chromatin, when visible, characteristically
and water molds, to name a few.   shows peripheral clumping. The amebic form
appears to be an intermediate stage between 
 

CHAPTER 2: Protozoan Infections   79 

the vacuolar form and the precystic form, as flatulence, mild to moderate diarrhea without
this stage allows the parasite to ingest bacteria fecal leukocytes or blood, nausea, vomiting, low
in order to enhance encystment. Studies grade fever, and malaise. Symptoms usually last
of Tan and Suresh have revealed that the about 3 to 10 days, but may sometimes persist
ameboid forms predominated in isolates from for weeks or months.  
symptomatic cases. It has been found that in subjects suffering
Granular forms are multinucleated and   from immunosuppression, Blastocystis showed  
are mainly observed from old cultures. The a significant association with gastrointestinal
diameter of the cell varies from 10 to 60 µm. symptoms. Other studies have also provided
The granular contents
contents develop into daughter   evidence of changes in the cellular immune  
cells of the ameba-form when the cell ruptures.  function of infected individuals.  
Multiple fission forms arise from vacuolated
Diagnosis 
forms. It is believed that these multiple fission
forms produce many vacuolated forms.   Specific diagnosis based on clinical
The size of the resistant cystic form is  presentation alone may prove
 presentation prove difficult, be
because
cause
about 3 to 10 µm in diameter,
d iameter, and has one or the spectrum of symptoms is seen in other
two nuclei. It has a very prominent and thick, intestinal infections. Laboratory detection of
osmophilic, electron dense wall. It appears the organism from stool is needed to
t o confirm
as a sharply demarcated polymorphic, but the diagnosis. Multiple stool samples should
mostly oval or circular, dense body surrounded  be collected from patients showing clinical
 by a loose outer membranous layer. This  signs and symptoms. Microscopic examination 
r  b
meicm osr caon poyuscolar r yes p cor niltlr aar stlayer
r  soenedns into pthaesefi b issiingcr deiar seecdt  f wechaelnsmcoenar ceisnutr saetf iuoln,  btuetchsenniqsiutievsity
u

described around the cyst at the ultrastructural are used. Hematoxylin or trichrome staining
level, and is the easiest diagnostic feature to offers a very convenient and easy method to
identify.  differentiate the various stages of Blastocystis.
 Blastocystis
It is postulated that the thick-walled cyst Leukocytes are usually seen in fecal smears and
may be responsible for external transmission, stool eosinophilia may also be observed. The
while those cysts with thin walls may
m ay be the organism can be cultured using the Boeck and
cause of reinfection within a host’s intestinal Drbohlav’s or
Drbohlav’s or the Nelson and Jones media.  
tract. 
Treatment 
Pathogenesis and Clinical Manifestations 
ocystisis difficult to eradicate. It hides
 Blastocystis
 Blast
Infection with  B. hominis is called in the intestinal mucus, as well as sticks and
 blastocystosis.  B. hominis as a cause of holds on to intestinal membranes. The drug of
gastrointestinal pathology is controversial. choice is metronidazole given orally, 750 mg
Several studies have shown that the presence three times daily for 10 days (Pediatric dose:
of the parasite in a majority of patients was not 35-50 mg/kg/day in three doses for 5 days)
associated with symptoms; or, it was found or iodoquinol given at 650 mg three times
with other organisms that were more likely to daily for 20 days. However, there have
hav e been
 be the cause of the symptoms. However
However,, other reported cases of resistance. Trimethroprim-
studies have concluded that the presence of sulfamethoxazole (TMP-SMX) has also been
 Blastocystis in large numbers produces a wide found to be highly effective against Blastocystis.
variety of intestinal disorders, such as abdominal  Nitazoxanide has been clinically tested on
cramps, irritable bowel syndrome, bloating,   patients with blastocystosis,
blastocyst osis, and was found to 
 

80  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

resolve symptoms in 86% of patients after 3  Blastocystis similar to those found in humans.
days of administration.  Evidence has also shown that  Blastocystis is
 present in house lizards and cockroaches,
Epidemiology 
raising the possibility that food and water
w ater
 Blastocystis hominis has been reported contaminated by fecal droppings of these “home
virtually worldwide, with infections occurring visitors” may
visitors”  may transmit Blastocystis . 
most commonly in tropical, subtropical,
subtropical, and  In the Philippines, studies of 32
developing countries. Studies from developed morphologically
morphologically similar isolates from different
countries have reported approximately 1.5 to hosts: 12 from humans, 12 from pigs, and 8
17.9% overall prevalence of  B. hominis . All from chickens, using the restriction fragment
fragment 
ages are affected, but symptomatic cases are length polymorphism
polymorphism (RFLP) analysis
a nalysis of small
more often found in children and in those with subunit rDNA (SSUrDNA), have shown
weakened immune systems. A prevalence of up up extensive genomic polymorphism.  
to 11.6% was
w as reported
reporte d from
from Stanford University Prevention and Control 
Hospital. Prevalence rates of 32.6 % and as high
as 52.3% had been reported from China and Available data on  B. hominis
hominis indicate that
Malaysia, respectively.  the disease can be prevented by consuming safe
Occurrence of the parasite in temperate drinking water. While food has not been fully
countries is generally associated with recent implicated, provisions for sanitary preparation
travel to the tropics and consumption of may be of value in efforts to prevent and
untreated drinking water. This indicates that   control this infection. The cysts of B. hominis
hominis  

iannf decittioisn miso pr eosliski b
 bely  tohr ocucguhr   tinhecr oor waldr eoduaten,d cteam
n p er r avtiuver eu,  pantdo  1h9avde asyhsoiw
  su aetseir staatnnceor tm
n nwr  o al
unsanitary conditions. Outbreaks of B. hominis hominis chlorine at the standard concentrations.  
in day-care centers have been reported in Spain References 
(5.3-10.3%), Brazil (34.7%), and Canada 
(13.4%). Avila MS, Garcia MR, Narcelles MV, Serra
In the Philippines, examination of FB, Tejida GM. Prevalence of intestinal
772 stools from consecutive patients at the   helminth and protozoan infections among
Department of Parasitology, College of Public food handlers in selected school canteens
Health, University of the Philippines Manila, in Manila [undergraduate special study].
showed a prevalence of 20.7%, sometimes with 2003. Located at: College of Public Health
concomitant infection with other intestinal Library, University of the Philippines
 parasites. Studies have also shown prevalence Manila. 
rates of 40.6% among food service workers Department of Parasitology. Diagnostic
in a tertiary hospital, and 23.6% among Laboratory Records. 1997. Located at:
food handlers in selected school canteens   College of Public
Publ ic Health Librar
Library,
y, University
in Manila. Stool surveys conducted by the of the Philippines Manila. 
Field Epidemiology Training Program of the Department of Parasitology. Diagnostic
Department of Health in Tapel, Gonzaga, Laboratory Records. 1998. Located at:
Cagayan Valley, andrates
showed prevalence Talavera, Nueva
of 20% andEcija
44%, College
of of Public
Publ ic Health
the Philippines Librar
Library,
Manila.   y, University
respectively.  Doyle PW, Helgason
Helgason MM. Epidemiology and
Some animals, like pig-tailed macaques,  pathogenicify
 pathogeni cify of Blast
 Blastocystishominiss. J Clin
ocystishomini
chickens, dogs, and ostriches may harbor   Microbiol. 1990;28:116 – 21.
21.
 

CHAPTER 2: Protozoan Infections   81 

Diaczok BJ, Rival J. Diarrhea due to Blasto

 Blastocystis
cystis Mclure HM, Strobeft EA, Healy GR.
hominis: an old organism revisited. South 1980 Blastocystis hominis
hom inis in a pigtailed
Med J. 1987;80(7):931 – 2.
2. macaque: a potential enteric pathogens
Esparar, DG, Belizario VY. Prevalence of for non-humans primates. Lab Anim Sci.
 parasitic infection
i nfection among
a mong food-h
fo od-handlers
andlers 1980;30(5):890 – 4
4..
in a dietary service of a tertiary hospital Rivera W, Tan MA. Molecular characterization
characterization
in Manila. 2003. Located at: College of   of Blastocystis isolates in the Philippines
Public Health Library, University of the  by riboprinting. Parasitol Res.  
Philippines Manila.   2005;96(4):253 – 7 7..
Garcia LS, Brucknel DA, Clancey MN. Clinical Rivera WL. Phylogenetic analysis of  Blastocystis
relevance of Blastocystis hominis. Lancet. isolates from animal and human hosts in the
1984;1:1233 – 4.
4. Philippines. Vet Parasitol. 2008;156:178 –  
Guirges SY, Al Waili NS. Blastocystis
 Blastocystis hominis:
hominis 82.
evidence for human pathogenicity and Rossingnol JF, Kabil SM, Said M, Samir H,
effectiveness of metronidazole
effectiveness metronidazole therapy. Clin
C lin Younis AM. Effect of nitazoxanide in
Exp Pharmacol Physiol. 1986;4:333 – 335.
335.   persistent diarrhea and enteritis
enteriti s associated
Haresh H, Suresh K, Khairul A, Saminathan  with Blast
 Blastocystis hominii.  ssClin Gastroenterol
ocystis homin Gastroent erol
S. Isolate resistance of  Blasto
 Blastocystis
cystis homin
hominis
is Hepatol. 2005;3(10):987 – 91.
91.
to metronidazole. Trop Med Int Health. Silberman JD, Sogin ML, Leipe DD, Clark CG.
1999;4:274 – 7.
7. Human parasite finds taxonomic home.
Jiang JB, He, JG.
J G. Taxonomic
Taxonomic status Blastocystis 
 Blastocystis  Nature.1996;380(6573):398.

KainhoK mCi,ni N. oP balr easM
 s y. a1n99H3J;,9(B1a0r )t:e2l – 
itoAl,TFor deeam u3k. deSn.t N
Tan iK  if iceawtioi ns,igahntds  colninci lalssr if eilceavtainonce, 
RL. Epidemiology and clinical features of Blastocystis spp. Clin Microbiol Rev.
 Blastocystis
associatedwith Blastocystishominis infection. 2008;21(4):639 – 6
65.
5. 
Microbiol Infect Dis. 1987;8(4):235 – 44. 44.   TanTC, Suresh KG. Predominanceof
Predomi nanceof Ameboid
Amebo id
Koutsavlis AT, Valiquette L, Allard R, Soto J. forms of Blastocystis hominis
hom inis in isolates
 Blastocystis hominis: a new pathogen in from symptomatic patients. Parasitol Res.
day-care centers? Can Commun Dis Rep. 2005;98(3):189 – 93. 93.
2001;27:76 – 84.
84. Valido E, Rivera W. Colony Growth of
Long HY, Handschack A, Konig
Koni g W. Blastocystis
 Blastocystis  Blastocystis
 Blastocystis hominis in simplified soft agar
hominis
hominis modulates immune responses and medium. Parasitol Res. 2007;101(1):213
2007;101(1):213 –  
cytokine release in colonic epithelial cells. 7.
Parasitol Res. 2001;87:1029 – 30.
30. Yoshikawa H, Yoshida K, Nakajim a A,
Markell EK, Udkow MP. Blastocystis
 Blastocystis hominis:
hominis Yamanari K, Iwatani S, Kimata I. Fecal-
 pathogen or fellow traveler?Am
traveler?Am J Trop
Trop Med oral transmission of the cyst form of  
Hyg. 1986;35(5):1023 – 6.
6.  Blastocystis
 Blastocystis hominiss in rats. Parasitol Res .
homini
Matsamuto Y, Yamada M, Yoshida Y. Light   2004; 94(6):391 – 66..
microscopical appearance and ultra- Zierdt CH.  Blastocystis hominis
hominis-past and future.
structure of  Blastocystishominis , an intestinal Clin Microbiol Rev. 1991;4:61.  
 parasite of man. Zentrabl Bakteriol
Mikrobiol Hyg B. 1986;264(3 – 4):379
4):379 – 85.
85. 
 

82  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Di 
entamoebafrag ll 
i 
s
i 
Vicente Y. Belizario, Jr., Timothy M. Ting

ientamoeba fragilis was first discovered by debris. No cyst stage has been identified. Except
Wenyon in 1909 but was firstfirst  described  for the absence of a flagellum, this protozoan is
in the scientific literature by Jepps and Dobell closely related to and resembles Trichomonas. 
in 1918. It remains neglected despite evidence  D. fragilis lives in the mucosal crypts of  
supporting its pathogenicity. It has been the appendix, cecum and the upper colon. TheTh e
identified in practically all regions of the world exact life cycle is unknown, although several
in which satisfactory iron-hematoxylin stained assumptions have been made from clinical
films have
films  have been carefully examined.  data (Figure 2.13). Direct human to human
Parasite Biology 
transmission is probably via the fecal-oral route
or via transmission of helminth eggs particularly
On the basis of electron microscopic, that of  Enterobius vermicularis
ver micularis .  Dientamoeba -
immunologic, and molecular phylogenetic like mononucleated and binucleated forms
findings, this protozoan, which was srcinally have been observed in the lumen of Enterobius
described as an ameba, is actually a flagellate adults and eggs present in the intestines. More
with only the trophozoite stage known (Plate recently, stools from macaques, gorillas, and
2.15). The organism measures about 7 to 12 µm   swine were found to carry  D. fragilis , thus
w heodnneuocr 
shiat p leti.wToh(er anr ueclyletahr r m r  f r oanur e)dr ooessenttoet-
o b
eeem aonf  ihmuaml r aenseinr vf oecir tsiomnas.y also b
 be  ppotential sour ccees 
have peripheral chromatin, and the karyosome Pathogenesis and Clinical Manifestations  
consists of four to six discrete granules. The
cytoplasm may contain vacuoles with ingested  frag ilis does not invade
 Dientamoeba fragilis
tissues, but its presence in the intestines
 produces irritation of the mucosa with secretion
of excess mucus and hypermotility of the
 bowel. Infections are usually asymptomatic. In
symptomatic
sympto matic individuals,
individuals,the onsetof infect
infection
ion is
usually accompanied by loss of appetite, colicky
abdominal pain, and intermittent diarrhea with
excessmucus,abdominaltenderness,abloating
sensation, and flatulence. Another common
symptom, reported in 11% of the patients,
was anal pruritus. This may partially be due
to the co-infection with  Enterobius. Peripheral
 Enterobius
eosinophilia can be observed in 50% of the
cases. Chronic infection of this organism can
mimic thebowel
irritable symptoms of diarrhea-predominant
syndrome (IBS), and some
Plate 2.15. Binucleate forms of trophozoites of experts have suggested ruling out infection with
De s ,stained with trichrome
i ntamoebafrag ill 
i  this organism first before diagnosing a patient
(Accessed from from  www.dpd.cdc.gov/dpdx)  as having IBS.
 

CHAPTER 2: Protozoan Infections   83 

Diagnosis  of the fresh specimen with polyvinyl alcohol

fixative oorr Schaudinn’s fixative has been found
Diagnosis of this organism is by observation to be helpful. 
of binucleate trophozoites in multiple fixed and
stained fresh stool samples. Fresh stool samples Treatment 
are necessary since the trophozoites degenerate Antimicrobial therapy is fo
followed
llowed by
after a few hours of stool passage. Multiple  
resolution of symptoms and eradication of  
e  ppolr re gsaniniscmr e.aU
stahm sentlheses stehnesilta  b
ibviotr yatof r ydetxeacmtiinger  D.  fra
 fragilis. Treatment
gilis Treatment is done with iodoquinol
is aware of the possibility that D. fragili
fragilissmay be
at 650 mg three times daily for 20 days. The  
 present in the fresh ffecal t he  protozoan
ecal films, the
 pediatri c dose is 40 mg/kg/day
 pediatric mg/kg/da y in three doses,
is easily overlooked. Purged stool specimens also for
fo r 20 days. Tetracycline
Tetracycline and metronidazole
 provide more
more suitable material
material for examination
examination have also been found to be effective.  
than the average formed stool. Even when Epidemiology 
formed, D. fragilis may be misdiagnosed as
other amebae. This organism is not detected by The organism has a world-wide distribution
stool concentration methods. Prompt fixation
fixation   with varying infection rates ranging from 0.4 to  
 

84  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

as high as 42%. In contrast to many pathogenic  population:: a preliminary

 population preliminary investigation. Vet
Vet
 protozoa, which have a high prevalence in Parasitol. 2007;145:349 – 5
51.
1. 
developing countries, high prevalence rates of   Girginkardesler N, Kurt O, Kilimcioglu A,
fragilis have been reported from developed
 D. fragilis Ok U. Transmission of  Dientamoeba
countries with high sanitation standards. Using  fragilis: evaluation of the role of Enter
 fragilis  Enterobius
obius
adequate culture techniques, the rates were as vermicularis. Parasitol Int. 2008;57:72 – 55.. 
high as 18% in Israel, 36% in Holland, and   Johnson E, Windsor J, Clark G. Emerging  
41.5% in Germany. from obscurity: biological, clinical, and
Prevention and Control 
diagnostic aspects of  Dienta
 Dientamoeba
moeba fragilis.
fragilis
Clin Microbiol Rev. 2004;17(3):553 – 770.0.  
Specific recommendations for prevention Johnson J, Clark C. Cryptic genetic diversity
and control cannot be made until there is more to Dientamoeba fragilis. J Clin Microbiol.
specific information concerning the method of 2000;38(12):4653 – 4 4..
transmission. Proper sanitation and disposal of Katz D, Taylor D. Parasitic infections of the
human waste are essential.  gastrointestinal tract. Gastroenterol Clin
 N. 2001;30(3):797 – 815.
815.
References 
Lagace-Wiens P, Van Caeseele P, Koschik C.
Banik G, Birch D, Stark D, Ellis J. A  Dientamoeba fragilis : an emerging role
 Dientamoeba
microscopic description and ultrastructural
microscopic ultrastructural in intestinal disease. Can Med Assoc J.
characterization
characterization of  Dienta
 Dientamoeba
moeba ffra
ragilis: an
gilis 2006;175(5):468 – 9 9..
emerging cause of human enteric disease.  Stark D, Barratt J, Roberts T, Marriott D,

BaniIkntGJ, PBar aarr siattot l.J,20M12ar ;4r i2o:t1t 3D

9 – , 5H3.ar kness  J, Hr aer 
 p skenteastsioJ,nEolf lidsiJe.nAtam
r evoie bwiaosif s.thAemclJinTir co p
al
Ellis J, Stark D. A case-controlled study of Med Hyg. 2010;82(4):614 – 9 9.. 
 Dientamoeba
 Dientamoeba fragilis infection
fragilis in children.
children. Stark D, Philipps O, Peckett D, Munro U,
Parasitol. 2011;138:819 – 23.
23. Marriott D, Harkness J, Ellis J. Gorillas are
Barratt J, Harkness J, Marriorr D, Ellis J, a host for Dientamoeba fragilis: an update
Stark D. A review of  Dienta
 Dientamoeba
moeba fragil
fragilis
is on the life cycle and host distribution. Vet
carriage in humans: several reasons why Parasitol. 2008;151:21-6.
this organism should be considered in the Stark D, Beebe N, Marriott D, Ellis J, Harkness  
diagnosis of gastrointestinal illness. Gut J. Dientamoeba fragilisas a cause of travelers’
Microbes. 2011;2(1):3 – 12.
12.  diarrhea: report of seven cases. J Travel
Barratt J, Harkness J, Marriott D, Ellis J, Stark   Med. 2007;14(1):72 – 3 3..
D. The ambiguous life of  Dientamoeba Windsor J, Macfarlane L. Irritable bowel
 fragilis: the need to investigate current syndrome: the need to exclude
hypotheses on transmission. Parasitol.  Dientamoeba
 Dientamoeba fragilis. Am J Trop Med Hyg.
fragilis
2011; 138:557 – 72.
72.  2005;72(5):501.
Crotti D, Sensi M, Crotti S, Grelloni V, Windsor J, Johnson E.  Dientantoeba fragilis:
Manuali E. Dientamoeba fragilis in swine  The unflagellated human flagellate. Brit J
Biomed Sci. 1999;56(4):293 – 306.
306.
 

CHAPTER 2: Protozoan Infections   85 

Plasmodiumspp.
Vicente Y. Belizario, Jr., Carlos Miguel P. Perez

alaria remains the leading parasitic disease Table 2.4. Millennium development goals: eight
that causes mortality worldwide. With  goals for 2015  

655,000 malaria-related deaths reported in

M 
2010 and an estimated 3.3 billion people at
risk for infection, the disease has been identified
 Achi 
eveun iversa
 p
 l rm
ii   aryeducat ii 
o n
 by the World Health Organization (WHO) 
as one of the three major infectious disease  
threats, along with human immunodeficiency
virus/acquired immune deficiency syndrome
(HIV/AIDS) and tuberculosis, which together
cause more than 5 million deaths each year.
Malaria leads to decreased social and economic
 producti vity and contributes
 productivity contribut es to a vicious cycle
Source: United Nations. General assembly, 56th session. Road
of disease and poverty. Young children and map towards implementation of the united nations millennium
 pregnant women are the p population
opulation groups declaration: report of the secretary-general (UN Document no.
 A1561326). New York: United Nations,
Nations, 2001.
mostly affected by malaria. Chronic malaria 
ysiac,alwahnidchmiesnatsaslogcr iaotwedthwainthd
liema pdas ir teoda pnhem treated. The group of parasites causing malaria
development
developm ent in children. In pregnancy,anemia  belongs to the genus  Plasmodium that is
is a leading contributor to maternal morbidity transmitted by the bite of an infected female
and mortality, and is associated with risk of mosquito belonging to the genus  Anopheles .
cardiac failure and adverse perinatal outcomes. The four species that are medically important
Anemia from malaria is also exacerbated by to humans are  Plasmodium falciparum
falc iparum ,  P.
anemia from concomitant helminth infections vivax,  P. ovale
ovale, and P. malariae. The first two
in both children and pregnant women.   are responsible for over 90% of all human
In 2000, the United Nations (UN) adopted malaria cases. More recently,  P . knowlesi has
the Millennium Declaration, serving as a  been described in humans in the Philippines
 blueprint
 bluepri nt for the eradication
eradicatio n of extreme poverty and most of Southeast Asia.  P . knowlesi ,
through eight quantifiable time -bound targets considered the fifth human malaria parasite,
known as the Millennium Development Goals is normally a parasite of long-tailed macaques
(MDGs) (Table 2.4). MDG 6 aims to reduce   ( Macaca
 Macaca fascicularis), but humans
fascicularis humans working in 
the burden of HIV/AIDS, malaria, and other
o ther nearby forestfringe pose greatrisk for infection.
diseases. The malaria component of MDG 6 The first
first naturally
 naturally acquired human infection
includes reducing incidence and mortality rates was reported in 1965 in Sarawak, Malaysia;
of the disease, increasing insecticide-treated
insecticide-treated bed other foci of infection have been reported in
net
age coverage among
and increasing children below
anti-malarial 5 years
coverage of
among
Thailand and China as late as 2008. In the
Philippines, the first reported case of P. knowlesi
knowlesi 
children below 5 years of age.   was described in 2006. Since then, the Research
Despite the high figures
figures  in mortality, the Institute for Tropical Medicine (RITM) has
disease is curable if promptly and adequately  reported nine cases of mixed malaria infection, 
 

86  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 positive for  P. knowlesi . The life cycle of  P

 P.. in humans consists ofschizogony, which leads to
knowlesi is microscopically indistinguishable the formation of merozoites, and gametogony,
from  P. malariae, and differentiation is only which leads to the formation of gametocytes. 
achieved through polymerase chain reaction The sexual cycle in the mosquito involves
(PCR) assay and molecular characterization.
characterization.   sporogony, which leads to the formation  
These protozoans are pigment producers of sporozoites. The life cycles of all human
hum an
and are ameboid in shape, with someso me being  species of malaria are similar. The infected 
more ameboid than the others. Their asexual female Anoph eles mosquito bites and sucks
cycle occurs in humans, the vertebrate and  blood from the human host. In the process,
intermediate host, while the sexual cycle occurs   salivary fluids containing sporozoites are also  
in the Anopheles mosquito, the invertebrate and
 Anopheles injected. These sporozoites, the infective stage
definitive host.
definitive host. of the parasite, are immediately carried to the
liver and enter the parenchymal cells. The
Parasite Biology 
 parasites then commence exo-erythrocytic
Various processes comprise the life cycle schizogony, which produces the merozoites
(Figure 2.14) of the parasite. The asexual cycle  in varying duration and amounts, depending  
 

CHAPTER 2: Protozoan Infections   87 

on the species. Merozoites proceed to the gut as an ookinete, which then develops into
 peripheral blood to enter the erythrocytes.
erythro cytes. Some an oocyst. The oocyst grows and produces
merozoites of P.vivax and P.ovale re-invade the sporozoites, which escape from the oocyst and
liver cells forming hypnozoites, while the other enter the salivary glands of the mosquito. These
species do not. These dormant exo-erythrocytic sporozoites may be injected into another human
hu man
forms may remain quiet for years. Within host when the mosquito takes a blood meal.
the red blood cell, the merozoite grows as a   The entire developmental cycle in the mosquito  
ring form developing into a trophozoite. The takes 8 to 35 days, depending to some extent
trophozoite has an extended cytoplasm and on ambient
a mbient temperature.
temperature.
a large chromatin mass which further divides   Morphologically, the early trophozoite
to form more merozoites within schizonts. form is ring-shaped with a red chromatin dot
The merozoites of P.
 P. falciparum develop in the
falciparum and a scant amount of blue cytoplasm when
 parasitop horous vacuolar
 parasitophorous v acuolar membrane
me mbrane (PVM)
(P VM) stained with Giemsa or Wright’s stain. The
within the mature red cells and modify the trophozoite form has a large chromatin mass
structural and antigenic properties of these and a prominent ameboid cytoplasm, which
cells. The parasites feed on the hemoglobin is spread through the erythrocyte. The parasite
resulting in the production of pigment known develops into a schizont when the chromatin has
as hematin. Soon after, the erythrocytes rupture divided into two or more masses of chromatin
and the merozoites are released into the blood,
bl ood, with small amounts of cytoplasm, the so-called
ready to enter new erythrocytes. This asexual merozoites. The number of merozoites is species
cycle is synchronous, periodic, and species-  dependent. Clumps of pigment accumulate in  
deter Smined.mer ozoites  develo p 
om  p  into Tihdedlgeaomf  eatomcaytue r setascgheizf oilnlst.the  entir e 
the m

microgametocytes
microgam etocytes (male) or macrogametocytes
macrogametocytes red blood cell and is characterized by a large
(female) which are picked up by feeding female chromatin mass and a blue cytoplasm with
mosquitoes for completion of the life cycle. In  pigment. It is round to banana-shaped. The
the gut of the mosquito, the male gametocytes microgametocyte has a lighter blue cytoplasm,
exflagellate and produce eight sperm-like while the cytoplasm of the macrogametocyte
microgametes which may fertilize the female is a darker blue. Species identification depends
macrogamete to form a zygote. The zygote on various characteristics of these stages of
 becomes motile and penetrates the mosquito’s
mosquito’s   development as described
d escribed in Table 2.5. 

Table 2.5. Comparison of morphological features of malaria parasites  

 

CHAPTER 2: Protozoan Infections   89 

yellowish

48hoursolress

Note: P. knowlesi is microscopically indistinguishable from P. malariae.

 period, the time between

bet ween sporozoite
sporozoi te injection with the associated asymptomatic intervals.
and the appearance of clinical symptoms, is Prodromal symptoms may include: a feeling
typically 8 to 40 days, depending again on of weakness and exhaustion, a desire to stretch
the involved species. For P. falc
falciparum, it lasts
iparum and yawn, aching bones, limbs, and back, loss
an average of 8 to 15 days, for P. vivax
vivax, 12 to of appetite, nausea and vomiting, and a sense of
20 days, for P. ovale
ovale, 11 to 16 days, and for P. chilling. At the onset, symptoms may include
malariae, 18 to 40 days. The incubation period malaise, backache, diarrhea, and epigastric
may range from 9 days to 3 years, depending discomfort. The classical malaria paroxysms
on the parasite strain, the dose of sporozoites have three stages: the cold stage, the hot stage,
inoculated, the immune status of the host, and and the sweating stage. The cold stage starts
the host’s malaria chemoprophylaxis  history. with a sudden inappropriate feeling of coldness
Partial or incomplete prophylaxis may prolong and apprehension. Mild shivering quickly turns
the incubation period several weeks after to violent teeth chattering and shaking of the
termination of medication. Any person who entire body. Although the core temperature
t emperature is
has traveled to a malaria-endemic area must be high or may be rising quickly, there is intense
considered at risk of developing malaria up to  peripheral
 peripher al vasoconstrictio
vasocon striction.
n. The pati
patient
ent may
2 years and even longer upon leaving the area.  vomit and febrile convulsions may ensue at
There are no absolute clinical features of this stage in young children. These rigors last
malaria except for the regular paroxysms of fever   for 15 to 60 minutes after which the shivering  
 

90  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

ceases, and the hot stage or flush phase begins. distribution. They also depend on the age,
The patient becomes hot and manifests with geneticconstitution,stateofimmunity, general
headache, palpitations, tachypnea, epigastric health and nutritional status of the host, and
discomfort, thirst, nausea, and vomiting. The on any chemoprophylaxis or chemotherapy
temperature may reach a peak of 41°C or even  previously used. 
more. The patient may become confused or There may be a tendency to recrudesce or
delirious, and the skin may be notably flushed
flushed   relapse over a period of months to several years. 
and hot. This phase lasts from 2 to 6 hours. In Recrudescencee is the renewal of parasitemia
Recrudescenc
the sweating stage, defervescence
defervescence or diaphoresis or clinical features arising from persistent
ensues with the patient manifesting with   undetectable asexual parasitemia in the absence 
undetectable
 profuse sweating.
sweating. The temperature
temperature lowers over
over of an exo-erythrocytic cycle. Relapse is renewed
the next 2 to 4 hours, and symptoms diminish asexual parasitemia following a period in which
accordingly. The total duration of a typical the blood contains no detectable parasites
attack is 8 to 12 hours. The classic periodicity (Figure 2.15). Relapses, which occur with vivax
of attacks develops only if the patient is left and ovale malaria, result from the reactivation
untreated until the time when the life cycle of hypnozoite forms of the parasite in the liver.
 phases become
beco me synchronized
synchro nized and sufficient Cold, fatigue, trauma, pregnancy, and infections
numbers of red blood cells containing schizonts including intercurrent falciparum malaria may
rupture at about the same time. The interval  precipitate reactivation.
reactivation.  
 between attacks is determined
determin ed by the length of The pathological processes in malaria
the erythrocytic cycle. For P. falciparum, it is 
falciparum are the result of the erythrocytic cycle. Once  
4oc8chuor  uor ns. aFltoer P   P . oval e,  par ox ysms
nate dayas.nFdor  P. malari
. viva x
malariae ae  ,  they tehr yethmr oecr oyzteosi,teths eocf ell P 
sr educe their  deif novr am
.  f al ci par um dae btihliety,
occur every 72 hours, causing paroxysms on the degree of which is directly proportional
days 1 and 4, hence the term, quartan malaria. to parasite maturity. This reduction in
Due to the lack of an exoerythrocytic stage in  deformability is due to changes in the red
 P
 P..knowle
knowlesi si, fever follows a quotidian pattern, or  blood cell cytoskeleton and the increase in
is noted to be non-relapsing.  membrane stiffness and cytoplasmic viscosity.
The five  species also differ in the age of
five species In the course of invasion, electron-dense sub-
infected erythrocytes. The non-falciparum membranous structures appear and enlarge.
species infect erythrocytes only of a certain These become the so-called “knobs” which are
age: P. vivax and P. ovale infect only young red important in cytoadhesion. They contain several
 blood cells, while P.
 P. malariae infects only aging
malariae histidine-
 proteins such as rosettins, riffins, histidine-
cells. This limits the number of red blood cells rich proteins (HRP), and the  Plasmodium
that can be parasitized to less than 3% of all  falciparum erythrocyte membrane protein 1
erythrocytes. P.
 P.falcipa rum, as well as P
falciparum  P..kno
knowlesi, 
wlesi (PfEMP-1), which is the most adhesive protein 
may infect erythrocytes of all ages. As the among the knobs. PfEMP-1 is encoded by a
infected erythrocytes rupture, more falciparum multi-gene family termed var and is clonally
malaria parasites are released
released to infect
i nfect more red variant enabling it to evade specific immune
 blood cells. The severity of complications
compli cations and  responses. Rosettins and PfEMP-1 are the  
mortality
increases..increase
increases as and
The course the severity
level of of
parasitemia
the attack ligands for rosette
 parasitized nonformation.
and non-parasiti zedThey
-parasitized cellsadhere
as wellto
of malaria depend on the species and the strain as blood platelets. In more recent studies, it
of the infecting parasite; therefore, geographical
geographical has been suggested that febrile temperatures
srcin of infection plays a major role in disease  induce the cytoadherence of the ring-staged  
 

CHAPTER 2: Protozoan Infections   91 

Figure 2.15. Diagram of the course of malaria infections showing the primar y attack, relapses,
and recrudescence (From World Health Organization. Chemotherapy of malaria and resistance to
antima lar ials: r e po r t of a  WHO sc ie ntif ic gr oup. Te c hnical r epo r t se r ies no . 529.  
Geneva: World Health Organization; 1973.)  

 P. falciparumerythrocytes, and that the factor  

falciparum cytokines at the time of schizont rupture.  
responsible for this heat-induced cytoadherence
cytoadherence The combination of altered red cell surface
is PfEMP-1.
PfEM P-1. HRP
HRP,, on the other hand, localize to   membranes and the host’s  immunological 
host’s immunological
the cytoadherence ligands making the adhesion response to the parasite antigens bring about the
more effective.   patholo gic changes such as alteration
 pathologic alteratio n in regional
Infected erythrocytes also undergo  blood flow in the vascular endothelium, altered
altered membrane transport mechanisms.  biochemistry, anemia, and tissue and organ
The hemoglobin is digested forming the hypoxia. Other destructive tissue processes
 pigment hematin, and
an d variant strain-
strain -specific include increased capillary permeability which
neoantigens
neoantigens are expressed. The soluble antigens allows fluid to leak into surrounding tissues, and
of P. falciparum are potent inducers of pro- congestion in blood vessels resulting in tissue
inflammatory as well as anti-inflammatory infarction and necrosis. 
cytokines from monocytes and macrophages. In severe forms of malaria, impairment
Glycosylphosphatidyl inositol (GPI) moieties of consciousness and other signs of cerebral
that are seen covalently linked to the surface dysfunction, such as delirium and generalized
antigens of these protozoans act like the convulsions, are commonly observed. Other
endotoxin of gram-negative bacteria, manifestations are severe hemolytic anemia
lipopolysaccharide (LPS). They stimulate the with a hematocrit less than 20%, hemoglobin
monocytes to release tumor necrosis factor levels less than 7 g/dL and hyperbilirubinemia
(TNF) or cachexin, which is implicated as with levels more than 50 mmol/L (Table
(Table 2.6). 
the cause of malarial fever. The fever, febrile Cerebral malaria generally manifests with
 paroxysms, headache,
headache, various
various aches and pains,
pains, diffuse symmetric encephalopathy. Other signs
and prostration, which are the more familiar and symptoms include retinal hemorrhage,
symptoms of an acute malarial attack, are  bruxism (fixed jaw closure and teeth grinding),
 probably the result of the release of these  and mild neck stiffness. Pouting may occur or  
 

92  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Table 2.6. Clinical features and laboratory findings in severe malaria infection  

Laboratoryresults

Prostration dL)
Failure to feed
Multiple convulsions*

Respiratory distress Hemoglobinuria

Circulatory collapse or shock (systolic blood pressure Hyperparasitemia (>2% or 100 000/μL in low intensity
transmission areas or >5% or 250,000/ μL in area s of high
Clinical jaundice
Other evidence of vital organ dysfunction
 Abnormal spontaneous bleeding Renal impairment (serum creatinine >265 μmol/L)
Pulmonary edema (radiological)

a pout reflex
reflex may
 may be elicited by stroking the affected. Malaria ARF is defined as having a
sides of the mouth. Lumbar tap usually reveals serum creatinine of more than 265 mmol/L
a normal to elevated opening pressure, clear (3 mg/dL) and a 24-hour urine output of
cerebrospinal fluid  (CSF) with fewer than 10
fluid (CSF) less than 1 ml/kg/hr, despite rehydration, in
leukocytes/mL, and slightly elevated protein and
leukocytes/mL,  patients with asexual forms of the parasite
CSF lactic acid concentration. If left untreated,    present in their peripheral blood smear. The  
symptoms progress to persistent coma and  patient may also present
prese nt with
wit h hyperkalemia
hyperkal emia
death. The neurological complications, once   and hyperuricemia earlier in the course.  
 promptly and adequately
adequately treated, are reversible The cytoadherence, rosette formation, and
and a majority of the patients make a complete sequestration of parasitized erythrocytes lead
recovery.  to a decrease in tissue perfusion resulting in
Respiratory findings are also a major decreasedrenalblood flow.The increase of TNF
feature of severe malaria. Altered pulmonary in tubular epithelial cells leads to inflammatory
function is common, and it includes air flow cell infiltration
infiltration in
 in the interstitium and altered
obstruction, impaired ventilation and gas tubular transport, which result in tubular
transfer, and increased pulmonary phagocytic damage and dysfunction. The presence of GPI
activity.
activity. In African children, pneumonitis from and other falciparum malaria antigens lead to
sequestered, parasitized RBC and inflammatory release of cytokines and mediators thatdecrease
cells are seen in postmortem pulmonary the systemic vascular resistance and increase
vasculature, while in adults, non-cardiogenic
non- cardiogenic renal vascular resistance. All these changes
 pulmonar y edema and acute pulmonary
 pulmonary pulmonar y distress eventually lead to acute tubular necrosis causing
syndrome (ARDS) may be observed. There is a acute renal failure. 
high mortality rate (over 80%) when pulmonary Malaria in pregnancy increases the risk of
edema develops in a patient with severe malaria. maternal death, maternal anemia, intrauterine
Factors which predispose to pulmonary edema growth retardation, spontaneous abortion,
include hyperparasitemia, renal failure, and stillbirth, and low birth weight associated with
 pregnancy.  risk for neonatal death. Non-immune pregnant
The incidence of acute renal failure (ARF) women are susceptible to all complications
reaches up to 60% of patients with severe associated with severe malaria such as cerebral
falciparum malaria, with more males being   malaria, hypoglycemia,
hypoglycemia, and pulmonary edema. 
 

CHAPTER 2: Protozoan Infections   93 

For partially immune pregnant women,  Not everyone infected with the malaria
especially primigravid, severe anemia may  parasite becomes
bec omes seriously
serio usly ill
il l or dies. In
I n areas
develop but the other complications of severe where endemicity is stable, repeated exposures
malaria are unlikely to occur. Falciparum to the parasite lead to specific immunity.  
malaria may induce uterine contractions, thus This restricts occurrence of serious problems
may push
severe the patient
malaria, t he prognosis
the to premature
prognosis of the fetuslabor. In 
is poor. in young mild
relatively children,
febrilewhile older
illness. patients
In people whohave
are 
Falciparum malaria in a young child is exposed to malaria for the first
first time,
 time, possible
considered a medical emergency for it can be outcomes may range from apparent resistance to
rapidly fatal. The initial symptoms may be   death. Any resistance, therefore, is nonspecific.
nonspecific.  
atypical and difficult to recognize, but within It also does not necessarily depend on prior
hours, life-threatening complications may start exposure to malaria and may be either acquired
to occur. The most common complications or innate. Poor prognostic factors in falciparum
of severe malaria in children are cerebral malaria include hyperparasitemia defined as
malaria, severe anemia, respiratory distress, and a peripheral count more than 250,000/µL or
hypoglycemia. Children with severe malaria more than 5% of the RBCs infected, and the
most commonly present with seizures. These  presence of mature or immature schizonts in
convulsions are common before or after the a peripheral blood smear. It has been shown
onset of coma and are significantly associated that a peripheral count of 10% or more of
with neurologic sequelae. Opisthotonos may red blood cells infected has a mortality rate
also be observed in some children. As much as   of 50%, particularly in non-immune cases,  

1w0il%
l doef veclho p elhaeo sucr hvivaes cher m
ildsr eqnuw e bi p
r  alr emsiasl,ar iiaa
 p does p
 p ter otr genatom
or i p sisenitn.cT tosr esncoef
ndai,ca b
luhde cdliene picacloim
cerebellar ataxia, speech disorders, generalized of corneal light reflex, respiratory distress
spasticity, or some behavioral disturbances (acidosis), circulatory collapse, decerebrate
(Table 2.7).  or decorticate rigidity, opisthotonos, and age  

Table 2.7. Comparison of sign and symptoms of sever malaria in adults and children  

Sigo
nsr mptom 
ympt Adults Children
Histoc yff  u gh 
or o Uncommon  
Uncommon Common 

Convulsions  Common  
Common Uncommon  
Uncommon

Dur atioio
lnff  ess 
ln -7ays 
5d 1-d2ays 

Resolutioc
ono
ff   ma  2-d4ays  1-d2ays 

Neur ologicsael quel ae  <5%   >10% 

Jaundice 
Jaundice  Common  
Common Uncommon  
Uncommon 
Pr etr eatmenht ypoglycemia   Uncommon  
Uncommon  Common 

Pulmonaryedema   Uncommon  
Uncommon Common 

a
Renf  illure Common  Uncommon  
Uncommon
CSFopen ingpr essur e  Usu all y
nor m
maal   Usu allyr 
r ais ed 

Respir ator y
distr es(sacidosis)  Sometime   Common 

Bleedin g/clottin g
distur ba
bances  Up10% 
to Rare 
 Abnormal brainstem re flex (e.g., oculovestibular, oculo cervical)   Rare  More common 
 

94  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 below 3 years. Other laboratory indicators of

 poor prognosis include blood glucose <2.2
mmol/L, raised venous lactic acid (>5 mmol/L),
more than three-fold increase in serum enzymes
(aminotransferases), hemoglobin concentration
lessserum
dl, than 5g/dL, blood
creatinine ureathan
more more265
than 60 mg/ 
mmol/L,
 peripheral polymorphonuclear leukocytes
with visible malaria pigment (>5%), low
antithrombin III levels, and very high plasma  
concentrations of TNF.
Diagnosis 
Plate 2.16. Plasmodu
i mfaci arumring form
lp fo rms
s
(Courtesy of the Depa rtment of Parasitolgy,
Parasitolgy, 
Prompt and adequate diagnosis of malaria UP-CPH)
is necessary for the disease to be managed
effectively, thus preventing the life
li fe threatening are not seriously ill, monitoring once daily
complications. Though malaria may present may be sufficient. Seriously ill patients should
with the classic paroxysms of fever with  be monitored two to three
three times daily until
asymptomatic intervals, initial symptoms are significant improvement occurs. Monitoring
non-specific and are not reliable in clinching the should be continued until there is clearance
clearance of
diagnosis. In fact, treatment based on clinical   parasitemia. 

ir nr adtiinognsalaldor nueguussuea.lly r esults in unnecessar y and
fi noi csr 
esta bAlilst heodu dghiagm toicscm
o petihcodi,a tgencohsniiscails atnhde
Microscopic identification of the malarial   personnel requirements often cannot be met,
 parasites in thick and thin blood smears stained  particularly
 particularly facilities in theperiphery
theperiphery ooff the health
with Giemsa or Wright’s stain is still important care system. This has led to the introduction
i ntroduction of
in making the definitive diagnosis and remains the malaria
malar ia rapid diagnostic
diagnostic tests (RDTs).
(RDTs). These
as the gold standard. Specimens may be taken tests make use of immunochromatographic
any time and all blood stages of the parasite may methods in order to detect  Plasmodium -
 be found. In falciparum malaria, only the ring specific antigens in a finger  prick blood sample.
forms (Plate 2.16) may be found, but 10 days Currently, the antigens being targeted by these
after the symptoms begin, gametocytes may be RDTs include: histidine rich protein II (HRP
found as well. Although there are no standard II), which is a water soluble protein
pro tein produced
recommendations on how often the blood  by trophozoites and young gametocytes of P.  P.
smears should be taken in order to diagnose arum; Plasm
 falciparum
 falcip odium lactate dehydrogenase
 Plasmodium
malaria, obtaining smears every 6 to 8 hours (pLDH), which is produced by both sexual 
is usually appropriate. This may have to be and asexual stages and can distinguish between 
continued until a diagnosis of malaria is made  P. falciparumand non- P. falc
falciparum, but not
iparum
or until malaria can be confidently ruled out.
confidently ruled among the non- P. falciparum
falciparum species; and
When malaria is a serious condition, this may odiumaldolase, an enzyme in the parasite
 Plasmodium
 Plasm

require repeatedatesting
to demonstrate positiveforresult.
several daysafter
Even in order
the
glycolytic pathway expressed by the blood
stages of all  Plasmodium species. Together
diagnosis of malaria has been made, peripheral with HRP II,  Plasmodium aldolase has been
 blood smears should still be obtained
obtaine d to monitor used in a combined immunochromatographic
the response to treatment. In individuals who   test targeting the panmalarial antigen (PMA).  
 

CHAPTER 2: Protozoan Infections   95 

These tests can be performed in 15 to 30 differentiate between currentand pastinfections

minutes without the use of electricity, special and are therefore most helpful in epidemiologic
equipment,, or any training in microscopy, and
equipment studies. Current studies are using PCR to
most kits
kit s have more than 90% specificity. More significantly enhance microscopic diagnosis of
recent studies have shown that test kits based malaria especially in cases of low parasitemia
on HRPand
92.5% II have
98.3%a sensitivity
respectively,and specificity
while  of 
kits based and in cases of mixed infection.  
on the pLDH antigen have a lower sensitivity Treatment 
(88.5%) albeit a higher specificity
specificity at
 at 99.4%. Antimalarial drugs have selected actions
The use of RDTs can be easily taught to village   on the different phases of the life cycle of the
health workers and the results can likewise be malaria parasite. These drugs may be classified
easily interpreted. The main disadvantages into causal prophylactic drugs, which prevent
of RDTs compared to microscopy are: the the establishment of the parasite in the liver,
lack of sensitivity at low levels of parasitemia; and blood schizonticidal drugs, which attack
the inability to quantify parasite density; the the parasite in the red blood cell, preventing
inability to distinguish among P
 P.. vivax, P. ovale,
ovale or terminating the clinical attack. Tissue
and P. malariae, as well as sexual and asexual
malariae schizonticides act on pre-erythrocytic forrns
stages; the persistently positive tests (for some in the liver. Gametocytocidal drugs destroy
antigens) despite parasite clearance following the sexual forms of the parasite in the blood.
chemotherapy; and the relatively higher cost Some drugs are hypnozoitocidal or antirelapse
 per test.  drugs, which
whic h kill the dormant
dormant forms in the liver.  
of  thIenPr ehcile p  bcetetdhien valir dioituys oaf r ea s
in pt sintueds iteos cdoenscdr ui b So pf othr oe notoi ciydsatsl  odnr utghse  ignuhti bwiatlltohf e thdevm
elo p uietnot,
sqm
few specific malaria RDT kits, results showed which has fed on a gametocyte carrier so that
sensitivity and specificity levels below the the mosquito cannot transmit the infection.  
WHO recommended ideal of 95% and 90%, The main uses of antimalarial drugs are:  
respectively. Reasons for these findings could  bbee
respectively. (a) protective (prophylactic), (b) curative
manufacturer-related
manufacturer-related problems, the instability (therapeutic), and (c) preventive. Drugs for
of the substances used in the diagnostic  prophylaxis
 prophyl axis are used before the infection
infecti on occurs
technique to varying environmental conditions or before it becomes evident, with the aim of
such as extremes of temperature and humidity,  preventi ng either the occurrence of the infection
 preventing
anduser-relatedproblems.Quality assuranceof or any of its symptoms. A blood schizonticidal
these malaria RDT kits is, therefore, necessary drug may have minimal effects on parasites
 before they
they are deployed on
on a larger scale
scale in growing in the liver, but if it is still present in
remote and rural areas. More recent studies are the blood when the merozoites leave the liver
now concentrating on quality assurance of these  and invade the blood cells for the firstfirst time,
 time, it
tests and on identifying the factors which may will effectively prevent symptomatic malaria.
affect RDT performance in the field.  Curative or therapeutic use refers to action on
Malaria can also be diagnosed serologically the established infection, which involves the use
 but presently available methods are not of blood schizonticidal drugs for the treatment
capable of making a definitive
definitive diagnosis
 diagnosis of of the acute attack and in the case of relapsing
acute malaria. Available serologic tests like malaria, radical treatment of the dormant liver
indirect hemagglutination (IHA), indirect forms. Prevention of transmission means the
fluorescent antibody test (IFAT), and enzyme-
enzyme - deterrence of infection of mosquitoes with  
linked immunosorbent assay (ELISA) cannot   the use of gametocytocidal drugs to attack the  
 

96  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

gametocytes in the blood of the human host. It  be given in pregnancy

pregnanc y and in children less than
also means the interruption of the development 4 years of age. 
of the sporogonic phase in the mosquito when In contrast with falciparum malaria, vivax
it feeds on the blood of an infected person who malaria remains sensitive to chloroquine.
chloroquine. Clinical
has been given the appropriate sporonticidal studies and extensive in vitro observations have
compound.  
Chloroquine was the mainstay of   shown that P. although
chloroquine, vivaxis still
regenerally
sistance issensitive
resistance prevalentto  
antimalarial treatment for the last 50 years. and increasing in Indonesia, Peru, and Oceania.
Because of emergence of multidrug-resistant Moreover, vivax malaria is sensitive to all other
(MDR) strains, subsequent chloroquine use  antimalarial drugs albeit slightly less sensitive to  
has been rendered ineffective against falciparum artesunate plus sulfadoxine-pyrimetham
sulfadoxine-pyrimethamine. ine. The
malaria, and the current DOH Malaria asexual stage of  P. vivaxremains susceptible to
Control Program (MCP) recommends the use  primaqu primaquine;ine; therefore,
theref ore, combination
combin ation treatment
t reatment
of artemisinin-based combination therapies with chloroquine and primaquine affords blood
(ACTs) for severe and uncomplicated
u ncomplicated falciparum stage and liver stage treatment, respectively.
malaria, replacing the chloroquine plus Often referred to as radical treatment, the use of
sulfadoxine-pyrimethamine combination. The  primaqu
 primaquine,ine, together with chloroquine,
chloroq uine, allows
following drug combinations are recommended: for the prevention of relapse in vivax malaria. In
artemether plus lumefantrine, artesunate plus comparison with no primaquine treatment, the
amodiaquine, artesunate plus mefloquine,  risk of relapse decreases for every additional mg/
and artesunate together with sulfadoxine-   kg of primaquine given. Repeated vivax malaria  
anyr tim aeltahr aiaml itnr e.atFmoer nstevsehr oeum
 p lda blaer iiaast, p
ar taer denter al r melua psts bese  p
ar r e  vde b
ntielidta. tAintgleatstanay14ag-de,ayhecnocuer steheoyf
without delay after rapid clinical assessment and  primaquine
 primaqu ine is needed for the radical treatment
confirmation of
confirmation of the diagnosis. The following of  P. vivax
vivax. 
antimalarial drugs are recommended:
recommended: artesunate Resistance of  P. malariae and  P. ovale
intravenous (IV) injection or intramuscular to antimalarials is not well characterized,
(IM) injection, quinine IV or IM, or artemether and infections with these species are still
IM. In a placebo-controlled trial, patients with considered sensitive to chloroquine. The
severe malaria who could not be treated orally treatment for relapsing fever caused by  P.  P.
and where access to IM and IV treatment was ovale is similar to that of vivax malaria (i.e.,
unavailable, a single artesunate suppository at chloroquine and primaquine). In the case of
the time of referral reduced the risk of death or mixed malarial infections, ACTs remain the
 permanent disability.  mainstay treatment. Moreover, the use of
Current guidelines also recommend   artemisinin-based compounds and a partner
the use of gametocytocidal drugs to reduce   drug with a long half-life (i.e., artesunate  
transmission. Seen in the context of malaria  plus amodiaquine and dihydroartemisinin
elimination, the use of primaquine 0.75  plus piperaquine)
pip eraquine) has been effective
eff ective against
again st
mg base/ kg body weight single oral dose   in chloroquine-resitant vivax malaria. Radical
demonstrates an added benefit to artemisinins treatment with primaquine should also be  
in eliminating gametocytes.toThe addition considered in cases of confirmed  P. vivax and 
single dose of primaquine current ACTsofisa  P. ovaleinfections.
therefore recommended provided that the risk Artemisinin and its derivatives ( Qinghaosu
for hemolysis in G6PD deficient patients is derivatives), artesunate, and artemether produce
considered. Moreover, primaquine should not   rapid clearance of parasitemia and rapid  
 

CHAPTER 2: Protozoan Infections   97 

resolution of symptoms. Because artemisinins of therapy. Resistance of a parasite to drugs

are rapidly eliminated in the body
body,, the duration is graded according to the patterns of asexual
of treatment is dependent on the partner
p artner  parasitemi a after initiation
 parasitemia initiat ion of treatment (Figure
drug being short acting or long acting. When
Wh en 2.16). RI is the mildest form of resistance which
 partnered with rapidly eliminated drugs is characterized by initial clearance of parasites
(tetracyclines
(tetracycline
of treatments is
andusually
clindamycin), a 7-day
required. course 
Treatment  but
the recrudescence occurs
start of treatment. within
It can a month after
be classified
classified as
 as 
duration can be reduced to 3 days when either early, when clearance occurs for the first
artemisinins are given in combination with 48 hours and recrudescence takes place within
slowly eliminated drugs such as mefloquine
mefloquine   the first 14 days after start of treatment, or late 
and amodiaquine. An additional advantage when there is also clearance within the first 48
from a public health standpoint is the ability hours and recrudescence occurs within the 14 th
of artemisinins to reduce gametocyte carriage, to the 28th day from the start of treatment. RII  
thus reducing the transmission of malaria. This
form of malaria control is particularly useful in
areas of low to moderate endemicity.  
Quinine sulfate plus doxycycline or
clindamycin serves as the second line drug when
artemisinins (e.g., IV artesunate) are unavailable
or when there is failure to respond to artemisinin
therapy.
therapy. The tetracyclines and clindamycin are  
kthneoywknilltot b r   salloawr ialyls. , Qaluthinoiungeh
r eacsittiever atnhteim
  eaf f 
h e p
has the disadvantage of producing toxic side
effects such as cardiotoxicity and cinchonism,
characterized by tinnitus, headache, and
 blurringg of vision.
 blurrin visi on. Also, rapid
r apid administration
administrat ion
of quinine is unsafe. Each dose of parenteral
quinine must be administered as a slow rate-
controlled infusion, and electrocardiographic
electrocardiographic
(ECG) monitoring and frequent assessment of
vital signs are required if quinines are used. Due
to the risk of congenital defects, tetracycline
is contraindicated in pregnant women and
children below 8 years.
years. Rather, quinine plus 
clindamycin taken for 7 days remains the
antimalarial of choice in pregnancy.  
The problem of drug resistance involves 
mainly chloroquine plus sulfadoxine- Figure 2.16. A WHO field test for response of
 pyrimethamine and certain strains of  P. malaria parasites to chloroquine 

 fal cip ar um . Such strains are often MDR.

arum (From World Health Organization. Chemotherapy
of malaria and resistance to antimalarials:
Asexual parasites are normally cleared from r e po r t o f a WHO sc ie ntif ic  gr o up. Tec hnic al
the blood three days after the start of treatment report series no. 329. Geneva: World Health  
and are definitely cleared 6 or 7 days after start  Organization; 1973.)
 

98  MEDICAL PARASITOLOGY IN THE PHILIPPINES 

shows an initial reduction in parasitemia after without previously meeting any of the criteria
treatment but there is failure to clear the blood of ETF; and (b) presence of parasitemia and
of asexual parasites and soon after an increase an axillary temperature of 37.5°C (or history
of parasitemia follows. RIII is the severest form of fever) on any day from Day 4 to Day 28,
of resistance in which parasitemia will either without previously meeting any of the criteria
show no significant
will eventually   with treatment oorr
change
increase. for ETF. Late
Late parasitological
transmission areas is definedfailure
defined as for intense
 as presence of  
MDR malaria is considered when treatment  parasitemi a on Day 14 and axillary temperature
 parasitemia
failure occurs with three or rnore antimalarial of 37.5°C without previously meeting any of the
agents. In this case, a combination of artesunate  criteria for ETF or late clinical failure.  
has been combined with mefloquine and is now For low to moderate transmission areas,
the first-line regimen for MDR malaria in some late parasitological failure is defined as presence
Southeast Asian countries.  of parasitemia on any day from Day 7 to Day D ay
Classification of response to malaria 28 and axillary temperature of 37.5°C without
treatment can be divided into early treatment  previou sly meeting any of the criteria for ETF
 previously
failure, late treatment failure, and adequate or late clinical feature. Adequate clinical and
clinical and parasitological response. Early  parasitol ogic response for intense transmission
 parasitologic
treatment failure (ETF) is present when there areas is defined as absence
abs ence of parasite
parasitemia
mia on Day
is: (a) development of danger signs or severe 14 (Day 28 for low to moderate transmission
malaria on Day 1, 2, or 3 in the presence of areas) irrespective of axillary temperature
 parasitemia;
 parasitemi a; (b) parasitemia
paras itemia on Day 2 higher 
hi gher   without previously meeting any of the criteria of  
than petr haetuDr ea;y(c0)  pcoaur anstitier m
em r eis p
a eocntivDe aoyf  3axwililtahr y iluF,r ela. te clinical f aaiilur e, or  late p
f EaT  par asitological
axillary ternperature of 37.5°C; and (d) In cases of renal failure in severe malaria, 
 parasitemia on Day 3 which is 2 25%
5% of count dopamine may be given at 3 to 5 µg/kg/
on Day 0. This classification
classification of  of ETF holds for minute. If the patient remains unresponsive
 both intense transmission
transmi ssion and low to moderate despite adequate rehydration and other forms
transmission areas. Late treatment failure (LTF) of therapeutic management, and blood urea
is further divided into late clinical failure and and creatinine are rising progressivel
progressively,
y, dialysis
late parasitological failure. The definitions for is indicated. 
these two would differ depending on whether For control of seizures, diazepam may be
the area is an intense transmission area or a given at 10 mg intravenous (pediatric dose at  
low to moderate one. Late clinical failure for 0.3 mg/kg IV up to 10 mg) or in cases of status
intense transmission areas is defined as: (a) epilepticus, phenytoin at a loading dose of 13
development of danger signs or severe malaria  to 18 mg/kg and a maintenance dose of 3 to 5
after Day 3 in the presence of parasitemia,  mg/kg per day (pediatric dose: loading dose of  
without previously meeting any of the criteria 15-20 mg/kg slow IV push and maintenance
of ETF; and (b) presence of parasitemia and dose of 5 mg/kg in two divided doses). The
axillary temperature equal to or greater than following are now not considered useful and are
37.5°C on any day from Day 4 to Day 14, therefore not recommended in the management 
without previously meeting any of the criteria
for ETF. For low to moderate transmission
of cerebral malaria: corticosteroids, other anti-
inflammatory agents, low molecular weight
areas, late clinical failure is defined as: (a) dextran, epinephrine, and heparin. 
development of danger signs or severe malaria Proper management of malaria also
after Day 3 in the presence of parasitemia,   includes general and supportive measures  
 

CHAPTER 2: Protozoan Infections   99 

especially in P. falciparum infections. If fluid malaria have shrunk considerably over the past
replacement or blood transfusion is necessary,
necessary, 50 years, but control is becoming more difficult,
it must be administered with care to avoid and past gains have been threatened. The spread
 pulmonaryy edema. Antipyretics
 pulmonar Antipyr etics and sponging
spongin g of the disease is linked to activities like road
for high fever are important especially in  building,
 buildin g, mining, logging, and new agricultural
agricultur al
childrenbetomonitored
should prevent convulsions. Blood sugar
regularly especially in   and
areasirrigation projects,
(e.g., forest fringe,particularly in “frontier”
mountain valleys and  
severe malaria. If hypoglycemia develops, 50 reclaimed areas). Elsewhere, disintegration
mL of 50% dextrose (1.0 mL/kg for children) of health services, armed conflict, and mass
diluted in an equal volume of infusion fluid  movements of refugees have worsened the  
should be infused over a 5-minute period, malaria situation.  
followed by a continuous intravenous infusion Malaria remains a public
pu blic health problem
of 5 to 10% dextrose.  today in more than 90 countries inhabited by
Epidemiology 
a total of some 3.3 billion people (Figures 2.17
to 2.19). Of these, 2.1 billion are at low risk
Malaria is the world’s most important (<1 case per 1,000 population), 94% of whom
tropical parasitic disease. The disease kills live in areas outside the WHO African region.
more people than any other communicable The 1.2 billion at high risk (>1 case per 1,000
disease except tuberculosis. In many developing
developing  population) live in the WHO African (47%)
countries, especially in Africa, malaria has an and Southeast Asian Regions (37%).
enormous toll on lives, medical costs, and days   In 2010, the WHO reported an estimated
of labor lost. The geographical areas affected by  216 million cases of malaria, of which 81% or  

Figure 2.17. Global distribution of malaria: malaria-free and malaria-endemic countries in phases of
control, elimination and prevention of reintroduction ( From W orld Health Organization. World Malaria
Report 2009. Geneva: World Health Organization; 2009.)
 

100   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

ineaAthf rr si coac,caunrr deda pi pnr 2o0xi1m0a, t9e1llyy%86o%
d se r e
f  wohf icthew
deaths were children under 5 years of age.
The estimated incidence of malaria has fallen
 by 17% globally between 2000 and 2010.
Large percentage reductions were seen in the
European (99.5%), American (60%), and
Western Pacific (86%) WHO regions. Likewise,
malaria specific mortality rates have fallen  by
25% between 2000 and 2010.  
According to the World Malaria Report
2011, the WHO cites a decreasing number
of malaria cases in a majority of countries
 belonging to the Western Pacific Region. A
greater than 50% decrease in cases were reported 
for China, Philippines, Republic of Korea,
Figure 2.19. Distribution of malaria i n the WHO Solomon Islands, and Vietnam, while a 25-50% 
Western Pacific Region: areas in red indicate decrease in the number
numb er of cases were seen
seenin Lao
malaria-endemic countries  People’s Democratic Republic, Malaysia, and
(Accessed from http://www.map.ox.ac.uk)  Vanuatu.
Vanuatu. No notable change in the number of
malaria cases were seen in Cambodia and Papua
171 million cases where in the African region,  New Guinea. 
with the Southeast Asian Region accounting for In the Philippines, malaria has not been
another 13%. An estimated 655,000 malaria   included among the 10 leading causes of  
 

CHAPTER 2: Protozoan Infections   101 

Figure 2.20. Malaria cases per 100,000 population in the Philippines from 2000 to 2009  
(From Department of Health-National Center of Disease Prevention and Control. Malaria medium term
development plan 2011-2016. Manila (Philippines): Department of Health; 2011.)  

morbidity since 2006. Cases have been notably reported in 2009 (Figure 2.21). Similarly, the
decreasing as reported in 2009 (Figure 2.20).
2.20). malaria morbidity rate has decreased by 58.3%,
However, disease prevalence,
prevalence, seen in the 2010 with 18,781 malaria cases reported in 2009.
DOH-Malaria Control Program (MCP) Among blood smears examined from 2005 to
report, remains markedly high in Regions   2009, 69.4 to 80% of patients were diagnosed
IV-B, Caraga, III, XII, and II. There remains with P. falciparum, 17.0 to 23.4% with P.vivax,
falciparum
an estimated 10.8 million people still at risk approximately 1% with P malariae, and a small
 P.. malariae
for the disease, consisting mostly of farmers, number of cases (0.5%) were diagnosed to have
indigenous cultural groups, miners, forest mixed malaria infection, falciparum and vivax
 product gatherers, and soldiers
soldiers.. Fifty nine out of malaria being the usual mixed infection.  
the 80 provinces in country are endemic for the Macrostratification of malaria endemic
Macrostratification
disease, with 60.4% of the endemic provinces areas serves to classify the different provinces
located in Luzon, 39.5% in Mindanao, and   based on annual incidence of the disease 
0.1% in Visayas. As of 2009, the provinces of in each respective province (Table 2.8).
Cagayan, Isabela, Palawan,Sulu, and Tawi-Tawi  Macrostratification
Macrostratifica tion provides an opportunity 
opportunity  
comprise the five provinces having the highest for planning, policy making, and resource
number of malaria cases reported.   allocationn of the provincial MCP. The number
allocatio
It appears that in areas of low malaria of provinces in Category
endemicity, there is a clustering of cases, from 26 in 2000, to nine inA2005
has and
beenfinally
reduced
finally  to
to
resulting in pockets of high endemicity. five in 2008. The values reported for Category
Mortality rate for malaria has markedly B provinces have changed from 22 in 2000 to
decreased by 88.2% from 2005 figures to values  31 in 2005, and to 27 in 2008. Malaria-free  
 

102   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Figure 2.21.
2.21. Malaria-related deaths per 100,000 population
population in the
the Philippines from 2005 to 2009
(From Department of Health-National Center of Disease Prevention and Control. Malaria medium term
development plan 2011-2016. Manila (Philippines): Department of Health; 2011.)  

Table 2.8. Macrostratification of malaria Philippines, the principal malaria vector is

endemic provinces according to annual  flavirostris , a night biter,
 Anopheles minimus var. flavirostris
incidence of malaria  
which prefers to breed in slow flowing,
flowing,  partly
shaded streams that abound in the foothill areas.
Occasionally, it has the ability to adapt to or
utilize new habitats such as irrigation ditches,
rice fields, pools, and wells. In Palawan, it was
observed to be mildly exophagic and zoophilic.
Its horizontal flight range has been reported
to be about 1 to 2 km.  Anopheles litoralis
litora lis is
associated with malaria transmission in the
coastal areas of Mindanao, particularly in Sulu. 
 provinces have increased from 13 in 2000, to  Anopheles
 Anopheles maculatus coexists with A.
maculatus  A. flavirostris 
 flavirostris
22 in 2009.
20 09. Four province
provincess in Category A, eight   in the portion of streams exposed to sunlight.  
 provinces in Category
Categ ory B and eight provinces
pr ovinces They appear to be responsible for malaria
in Category C have been reclassified
reclassified to
 to the transmission at higher altitudes.  Anopheles

immediate lowerNueva
categories mangyanus has the same breeding habitats and
2005 to 2009. Ecijarespectively,
is noted tofrom
have seasonal prevalence as A. flavirostris
 A. flavirostris  but
  but appears
appears
shifted into a higher category (Figure 2.22).   to prefer habitats located in forest fringe.  
Peakk transmission occurs at the
Pea t he beginning Malaria can also be transmitted through
and at the end of the
the rainy season. In the   blood transfusion from infected donors, and 
 

CHAPTER 2: Protozoan Infections   103 

Figure 2.22. Macrostratification of provinces in the Philippines according to category by average

malaria cases: note that the Isabela, Cagayan, Palawan, Sulu, and Tawi-Tawi remain  

Category A provinces as of 2008 (From Department

and Control. of Health-National
Malaria control Center
program. 2009.)   for Disease Prevention  

 by contaminated
contaminat ed needles and syringes.
syring es. Blood  breeding sites, and estimation
est imation of mosquito
mosq uito
from semi-immune donors without clinical density. 
symptoms may contain malaria parasites. In Prevention and Control 
congenital malaria, infected mothers transmit
 parasites to their child before or during birth.  Early diagnosis and prompt treatment
The evaluation of the amount and of malaria are essential for malaria control. 
conditions of transmission of malaria in a Breeding sites of  Anoph
 Anopheles
eles fla
flavirostris should
virostris
given locality is called the malaria survey.  be detected early and contained. Personal
Disease control efforts must always take into  protection
 protecti on measures
measur es against mosquito
mosquit o bites
consideration the findings of the malaria   are also helpful and cost-effective. The use  
survey. The survey involves looking into of insecticide- (permethrin or deltamethrin)
epidemiologic data regarding the disease, such as 
epidemiologic treated nets (ITNs) and long lasting insecticide- 
malaria mortality and morbidity, investigations treated nets (LLIN) remains the major vector
relating to the human host, and investigations control strategy coupled with indoor residual
relating to the insect vector. Investigations spraying
relating to the human host include blood and situations,(IRS),
areaswith
withthestable
lattertransmission
used in epidemic
but
spleen examinations. Investigations relating without reduction of malaria incidence, and
to the vector, on the other hand, may include areas of displaced populations. Wearing of
identification of
identification  of mosquito vectors and their   light colored clothing, which cover most of the 
 

CHAPTER 2: Protozoan Infections   105 

 body (since dark colors attract mosquitoes), and rice fields and bacterial insecticide (PG-14
using insect repellants containing DEET  Bacillus thuringiensis ), and chemical control
(N,N-diethyl-m-toluamide, optimally as a 35% such as the use of mosquito repellants and
concentration lotion) on exposed parts of the insecticide treated mosquito nets. 
 body, using a insect spray containing
containing pyrethrum
pyrethr um In the field of molecular entomology,

in living
as areas,spray
a repellant and use
forofclothing
permethrin
haveinsecticide stable germline
known to   mosquito transformation
is being the  Anopheles
investigated.ofThis research 
 be effective personal protection
protectio n measures as well.   involves inserting genes (e.g., immune response
Chemoprophylaxis may be protective to   genes) that will inhibit the development of
travelers who have no immunity to malaria, the parasite in the mosquito. With the recent  
although no chemoprophylactic regimen sequencing of the genomes of  Plasmodium
ensures 100% protection. Because of this, iparu m and of the  Anoph
 falciparu
 falc eles mosquito,
 Anopheles
 precautions to avoid mosquito bites are new areas of research for malaria treatment and
needed even if antimalarials have been taken.  prevention are n
now
ow being explored. 
Prophylactic drugs should be taken with good References 
compliance for the duration of the stay and
should be continued four weeks after the last Anstey NM, Jacups SP, Cain T, Pearson, T,
 possible exposure
exposure to infection
infection since the parasites
parasites Ziesing PJ, Fisher, DA, et al. Pulmonary
may still emerge from the liver after this period. manifestations of uncomplicated
An exception would be atovaquone/proguanil falciparum and vivax malaria: cough, small
which can be stopped one week after return.  airways obstruction” impaired gas transfer,  

whelor er om
C lymdeunedteod P f .or viavr a x
quailnar eiaisisoenxlcylur esicvoem eaos r anctdiviitnyc.r JeaIsnef dec pu is.o2n0a0r y2; p85h(a9g)o:1cy3t2ic6 – 334.
t Dlm 4. 
where there is low risk of chloroquine-resistant  Beeston JG, Brown GV. Pathogenesis of
 P. falciparum. Those traveling to areas where
falciparum falcipar um malaria: The roles
 Plasmodium falciparum
levels of resistance to chloroquine are high may of parasite adhesion and antigenic variation.
use mefloquine, doxycycline or atovaquone/ Cell Mol Life Sci. 2002;59(2):258 – 
2002;59(2):258 – 2
27.7. 
 proguani l. Strategies
 proguanil. Strateg ies implemented
imp lemented to control Belizario VY, Pasay CJ, Bersabe MJ, de Leon
malaria in pregnancy include the use of ITNs
I TNs WU, Guerrero D, Alcantara S, et et al.
and intermittent preventive treatment, which Field and laboratory evaluation of rapid
involves providing all pregnant women with at diagnostic test for malaria. Final report
least two preventive treatments of an effective 2003. Geneva: World Health Organization;
antimalarial drug. 2003. 
Work is on-going
on-going for the development of Belizario VY, Saul A, Bustos MDG, Lansang,
an effective malaria vaccine. Among the vaccine MA, Pasay, CJ, Gatton M, et al. Field
types being developed are the “sporozoite”  epidemiologic studies on malaria in a
vaccines, “asexual”  vaccines, and the “altruistic” or known endemic community in Bataan.
 
“transmission blockin
 blocking”g”  vaccines. Combination Acta Trop. 1997;63:257
1997;63:2 57 – 6
66.
6.
vaccines derived from multiple parasite life stages Bustos, MD. Clinical aspects, chemotherapy,
chemotherapy,
are also being
b eing developed.  and drug resistance. In: Philippine Council
Malaria control also includes proper for Health Research and Development.
vector control. This can be done through State of the art: malaria research in the
environmental modification, biological control Philippines. Taguig: Departmentof Science
which includes using larvivorous fish in streams   and Technology; 1999. 
 

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Bustos MD, Saul A, Salazar NP, Gorres NA. Myjak P, Nahorski W, Pieniazek NJ, Pietkiewitcz  
Profile  of Morong, Bataan, an area of low
Profile H. Usefulness of PCR for the diagnosis of
malaria endemicity in the Philippines. Acta imported malaria in Poland. Eur J Clinl
Trop. 1997;63:198 – 208.
208. Microbiol Infect Dis. 2002;21(3):215 – 88.. 
Cabrera BD, Ramos OL, Cruz LT. Malaria Serghides L, Kain KC. Mechanism of protection
transmission
water breederby Anopheles,littoralis,
inPangutaran,
inPangutaran Repaublic
salt 
Sulu, Republic induced by Vitamin
malaria.Lancet. A in falciparum
2002;359(9315):1404 – 66.. 
of the Philippines.
Philippin es. Southeast Asian
Asi an J Trop
Trop Warrell DA, Molyneux ME,
M E, Beales PF.Severe
Med Public Health. 1997;193 – 204.
204. and complicated
complicate d malaria. 2nd ed. Trans
Trans R
De Las Llagas LA. Malaria vectors and vector Soc Trop Med Hyg. 1990;81:521.
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art: malaria research in the Philippines. Geneva: WorldHealth Organization;199
Organizati on;1994. 4.  
Taguig: Department of Science and World Health Organization. Chemotherapy of
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De paor ntm oseisaaltnhd. tPr ehaitl pp
thendt iaogf nH r  malalr air aia.
imenint ef om Wor r  or et a2lt0h09O. r Ggaeniezvat:ioW
lde pH n.or 
W r ldeam
ldoH lthala r iiaa
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66.
 

CHAPTER 2: Protozoan Infections   107 

Babesiaspp.
Florencia G. Claveria 

abesia spp. is a hemosporidian parasite that infect

that causes babesiosis, a hemolytic disease   smaller andred blood
can cells
easily be (RBCs)
(RB Cs) are generally
misidentified.   Babesia 
 Babesia 
commonly referred
referred to as tick, splenic, redwater, spp. are largely host-specific,
host- specific, and
 and non-host
Texas, or Nantucket fever.  Babesia was first specific species utilize only a narrow range
documented in cattle in 1888 by Dr. Victor of mammalian hosts like cattle and rodents.
Babes, a Romanian scientist, who described  Some species infecting mammals exhibit cross-
cross- 
symptoms of severe enzootic hemoglobinuria. infectivity and induce cross-immunity between
 Babesia has a worldwide distribution and host species. 
comprises approximately 73 to 100 species Hard ticks (family Ixodidae) are the
infecting wild and domestic animals, as well known biological hosts of  Babesia, however,
 Babesia
as humans. Babes ia spp. are generally specific
 Babesia transmission of  Babesia by the soft tick,
to their vertebrate hosts, and are transmitted Ornithodoros erraticus has been reported. Tick
 by Ixodidae or hard ticks. In humans, species that have been established as putative
transmission through blood transfusion, organ vectors are  Boophilus spp.,  Rhipi
 Boophilus cephaluss spp.,
 Rhipicephalu
transplantation, and transplacental route have  Ixodes spp.,  Hyalomma spp.,  Haemaphysal
 Haemaphysalisis
 been documented.  spp., and  Dermace ntor spp. Of the 53 tick
 Dermacentor

esti bc  a bneim
domA si aolsi,s itaf uf nedctesnia bw der inr gasnga beoouf t
lyi b  bs peecnier secinogcr niimzeidn.atTedheatsr avnescm
toir sss,ioonnltyo 1h7um
havnes
huge economic losses to agriculture. The of the rodent B. microti and the cattle forms of  
increasing association between man and animals ia is generally associated with Ixodesspp.
 Babesia
 Babes
has resulted in increased infection, not only Unlike the genus Plasm odiumand Theileria, 
 Plasmodium
among the immunocompromised individuals  Babesia does not undergo exo-erythrocytic
 but also among the general populace. To merogony; daughter progeny are not housed in
increase public health awareness, a better  parasitop horous vacuoles; and residual bodies
 parasitophorous
understanding of the parasite biology and   are usually non-existent in infected RBCs.  
its tick vector, the disease it causes, and its The  Babesia life cycle undergoes three
epidemiology particularly in the Asia- Pacific, developmental phases. In the mammalian
is imperative.  host, (a) merogony in the RBC;
RBC ; and in the tick
vector, (b) stages of gamogony in the gut and
Parasite Biology 
epithelium; and, (c) sporogony accompanied
 Babesia is a heteroxenous
heteroxenous parasite requiring with multiple fission in various cells and organs  
mammals as primary hosts, and ticks as forming sporokinetes, and the development of
intermediate hosts or vectors. On account of infective sporozoites. A few hours after blood
the disparity in the morphological features   ingestion, the intra-erythrocytic merozoites in
of the intra-erythrocytic forms in different the gut of engorged ticks undergo morphologic,
host species, there exist about 100 species or  physiologic/metabolic, and antigenic 
forms. The tendency of Babes ia spp. to take on
 Babesia changes, and differentiate into gametocytes
 pleomorphic
 pleomorp hic forms in different
differe nt hosts obscure
obscur e that eventually develop into gametes. Post-
their identification
identification at
 at the species level. For fertilization, the zygote begins to infect the
example, its close relative, the Theileria spp.  gut epithelial cells where it undergoes multiple 
 

108   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

fission, and eventually forms sporokinetes. Once the organs of the larva, nymphs, and adult
the sporokinetes are released, they continue to ticks. With the stage-to-stage (transstadial)
infect and multiply in various organs, including transmission, each of the developmental
developmental stages
the ovaries of the replete tick, until death ensues. is generally capable of parasite transmission to
The transovarian route represents one pattern mammals. The complicated phase of  Babes
 Babesia
ia

of parasite transmission
terminates with the deathinofthe
thevector,
vector.which
  life cycleof
formation inthe
theinfective
tick vector ends with
sporozoites the  
in various
With the passage of sporokinetes to eggs organs or in the salivary glands, for subsequent
(transovarian), similar cycles of multiple fissions transmission to the mammalian hosts during
continue to take place in the embryo and in   blood feeding (Figure 2.23). 

Pathogenesis and Clinical Manifestations  bigemina (4-5 µm by 2-3 µm) and  B. caballi (3
µm by 2 µm) are less virulent. Several factors can
Smaller forms like  Babesia bovis (2.4 µm
 Babesia
influence the susceptibility of hosts to infection,
 by 1.5 µm) and B. equi
equi (2 µm by 1 µm) are
like the age and breed of farm animals, and the
more pathogenic, while larger forms such as B.  health and immune state of humans.  
 

CHAPTER 2: Protozoan Infections   109 

Both innate and acquired immunity Diagnosis 

contribute to the resolution of the primary
 Babesia
 Babes ia parasites are usually detectable in
infection and provide protection against
subsequent exposures. The importance of the  blood smears only during the acute stage of the
t he parasites infection, and animals that survive the initial
spleen in the elimination of both the
infection can become lifelong carriers. Previous
and infected RBCs
susceptibility is seen in the
of splenectomized orincreased
inherently   infections can be demonstrated serologically.  
asplenic mice to infection. Murine hosts osecf oi pnitciveexadmiaignnaotisoisn r eoqf  uGir ieesmdsiar -esctai
micr D t ned
depleted of macrophages exhibit either high
mortality or become unprotected when exposed.    peripheral blood smears for the presence  
The transfer of primed macrophages, as opposed of Babesia , showing its established unique
to transfer of primed
prime d T-cells,
T-cells,provides protectio n morphological features. To rule out the
provid es protection
against B. microt
microtii in naive mice. The resolution
misdiagnosis from closely related hemosporidians
hemosporidians
like  Plasmodium spp., and the causative agents  
of babesiosis is principally mediated by gamma
interferon produced by CD4+ T helper-1
h elper-1 cells, of Lyme disease, and granulocytic erlichiosis
infecting humans, the parasite dimensions
alongside macrophage activation. While B  
cell-depleted mice are capable of controlling and pleomorphism (ring form, pear-shaped,
 primary infection,
i nfection, antibodies
antibodi es are still useful and “Maltese cross” or tetrad form) need to be
in the clearance of extracellular parasites in
ascertained, including the absence of pigments
in infected RBCs. In cases of low-grade
circulation. Despite low parasitemia in the
 peripheral circulation
circulatio n among infected
i nfected cattle,  infection or parasitemia, detection can be very
difficult, thus, appropriate serological assays, 
er eydths r coacuystiensgacr er s b
icna pf eiclltaer dy  b eqr uale b
stea br  edsioinsist,hae molecular gene analyses, and epidemiologic
epi demiologic
similar manifestation of falciparum malaria.  data, including data on ticks and reservoir
In humans, infections with B. microti or
or carrier hosts (epizootiological), may be
extremely useful.  
microti-like species may be asymptomatic
 B. microti
Several serological tests are generally
or may result in mild to severe clinical signs
and symptoms. Fatigue, malaise, anorexia, and employed for the detection of babesiosis. The
immunofluorescent assay (IFA) is widely used
weight loss begin to manifest approximately
one to six weeks post-exposure followed  
in acute cases and in epidemiological studies.
Although sufficiently
sufficiently sensitive,
 sensitive, IFA has the
 by non-periodic or intermittent fever (38-
following drawbacks: non-differentiation
40°C), chills, and sweats accompanied
with headache, myalgia, arthralgia, nausea,  between active and past exposures, possibility
possibilit y
of cross-reactivity between antigens of
vomiting, and prostration. The patient may
also manifest emotional lability, depression,   closely related species, and subjectivity in the
quantification of the intensity of fluorescence.
fluorescence.  
and hyperesthesia. In severe cases, hemolytic  
anemia and hemoglobinuria with jaundice  w.er mdiiclur otit oi nasnatni b
aAnttlio- B
 B.  bdoduier sincgr otss wihthase,
he-r aecaucte p
 become apparent, with pulmonary edema being antigens of other Babes  Babesia ia spp. Also, antigens of  
the most frequently observed complication 
microti occasionally cross-react
 B. microti cross-react with sera of
of the disease. The severity of infection with
 possible fatal outcome is generally associated titer. Torule mout
confirmed alarial casescross-reactions
possible with aeactions,
cross-r >1:16 antibody
, a 1:64
with the elderly, the splenectomized and
immunocompromised, and those manifesting
manifesting serum dilution is highly recommend
recommended.
ed. In cases
evidence of Lyme disease. 
of low parasitemia, experimental inoculation of
specific pathogen-free hamsters with infected 
 

110   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 blood or NOD/sch- scid mice with the patient’

 patient’ss The drug combination azithromycin and
 blood can be useful in parasite detection and atovaquone is as effective as clindamycin-
identification.  
identification. quinine, with less adverse effects. Both drug
The polymerase chain reaction (PCR) is combinations are ineffective in suppressing
highly specific and is generally considered to
to disease progression in immunosuppressed

 be the goldunrealistic

however, standard for
for Babesia detection. It is,
 Babesia
epidemiologic surveys   patients. Very recently, therepatients
Very
of immunocompromised have been reports
who,  
 because it
i t is time consumin
c onsumingg and expensive.
expen sive. during 28 days of uninterrupted treatment
The current practice is the use of PCR in the with azithromycin- atovaquo ne, manifested
isolation of the SSU rDNA from asymptomatic  recurrence of marked parasitemia, suggesting  
 patients, followed
f ollowed by gene sequencing
seq uencing and its the development of drug-resistant  B. microti.
comparison with known SSU rDNA gene Artemisinin, pyrimethamine, and
sequences from pathogenic strains.    pamaquinee can strongly
 pamaquin strong ly inhibit
inhi bit the growth of  
The continued work on the isolation of  B. equi and B. caballi in vitro. Pyrimethamine
specific and highly immunogenic antigens   can indirectly interrupt the parasite life cycle
of Babesia species and isolates, and their through its inhibitory effect on dihydrofolate
intended utilization in the development reductase, essential in folate metabolism, while
of immunochromatographic
immunochromatographic test (ICT)
(ICT) is   pamaquine can interfere in the recycling of
 practicable for
f or epidemiologic
epidemi ologic surveys
su rveys in the
t he endosomal proteins into the plasma membrane
field. ICT is simple, quick, reliable, sensitive,  by direct interaction with the endosomes. 
and inexpensive, and has gained acceptability in   Epidemiology 
tChuer dr eiangtnlyo,sitshoef r  b
e oatr he aIcCuTte astnr d p inf setcitcikosns.
i plsatoenr  tdi p Babesiosisis essentially a zoonotic infection,
employed in the detection of infected livestock.  regarded of major economic importance  
Treatment 
to livestock, particularly in the cattle and
horse industry. Its documentation in humans
Thestandardtreatmentofhuman babesiosis worldwide has increased its recognition as  
utilizes a drug combination of clindamycin and a disease of public health concern. The first
quinine, or azithromycin and atovaquone. The human case attributed to the cattle form was
clindamycin and oral quinine combination reported in 1956, in Europe, and followed
was first used in 1982 in a newborn infant with reports of more cases in Europe and in
suffering from babesiosis, and since then, this
t his  North America, including the discovery of
combination has become the drug of choice. the transmission of a B. microti
microti-like species to
Clindamycin is given 1.2 g intravenously twice humans in 1970. A review of the 136 human
a day or 600 mg orally three times a day, and cases examined in New York (1982-1991)
combined with oral quinine at a dose of 650 revealed almost all cases were among those
mg three times a day.
day. Clindamycin-atovaquone living in Suffolk, Long Island. Of the 103
combination is efficacious in clearing the (76%) who were hospitalized, seven patients
 parasites in normal individuals and prevents  previously underwent
underwent splenectomy,
splenectomy, 31 patients
recurrence of infection, but produces adverse had symptoms of babesiosis and Lyme disease,
effects like vertigo, tinnitus, and gastrointestinal and seven died. The Asian cases reported have
symptoms. Supportive and symptomatic  been few and sporadic with the first records in
management is important. In severe cases where 1984, in Yunnan, China, and a recent report
there is progressive exacerbation of hemolytic in Japan attributed to B. microti (Table 2.10). 
anemia, total blood exchange may be indicated. 
 

CHAPTER 2: Protozoan Infections   111 

Table 2.10. Summary of human cases of babesiosis reported in some Asian countries

Lo cation   Signa mptoms 

s ndSy mpt Diagnosis 
Yunnan, China Fever,
Fever, jaundice, anemia, cutaneous edema;   Initially malaria, then babesiosis 
myalgia, malaise, nausea, prolonged and
repeated illness; periodic fever (39.5-41.0°C),
with renal transplantation prior to onset of fever  

Taiwan Headache, malaise, fatigue, dullpaininuppe r Gallstone with hepatosplenomegaly

aebwdm
f  om
onetnh,s,a h
ne f rr e
dm lyu
 oq cnatnm
ti e f ever , chill f or  a 
ildia
em and babesiosis  

Mongolia High fever,

fever, chill, nightly sweating, myalgia, low  Babesiosis
grade parasitemia 

Japan Fever,malaise, excretionofdark-colore durine, Babesiosis

progressive hemolytic anemia  

The Centers for Disease Control and habitation with livestock and wild animals,
Prevention, USA has confirmed more than and where ticks were abundant. The parasites
40 human cases that contracted the disease detected were pyriform-shaped, suggestive of
from transfusion of packed RBC and tested  Babesia . One case recorded in the rural area
 positiv e for anti-
 positive anti - B. microti antibodies. In Asia,
 B. microti in Southwestern Taiwan was serologically and
the two cases have been b een associated with renal morphologically diagnosed with a chronic and
transplantation and blood transfusion. Thus,   subclinical infection of a geographic isolate
subclinical or asymptomatic cases cannot simply of Babes ia named Taiwan isolate
 Babesia i solate (TW1). The
 be ignored, considering their potential role in detection of anti- Babesia antibodies in 83%
the spread of human babesiosis.    Rattus coxingaendemic in the locality where the
coxinga th e
Phylogenetic
Phylogenetic analyses of the gene sequences Taiwanese patient lived, suggested the rodents
of the SSU rDNA of  Babesia spp. obtained as the highly likely source of infection. The SSU
from human cases helped clarify three
t hree patterns rDNA isolated from the Japanese patient and
or groupings, worldwide, namely: (a) human from the NOD/sch- scid scid mice inoculated with
 babesiosi s attributed
 babesiosis attribut ed to the B. divergens
divergens-related the patient’s blood revealed 99.2% sequence
 parasites in Europe;
Europe; (b)
(b) human
human babesiosis caused homology with the US B. microti SSU rDNA
 by B. microti  principally in the Northeastern (Genbank/EMBL/DDBJ: U09833).
USA; and (c) human babesiosis caused by newly In Japan the wild rodents,  Apo dem
demus
us
emerging species,
species , the WA1-type in the Western  speciosus and A. argente
 speciosus us, are infected with B.
argenteus
USA, tentatively grouped with  B. microti or microti-like forms. In Taiwan, the bandicoot
alternatively with Theileria spp. Recently in rats,  Bandicola indica
i ndica , and the spiny rat,  R.
Italy and Austria, parasites obtained from coxinga , carry morphologically similar  B.
splenic cases revealed SSU rDNA sequences  microti -like forms. The TW1 isolated from  

more closely related to B. odocoileus

odocoileus, a species
that bears morphological, molecular, and  
the first human case in Taiwan is serologically
related to the US B. microti SSU rDNA. 
immunological similarities with  B. divergens
divergens. In the Philippines, studies on animal

The B. divergens
divergens
expanded -related
to include species
 B. odocoileusnow
odocoileus has been 
and possibly  babesiosis
concentrateddhave
concentrate been limited
on hematological
hematologica and mainly
l parameters and
 B. bovis . In Asia, the etiologic agent of human clinical manifestations in cattle B. bigemina
bigemina and 
 babesiosiss has been id
 babesiosi identified microti or  
entified as  B. microti  B. argentina (syn. B. bovis ), and B. canis . Using
 B. microti-like isolate or strain. the ICT, 13 (28%) stray
st ray dogs in an impounding
Human cases recorded in China were facility in Dasmarinas, Cavite tested positive for
generally among farmers living in close   anti-p50 truncated B. gibsoni
gibsoni antigen. The dogs 
 

112   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

had infestation mainly with Rhipi cephaluss ticks,

 Rhipicephalu In Europe and the USA, the Ixodes ricinus
suggestive of their putative role in the spread of and Ixodestriangulicep, and the Ixodesscapularis
triangulicep scapularis
canine babesiosis in the country. and Ixodes pacificus  are the principal vectors,
 Ixodes pacificus
Slaughtered and race horses in the respectively. In Asia, the tick vectors are poorly
Philippines tested seropositive for  B. caballi established. The predominance of  Ixodes

and/or B. equi infection, using ICT containing a

recombinant caballii 48-kDa rhoptry protein 
 B. caball
atus in Southeast Asian countries makes
 granulatus
 granul
it a favorable vector, though this warrants 
(rBc48) and a recombinant truncated B. equi confirmation (Plate 2.17). In Japan,  Ixodes
merozoite antigen 2 (rEMA-2t). Serological ovatus has been suggested as a highly likely
data correlated well with the detection of the   tick vector of human babesiosis for its human
morphologies of the specific etiologic agent(s)  biting activity.  
in blood smears.  

Plate 2.17. Ixodess

odessp. A. Non-eng orged female. B. Engorged female. C. Mouthparts showing
the hypostome (H), pedipalp
pedipalp (P), and scutum (S). (Courtesy of Ms. Mary Jane Cruz-Flores
and Dr. Florencia Claveria)
Claveria)

Prevention and Control  serological surveys reveal more of subclinical or

asymptomatic
asymptomat ic cases. Human cases of babesiosis
Babesiosis is essentially a zoonotic infection, are generally associated with splenectomized
and its transmission to man through the  
and immunocompromised patients, and
 bite of the tick vector is incidental. Effective
noteworthy are the cases acquired through
 preventi on strategies
 prevention strateg ies include
inclu de avoiding
avoidi ng tick-
tick -  blood transfusi
t ransfusion
on and organ
org an transplantation
transpl antation..
infested areas, remaining covered with clothing, There may be a need to consider the inclusion
and immediately removing any attached ticks. of screening procedures for B. microti
microti for blood
As the parasite is capable of stage-to-stage
and organ donors in high risk areas.  
 passage, each of
o f the developmen
de velopmental
tal stages is 
capable of parasite transmission to mammals. References 
The application of bug repellents in clothes Allsopp MT, Allsopp BA. Molecular sequence
like N,N-diethyl-meta-toluamide (DEET)
and acaricides like permethrin may be useful. evidence for the reclassification of some
 Babesia species. Ann N Y Acad Sci.  
The rodent population should be controlled as 2006;1081:509 – 17.
17.
well, as they are major carriers or reservoirs of Clark IA, Allison AC.  Babesia microti and
the parasite. 
 Plasmodium berghei yoelli infections in
In low grade and chronic infections,
mice. Nature. 1974;252:328 – 9 9..
 babesiosis is generally
generally asym
asympt
ptom
omta
taic
ic.. Worldw
Worldwid
ide,
e, 
 

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CHAPTER 2: Protozoan Infections   115 

membrane recycling from endosomes to of resistance to azithromycin-atovaquone

the plasma membrane through a direct in immunocompromised patients with
interaction with endosomes, which does  Babesia
 Babesia microt i infection. Clin Infect Dis.
microt 
not involve neutralization of endosomal 2010;50:381 – 6
6..
 pH or osmotic swelling of endosomes.
endosom es. Eur Yamane I, Thomford JW, Gardner IA, Dubey
J Cell Biol. 2000;79:394 – 9.
9. JP,
JP, Levy JP,
JP, Conrad PA. Evaluation
Evaluat ion of
Van Peenen PF, Chang SJ, Banknieder AR,   the indirect fluorescent
fluorescent antibody
 antibody test for  
Santana FJ. Piroplasm from Taiwanese diagnosis of  Babes
 Babesia
ia gibsoni infections in
gibsoni
rodents. J Protozool. 1977;24:310 – 
1977;24:310 – 2.
2.   dogs. Am J Vet Res. 1993;54:1579 – 884.
4. 
Wittner M, Rowin KS, Tanowitz HB, Hobbs Zamo to A, Tsuji M, Wei Q
Zamoto Q,, Cho SH, Shin
Sh in EH,
JF,
JF, Saltzman S, Wenz B, et al.
al . Successful
Successfu l Kim TS, et al. Epizootiologic survey for
chemotherapy of transfusion babesiosis.  Babesia
 Babesia microtiamong small wild mammals
microti
Ann Int Med. 1982;96:601 – 4. 4. in northeastern Eurasia and a geographic
Wormser GP
Wormser GP,, Prasad A, Neuhaus
N euhaus E, Joshi S, diversity in the beta-tubulin gene sequences.
 Nowakowski
 Nowako wski J, Nelson J, et al. Emergence   J Vet Med Sci. 2004;66:785 – 92.
92.
 

116   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Blood and Tissue Flagellates

Vicente Y. Belizario, Jr., Julius R. Migriño, Jr.

ocally acquired
and tissue infections
flagellates havedue
nottoyet
thebeen
blood  get infected
mucosa, andinclude the skin,
placenta.   gonads, intestinal

L 
documented in the Philippines. However,
 because of fast and easy travel, as well as
increased human migration, imported cases
It has been well established that the
arthropod vector responsible for propagating
this parasite are the reduviid bugs, belonging
from endemic countries may become future   to the genera Triatoma, Panstrong ylus , and
 Panstrongylus
sources of local infection. This scenario is  Rhodnius . These arthropods thrive under
 possible because the vectors
v ectors of Trypanosoma squalid housing conditions such as thatched
cruzi, Triatoma and Rhodnius bugs, are found roofs and mud walls, commonly seen in poor
in the country. In the same manner, the rural communities. Zoonotic mammalian
Philippines has a number of Phleb otomus spp.,
 Phlebotomus reservoir hosts have been identified, including
which can serve as vectors for Leishm ania spp. 
 Leishmania domestic animals, armadillos, raccoons,
rodents, marsupials, and even some
so me primates. 
Trypanosomacruzi T. cruzi exhibits all four stages of
development: amastigote, promastigote,
Trypanosoma cruzi is the etiologic agent of   epimastigote, and trypomastigote. In humans,  
r  aAr m
Thiasgais  tdhiseeaosnelyo p
C aseitr eictahnat r w oviear seisd.
y paasndoisocm tr y pomastigotes ar e f ound in the bloodstr eam,
and studied before it was known to cause a nd amits
aInside astiinsect n tissuethe
gotes  ivector, s (Figur e 2.24).
cellamastigote,
disease. More than 100 years ago, Carlos Chagas
Ch agas epimastigote, and promastigote forms occur
found that the trypanosomes he dissected from in the midgut, while the infective metacyclic
the intestine of a triatomid bug were the same trypomastigote appear in the hindgut.  
 parasites found in the blood of a child suffering Amastigotes are round or ovoid in shape
from fever and enlargement of the lymph nodes. and measure from
fro m 1.5to 4 µm in diameter. They
Since then, the understanding behind the are usually found in small groups of cyst-like
disease that this protozoan causes has shown collections in tissues.  
 profoundd changes in terms of pathophysiolog
 profoun pathoph ysiology,
y, The long slender trypomastigotes are 16
diagnosis, and treatment.   to 20 µm in length while the short, stumpy
Parasite Biology 
forms measure around 15 µm (Plate 2.18).
The posterior end is usually pointed. The
T. cruzi belongs to the trypanosome undulating membrane is narrow with two to  
group Stercoraria . Trypanosomes under this three undulations, and a single thread-like
group multiply within the mammalian host   flagellum srcinating near the kinetoplast
in a discontinuous manner. Unlike other  provid es the parasite
 provides parasi te with mobilit
m obility.
y. In stain
stained
ed
trypanosomes, it is an intracellular parasite, with specimens, trypomastigotes are characteristically
characteristically
myocytes (particularly myocardial tissues) and C-shaped. They have also been described as
cells of the reticuloendothelial system being the U- or S-shaped with a prominent kinetoplast,
most heavily infected cells. Other tissues that   characteristic of the species. 
 

CHAPTER 2: Protozoan Infections   117 

Figure 2.24. Life cycle of Trypanosomacruzi  

(Accessed from www.dpd.cdc.gov/dpdx)
from www.dpd.cdc.gov/dpdx) 

The trypomastigotes of T. cruzi do not

multiply in the bloodstream. Soon after their
entry into the human host, the metacyclic
trypanosomes are engulfed by macrophages
of the reticuloendothelial system and multiply
through binary fission as amastigotes. 
Amastigotes develop into trypomastigotes,
and the cells lyse in 4 to 5 days. The
T he released
trypomastigotes enter the bloodstream, ready to
replicate again once they enter another cell or
are ingested by an insect vector. Once
O nce ingested
 by the intermediate host, the trypomastigotes
 pass through the posterior portion of the
insect’s midgut and become epimastigotes,
where they multiply via longitudinal fission.
Infective metacyclic trypomastigotes appear
Plate 2.18. Trypanosomacruzi ttryp
rypomastiig
gote in th
thiin
in the insect’s rectum 8 to 10 days
d ays after
blood smears stained with Giemsa (Accessed
from www.dpd.cdc.gov/dpdx)
from  www.dpd.cdc.gov/dpdx)   infection, and are passed in the bug’s feces.
The metacyclic trypomastigotes gain entry 
 

118   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

into the body through broken skin, or through result in cardiomegaly, congestive heart failure,
mucous membranes that are rubbed with fingers thromboembolism, and even arrhythmias. Less
contaminated with the bug’
the bug’ss feces. severe signs and symptoms associated with
the chronic phase of the disease include chest
Pathogenesis and Clinical Manifestations  
 pain, palpitations,
palpitations, dizziness, syncopal
syncopal episodes,
Chagas disease can be divided into an abnormal ram findings, achalasia
acute and a chronic phase. The acute phase is  associatedelectrocardiog
with megaesophagus, and chronic  
characterized
characterized by a focalor diffuse inflammation constipation associated with megacolon.
megacolon. About
mainly affecting the myocardium. Non- one-third of patients in the latent stage develop
specific signs and symptoms, such as fever, some manifestation of chronic Chagas disease 
malaise, nausea, vomiting, and generalized after several years or decades. The majority of
lymphadenopathy often accompany the acute symptomatic, chronic patients manifest with
 phase. Cutaneous
Cutaneo us manifestations
manifestati ons of the disease the cardiac form, while the rest develop the
can sometimes appear during this phase, gastrointestinal form. 
usually associated with a localized inflammatory Diagnosis 
reaction at or near the site of inoculation.  
Chagomas are furuncle-like lesions associated A complete patient history is the primary
with induration, central edema, and regional tool for diagnosing Chagas disease. Possible
lymphadenopathy. These lesions represent exposure to T. cruzi should be established, and
the site of entry of the parasite. If the parasite risk factors such as place of residence or work,
 penetrates through the conjunctiva, eyelid  recent blood transfusion in an endemic area,  
swelling called R omaña s sig may f or m. This
’ and contact or  ex posur e toT . cr u z i inter mediate
lesion is ral r acter izand
chaedema
 bipalpebral
 bipalpeb y unilativitis,
conjunct er al  p
ed  bconjunctiviti nlemay
s,aiand ss host The d be  evaluadiagnosis
shouldefinitive ted. of Chagas
involve the lacrimal gland and surrounding disease during its acute phase relies on direct
lymph nodes. After 1 or 2 months, symptoms visualization of the parasites in thick and thin
resolve, and the patient goes into a latent or  blood smears using Giemsa stain. Cerebrospinal
Cerebros pinal
indeterminate, but usually asymptomatic phase. fluid (CSF), tissue samples, or lymph can also be
During this phase, patients infected with T. used for parasite visualization.
visualization. However,
However, only in
cruzi are still capable of transmitting it to others the
thefirst
first  two months
m onths o
off acute dis
disease
easecanT. cruzi
through insect vectors, blood transfusion, or trypomastigotes be seen by direct examination.
organ transplantation.  Other diagnostic techniques include
The pathophysiology of the chronic concentration methods (microhematocrit),
 phase of the
th e disease was initiall
i nitiallyy thought
thoug ht to  blood culture, and polymerase chain reaction
 be autoimmune in nature; however, this is (PCR). Xenodiagnosis, wherein laboratory-
controversial. Newer evidence shows that reared triatomine bugs are allowed to feed on
chronic Chagas disease is multifactorial,   suspected patients and are later examined for the
and dependent on the interaction between  presence of T.cruzi metacyclictrypomastigotes,
 parasite and host. Nonetheless, the chronic may also be utilized as a diagnostic modality.  
 phase is manifested
man ifested by fibroti
fibroticc reactions tthat
hat During the chronic phase, a variety of
cause injury to the myocardium, cardiac serologic tests may be used, such as enzyme-
conduction network, and enteric nervous linked immunosorbent assay (ELISA), indirect
system (decrease in nerve ganglia leading to hemaglutination, indirect immunofluorescence,
megasyndromes). The heart is the primary and PCR. The WHO recommends using at
organ affected during this phase, which may   least two techniques with concurrent positive
positive 
 

CHAPTER 2: Protozoan Infections   119 

results before a diagnosis of Chagas disease The prevalence and distribution of

is made. For the cardiac form of the disease, American trypanosomiasis
trypanosomiasis has been continually
ECG and echocardiography may show atrial shifting. Endemic regions include most of
fibrillation/flutter, low QRS voltage, dilated Central America and the southern cone of South
cardiomyopathy, and tricuspid and mitral America. Several factors tend to determine the
regurgitation. The gastrointestinal form is changes inIn
prevalence of the in
disease in endemic
usually diagnosed by barium esophagogram   countries. certain regions Mexico, delayed 
(esophageal dilatation) and barium enema control policies and mobilization probably
(megacolon of the sigmoid and rectum).   contributed to an increase in prevalence. In
the past 25 years, there have been
b een several 
Treatment 
international efforts to control and prevent the
Two drugs are recommended for the disease in these endemic areas, most notably
treatment of acute phase Chagas disease: vector control strategies, and improved blood
nifurtimox and benznidazole. These drugs are transfusion safety regulations. Brazil, Chile,
usually associated with severe side effects: (a) Uruguay, and several areas of Argentina and
nifurtimox may cause weight loss, anorexia, Paraguay have eliminated the vector Triatoma
 behavioral changes, and an antabuse effect; (b) infestans. However, the disease persists due to
 benznidazole
 benznidazo le may cause rashes, bone marrow emergence of secondary domestic vectors, and
suppression, and peripheral neuropathy.  vector resistance to insecticides.
Other classes of drugs, such as allopurinol Initially thought to be confined within the
and itraconazole, have been shown to halt the  Latin American region, countries such as USA,  
 pr ogr ession into car diomyo pathy, although no Auanstar dalai,aS p
C h aviens, eFer nanacneu,  m
Sw n,  ar nildy
 bietr zeor f lacnasde,sJ,apr aim
damage r eatmenby
f or m of  tcaused as  bdisease.
t hthe n to r edrugs
een showNewer ver se due to human
hum an migration
migrati on patterns
patter ns as well as rfom
rfom
such as triazole derivatives (posaconazole,  blood transfusion,
transfusi on, organ donation and vertical
ravuconazole) and cruzipain inhibitors   transmission. However, these countries are still
(a parasite protease) are currently under regarded as non-endemic, and majority of the
development.  cases are attributed to imported infections from
Symptom-specific management is used endemic areas. 
to treat patients with chronic manifestations. Chagas disease is included in the WHO list
Cardiac manifestations are controlled by of Neglected Tropical Diseases (NTDs),
(NT Ds), and is
 pacemakers and
an d antiarrhythmic
antiarr hythmic drugs, such
suc h the leading cause of parasite-related deaths in
as amiodarone, while megasyndromes are Latin America. In 2003, it ranked 3rd as the
managed with special diets, laxatives, and leading cause of parasitic infection in the world,
surgical procedures.   behind malaria and schistosomiasis.
schistosomiasis.  

Epidemiology  Prevention and Control 

Chagas disease is estimated to have infected There have been major breakthroughs
more than 10 million people worldwide. Most in the control and prevention of American  
cases are reported in the Latin Americas, where trypanosomiasis,
trypanosomiasis, particularly by Brazil, Chile,
more than 25 million people are at risk for the and Uruguay. Vector control and blood
disease. Serologic techniques have identified that transfusion regulations have delivered positive
up to 13% of populations in certain endemic outcomes, in terms of disease prevention in
regions are positive for T. cruzi antibodies. An these countries. Spraying of insecticides, use
estimated 10,000 to 12,000 people die of the of insecticide-treated bed nets, and house
disease annually. improvements to prevent vector infestation  
 

120   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

have been proven cost-effective.

cost-effective. International highly fatal disease caused by two subspecies of
organizations such as the WHO and the Trypanosoma bru cei: T. brucei gambiense and T.
brucei
manufacturers of the antiparasitic drugs are brucei rhodesiense. A third subspecies, T. brucei
working in tandem to ensure the availability of brucei , primarily affects wild and domestic
drugs for the treatment of the disease.   animals; collectively, the three subspecies
In Mexico and non-endemic countries represent the Trypanosoma brucei complex. The
near endemic countries, the coverage, quality earliest reports of sleeping sickness in Africa 
and safety of blood transfusion screening  date back to 1734, while the
th e formal correlations
is being evaluated as avenues for disease    between the symptoms, the parasite in blood
 prevention. Vaccine development has not and CSF, and the relationship between the 
yet been successful, but the advent of newer  parasite and its insect vector were established
establ ished
technologies and characterization
characterization of
o f the T. cruzi during the early 1900s. 
genome may aid in future vaccine research. 
Parasite Biology 
Trypanosomabruceg i ambe i nse Members of theT. brucei complex belong to
Trypanosomabrucerihodes iense the trypanosome family Salivaria. The parasite
is usually transmitted via the bite of the blood-
Human African trypanosomiasis (HAT), sucking tsetse fly (Glossinaspp.) feeding from an
also known as African sleeping sickness, is a   infected mammalian host (Figure 2.25). Since  
 

CHAPTER 2: Protozoan Infections   121 

the disease relies heavily on the tsetse fly for its through mechanical methods (accidental needle
transmission, HAT cases are localized in regions  pricks, other blood sucking insects), as well as
of sub-Saharan Africa, primarily in remote rural vertically,
verticall y, vvia
iamother-to-child
mother-t o-child infection
infecti on through
areas where tsetse fly
fly habitats
 habitats are located.  the placenta. 
T. brucei gambiense is localized mostly in
Pathogenesis and Clinical Manifestations  
the western
Africa. and central
It primarily regions
affects of sub-Saharan
humans, but utilizes   Human African trypanosomiasis has two  
dogs, pigs, and sheep as reservoir hosts. It is types, acute and chronic, depending on the
responsible for the chronic type of sleeping subspecies causing the disease. Trypanosoma
sickness, and accounts for 95%of all HAT cases.  brucei gambiense sleeping sickness manifests
T. brucei rhodesienseis found in east Africa months or years after initial infection, while
and is primarily a zoonosis of cattle and wild symptoms of T. brucei rhodesiense sleeping
animals, with humans being accidental hosts. sickness may appear just weeks after infection. 
It causes the more acute and rapidly fatal form The initial lesion of African trypanosomiasis
trypanosomiasis
of sleeping sickness, and accounts for the  begins as a local, painful, pruritic,
pruriti c, erythemat
erythematous
ous
remaining 5% of HAT cases.  chancre located at the bite site, progressing
Only the epimastigote and trypomastigote
trypo mastigote into a central eschar, and resolving after 2 to
forms are exhibited by the T. brucei complex. 3 weeks. This trypanosomal chancre is more
mor e
The trypomastigotes are polymorphic: there common in Gambian sleeping sickness. Several
are typical slender forms, and short, stumpy days after the development of the chancre,
forms. They are flattened and fusiform in   usually within 3 to 10 days, the next stages of  
sha pe,  14 o 33 µm in length and 1.5 to 3.5 the disease manif est. 
µm inposteriorly.
 blunt posteri  The b
width.orly. The cent er s anlocated
 ta prally
odycentrally  ancleus
ter ior lynucleus
nu d is oth late.
earlyBand ty pesDuring
  of  H
Duri ngAthe nder gphase
T  uearly twoof
o ase
ph   stHAT,
ages:,
HAT
contains a large central karyosome. There is an called the hemolymphatic stage, the parasites
undulating membrane, and a single flagellum  prolifer ate in the bloodstream and lymphatics.
 proliferate lymphat ics.
that runs along the edge of the undulating The patient may manifest with irregular bouts
membrane and becomes free anteriorly.   of fever, headache, joint and muscle pain, and
Once ingested by the intermediate malaise. Anemia, myocardial inflammation,
host, Trypanosoma brucei trypomastigotes   disseminated intravascular coagulation, and
undergo several developmental changes from renal insufficiency may occur. Frequently,  
trypomastigote into procyclic forms in the in Gambian trypanosomiasis, the posterior
insect’s midgut. After multiplying for 15 to 20 cervicallymph nodes are enlarged, non-tender,
days, the epimastigotes migrate to the foregut and rubbery in consistency (Winterbottom’s
into the insect’s  salivary glands, where they
insect’s salivary sign). Other lymph nodes, such as axillary
mature into metacylic trypomastigotes. When   and supraclavicular lymph nodes, may also be
the infected fly bites another mammalian host, involved in both types of sleeping sickness. The
these infective trypomastigotes are injected into signs and symptoms manifested within this
the new host where they multiply and mature  phase are due to tissue
tissue damage, either from
in blood and connective tissue. In humans,    parasitic toxins or immune complex reactions
T. brucei lives in the blood, in the reticular that target organs and RBCs. The early systemic
tissue of lymph and spleen, and the CSF. The  phase lasts from 1 to 6 months. 
long, slender trypomastigotes multiply by The late phase of the disease, known as
longitudinal binary fission.  the meningoencephalitic stage, marks the
Though mostly transmitted through its involvement of the central nervous system.
insect vector, the disease can also be transmitted  The brain and meninges become involved 
 

122   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

as the parasites find

find their
 their way into the CNS due the relative higher levels of parasitemia.
through the bloodstream. This usually occurs Serial examinations may be necessary due
3 to 10 months after initial infection in to varying levels of parasitemia. Other  
Gambian infections, but can manifest after diagnostic techniques include enzyme-linked
 just a few weeks in Rhodesian trypanosomiasis.
trypanosomiasis. immunosorbent assay, immunofluorescence,
 Neurolo
 Neurologic
gicbehavioral
symptoms
sympt omschanges,
become
beco me headache,
evident,
evident , such indirect hemagglutination test, mini-anion
as apathy, and  exchange centrifugation technique, and PCR.  
sleep pattern changes. These may be followed CSF examination is mandatory in patients
 by more
more severe symptoms,
symptoms, such
such as convulsions,
convulsions, with suspected HAT to detect CNS involvement.
tremors, speech defects, disturbances in speech   Abnormal CSF findings include increase in cell  
and reflexes,  and even paralysis. Kerandel’s  sign count, opening pressure, protein concentration,
may manifest as a deep, delayed hyperesthesia and IgM levels. The latter is considered
(delayed bilateral pain out of proportion to  pathognomonic
 pathogn omonic for
f or the meningoencap
men ingoencaphalitic
halitic
the extent of tissue injury). In the later stages, stage of the disease.  
somnolence manifests, followed by a deep coma. Card agglutination test for trypanosomiasis
Death eventually follows either from the disease (CATT) detecting circulating antigens in
itself, or from intercurrent infection due to  persons infected with T. brucei complex is
immunosuppression.   available commercially
commercially and can be used in the
Areas of the CNS usually involved in the field setting to screen at-risk populations. This
meningoencaphalitic phase include the frontal technique provides a rapid and highly specific
lobes, pons, medulla, and perivascular areas.  method of screening for HAT cases; however,  
Par asites may al o b seen in the CSF. Aut  p y the method has low s sensitivi y f or c r tain str ain s
f HATand
osmall,  paticonfluent edema and num
ents r evealshemorrhages.   er ous, of  T . br  ucei  g ambien e in cer tain ar eas of  West 
Africa.
Trypanosomes
Trypanos omes are able to evade the immune
i mmune Treatment 
response of the host through a process called
antigenic variation. This refers to the ability Treatment of African sleeping sickness
of the trypomastigote to continuously change depends on the stage of the disease. For the first
its surface coat, composed of variant surface stage, intravenous suramin sodium for both T.
glycoproteins, so that the host’s antibodies bruceigambiense and T. brucei rhodesiensee, and
bruc ei rhodesiens
cannot recognize the parasite in subsequent intramuscular pentamidine for the Gambian
recurrent waves of parasitemia.   form can be used. These drugs have side effects,
which include fever, rash, renal insufficiency,
Diagnosis 
muscle pain, and paresthesia for suramin; and
Diagnosis of human African trypanosomiasis tachycardia, hypotension, and hypoglycemia
depends upon the demonstration of highly for pentamidine. These drugs do not cross the
motile trypomastigotes in expressed fluid from   blood-brain
 blood- brain barrier,
barrier, and so, they cannot be used
a chancre, lymph node aspirate, and CSF.   for the CNS stage of the disease.  
Thick and thin blood films can be stained Once CNSinvolvement occurs, intravenous
intravenous
with Giemsa. Buffy coat concentration method melarsoprol is the drug of choice for both types
is recommended to detect parasites when of sleeping sickness. This arsenic-containing
they occur in low numbers. Examination for drug can cause fatal arsenic encephalopathy
trypomastigotes is usually done during the (usually prevented by co-administration of
hemoly mphatic stage
hemolymphatic stag e of the disease
disease,, and is more corticosteroids), and resistance to the drug 
useful for the diagnosis of T. brucei rhodesiense  has also been observed. A febrile
f ebrile episode 
 

CHAPTER 2: Protozoan Infections   123 

called a Jarisch-Herxheimer reaction due do their laundry. Rhodesian trypanosomiasis

to trypanosome lysis may occur following is an occupational hazard for persons working
melarsoprol treatment.  in game reserves, and may also be a threat to
A second-line drug, nitrofurazone, is used visitors of game parks. Cattle and game animals
in cases of melarsoprol treatment failure. A like antelopes can serve as reservoir hosts for
newer drug, eflornithine, is less toxic than the parasite. 
melarsoprol, and can also be used during 
the hemolymphatic stage; however, it is only Prevention and Control 
effective against T. brucei gambiense . Recent Vector
Vec tor control is the primary method used
evidence has shown that a combination in the control and prevention
pr evention of African sleeping
treatment of oral nifurtimox and intravenous   sickness. Tsetsefly trapping is the main strategy
eflornithine is of similar efficacy  compared to employed to decrease the vector population.
longer intravenous monotherapy with either Use of insecticides and protective clothing are
agent. Combination therapy is advantageous recommended to prevent contact with the insect
due to the relative ease in administration, and vector. Regulation and treatment of reservoir
a decreased risk of developing drug resistance. hosts such as cattle and game animals are also
Although nifurtimox is currently registered as  being looked upon as an effective means of
a drug against American trypanosomiasis, its  preventing disease transmission. 
use in the nifurtimox- eflornithine combination Several programs developed to eliminate the
treatment (NECT) has been included in the insect vector have been in place in Africa. The
WHO List of Essential Medicine. Kwando-Zambesi Regional Tsetse Eradication  
Epidemiology   pr o ject  star  ed i Botswa a, and in2000,  the Pan
Sleeping sickness affects around 300,000 A f r ican Tse(PATTEC)
Campaign tse and Tr y pawas
nosoestablished. cation
miasis Er ad iAerial
to 500,000 people in 36 countries within
w ithin sub- and localized spraying of insecticides in Angola,
Saharan Africa. It is estimated that more than Botswana, Namibia, and Zambia has eradicated
50 million people are at risk of infection. In the the tsetse fly
fly in
 in these African countries.  
last 10 years, most reported cases came from The WHO has established partnerships
the Democratic Republic of Congo (DRC), with private companies such as Aventis Pharma
followed by the Central African Republic. (Sanofi-Aventis) and Bayer HealthCare to
Other countries such as Angola, Cameroon,  providee surveillance
 provid surveill ance and management
managemen t support
Chad, Congo, Côted’Ivoire, Equatorial Guinea, to endemic countries.  
Gabon, Guinea, Kenya, Malawi, Nigeria,
Sudan, Uganda, United
Uni ted Republic of Tanzania, Leishmaniaspp.
Zambia, and Zimbabwe have also reported
cases.  Early descriptions of leishmaniasis have been  
During the turn of the century, between found as early
American as thedocumented
Indians first century A.D., where
the disease in  
10,000 and 40,000 annual cases of HAT were
 being reported. However, newer data from the  pottery figures. Cunningham studied the “Delhi
 boil”  in India back in 1885, and Leishman had
 boil”
WHO has estimated more recently that new
cases have dropped below the 10,000 mark, a  properl
 properlyy identified
1903. Leishmania  the intracellular
 Leishmaniabrazil
parasites in
iensiswas later identified
braziliensis
first in 50 years.
50  years. 
Tsetse flies live near the banks of rivers and in 1911 by Gaspar Viana, as was the insect
i nsect
streams, therefore transmission can readily occur vector which transmitted the parasite in 1922
when people frequent these areas to swim and    by Henrique Aragao.
 

124   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Parasite Biology  Mexico, Central America, and some parts of

South America, as well as the Amazon rain
Leishmaniasis
Leishmaniasis is a disease caused by infection forest, and is usually caused by L. mexicana
mexicana, L.
of the diploid protozoa belonging to the genus
amazonensis ,  L. guyanensis, L.
L. guyanensis  L. braziliensis, and L.
braziliensis
nia. This genus is actually divided into
 Leishmania
 Leishma
chagasi. Arthropods, particularly sandflies  of the
two subgenera, differentiated from one another
 by the location of their development inside  genera
(New World), act as(Old
 Phlebotomus
 Phlebotomus World)
the insect and Lutzo
 Lutzomyia
vector
myia
for these  
or ic, .asCwur er lel natslythtehear eaasr iena bwohuicth
theyinasr eectenvdecetm  parasites. Dogs are the primary reservoir in
15 species of Leishmania which cause clinical
urban areas, and rodents also act as reservoirs
in both urban and rural areas.  
manifestations in humans. This diverse pool
 Leishmania spp. produce amastigotes
of different species is historically divided and intracellularly in the mammalian host, and
classified based
classified  based on their biological, clinical,
 promastigotes
 promasti gotes in the
th e hindgutV (ianniasubgenus),
geographic,
geographic, and epidemiological
epidemiological characteristics.  midgut (Viannia and  Leishmania subgenera),
Epidemiologically , the  Leishmania spp.
and proboscis ( Viannia and Leishmania
are divided into Old World and New World
subgenera) of the insect vectors. Amastigotes are
leishmaniasis. In the Old World, the common
ovoid or rounded bodies measuring 2 to 3 µm
species involved are  L. tropica (Asia and in length and live intracellularly in monocytes,
Eastern Europe),  L. aethiopica (Africa) and 
 polymorphonucl
 polymo rphonuclear
ear leukocytes,
leuko cytes, or endotheli
en dothelial
al
 L. major . New World leishmaniasis affects  
cells. The nucleus is large, while an axoneme  
 

CHAPTER 2: Protozoan Infections   125 

arises from the kinetoplast and extends to the incubation period ranges from two weeks to
anterior tip.  several months. An erythematous papule or
Promastigotes have a single free flagellum nodule, called an “oriental button,”
  button ,”  is produced
arising from the kinetoplast at the anterior end. at the inoculation site. The lesion has raised
They measure 15 to 20 µm in length and 1.5 to  edges and a central crater. During the course
3.5 µm in width.
the proboscis Thesandfly
of the infective
 arepromastigotes
injected into thein  of several
ulcer weeks, theinpapule
as it enlarges forms
size. The a violaceous
lesion may heal 
host’s skin during feeding (Figure 2.26). They spontaneously after a few months, leading to
then invade the cells of the
t he reticuloendothelial a disfiguring
disfiguring scar;
 scar; in the case of New World
system, transform into amastogotes, and  leishmaniasis, CL may progress to other forms 
multiply via binary fission. When the parasitized of leishmaniasis. 
cell ruptures, the amastigotes that are released B. Diffuse Cutaneous Leishmaniasis 
either invade new cells, or are taken up by
sandflies during feeding, where they transform The manifestation of DCL, also called
into promastigotes in the gut, multiply by anergic or lepromatous leishmaniasis, is
 binary fission,
fission, and
 and migrate to the foregut.   characterized
characterized by a localized, non-ulcerating
 Leishmania spp. may also be transmitted  papule, eventually developing numerous
congenitally, through blood transfusion, by diffuse satellite lesions that affect the face and
contamination of bite wounds, and by direct extremities. This type of leishmaniasis may be
contact with contaminated specimens.   initially diagnosed as lepromatous leprosy. 
Pathogenesis and Clinical Manifestations   C. Mucocutaneous Leishmaniasis  

into Clinically, leishmaniasis

four categories: cutaneouscan be divided
leishmaniasis Mucocutaneous
in about leishmaniasis
2 to 5% of persons develops
infected with L.
(CL), diffuse cutaneous leishmaniasis (DCL), braziliensis, either concurrently or even several
mucocutaneous leishmaniasis (MCL), and years after the resolution of skin lesions. It
visceral leishmaniasis (VL). The wide spectrum may be also due to the contiguous spread of
of symptoms manifested by leishmaniasis is cutaneous leishmaniasis caused by  L. tropica
tropica.
often compared to leprosy, where the localized
localize d Involvement of the mucous membranes of the
CL is similar to tuberculoid leprosy, and DCL nasal and oral cavities results in nasal stuffiness,
is similar to lepromatous leprosy.   discharge, epistaxis, and destruction of the
The immune response of the host against nasal septum. This disfiguration is often called
the infection depends on  Leishmania-specific
 Leishmania espundia. Progression into the pharynx and
Th1-type CD4+ T-cells, macrophages, and larynx may threaten the airway passage, and
cytokines. However, other factors such as may lead to dysphonia, dysphagia, and even
genetics, nutritional status, and environmental aspiration pneumonia. 
factors may affect the outcome of infection.  Lesions usually manifest with few parasites.
 A. Cutaneous Leishmaniasis  
Systemic Th1 response is strong in cases of
MCL, with increased levels of peripheral
Cutaneous leishmaniasis is the most mononuclear cells in the blood.  
common form of the disease, and is caused D. Visceral Leishmaniasis  
 by several species
s pecies of  Leishmania, including L.
 Leishmania
tropica (dry or urban oriental sore), L. major Visceral leishmaniasis (or kala azar ),), is a
(moist or rural oriental sore), and L. mexicana disseminated parasitosis primarily caused by  L.
(chiclero ulcer, usually affecting the ears). The   donovani complex: L. donovani, L.
 L. chagasi , and 
 

126   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 L. infantum . It has an incubation period of 2 to found useful. Animal inoculation using
8 months, but clinical symptoms in previously hamsters could detect low intensity of infection. 
infected but asymptomatic persons may The leishmanin skin test (Montenegro
appear during immunocompromised
i mmunocompromised states. skin test) can be used to identify exposure to
This manifestation of the disease stems from the parasite. It is usually positive in cases of CL
the spread of parasites into the bone marrow, and MCL, but is negative in cases of DCL and
spleen, and liver. kala azar .
In the acute phase, twice-daily fever spikes Immunologic assays such as ELISA and
(double quotidian), with accompanying chills rk39 antigen dipstick test have demonstrated
may be present, which might be mistaken for   high sensitivity and specificity for VL in  
malaria. During the subacute and chronic certain immunocompetent patient populations.
course, common signs and symptoms include Direct agglutination, urine antigen assays, and
fever, weakness, loss of appetite, weight loss, newer tech niques such as flow cytometry and
hemorrhage, and abdominal enlargement molecular diagnostic modalities (polymerase
associated with hepatosplenomegaly.   chain reaction, RFLP analysis) are also being
Phagocytosed
Phagocyto sed amastigotes are present only used; the latter may be used to identify the
in small numbers in the blood. However, they species of Leishmania.
are numerous in the reticuloendothelial cells of Treatment 
the spleen, liver, lymph nodes, bone marrow,
intestinal mucosa, and other organs. In patients Primary pharmacologic treatment is
with VL,  Leishm ania-specific Th1 response  iiss  
 Leishmania  based on antimony ccompounds,
ompounds, n
notably
otably the 
u sually low or   a bsent.  VL, f lef t untr eated, has  pentavalent antimonials: sodium sti bogluconate
a  gr ePost- thanazar 
ater kala 95dermal
m or leishmaniasis
d%ermal tality r ate. (PKDL)  nd n-m
adrugs areethstill lucaminused
yl-gbeing uminewhere
eglareas
e (min ). These
is a sequela of visceral leishmaniasis, usually seen susceptibility is still good, due to its low
in endemic areas. It manifests as a cutaneous cost. However, primary treatment failure and
eruption resulting in hypopigmented
hyp opigmented macules, relapses are often observed using these drugs,
malar erythema, nodules, and ulcerations. These especially in patients with AIDS. Side effects
lesions usually manifest a few months to several such as abdominal pain, nausea, arthralgia,
years after treatment.   and even fatal arrhythmias are high using
these drugs, and treatment should only be
Diagnosis 
done after consultation with infectious disease
Diagnosis of active leishmaniasis is based on experts. Treatment with the antimonial drugs
the microscopic demonstration of Leishmania requires daily intramuscular or intravenous
from lesion and tissue
t issue scrapings, aspirates, or administration for up to 4 weeks, and hospital
 biopsy. Giemsa
G iemsa and hematoxyl
h ematoxylin-
in-eosin
eosin stains
stai ns confinements are necessary.
are necessary. 
are often used in microscopic and histologic In cases where there is treatment failure
samples, and the demonstration of amastigotes with antimonials, or in areas where resistance
confirms the diagnosis of leishmaniasis. Cultures is high, intravenous amphotericin B is the drug
are unreliable due to the difficulty
difficulty  of isolating of choice. Amphotericin B has a high cure rate;
the parasites, especially in old lesions. There are however,r, the associated side
howeve si de effects,
effects , aswell as the
however reports of successful primary isolation cost and availability of the drug are significant
of the New World cutaneous leishmania using limiting factors. Lipid-based preparations of the
the Novy, MacNeal, and Nicolle medium drug (AmBisome) are currently being utilized as
(NNN). The Schneider’s
Schneider’s medium
 medium was also   a highly effective, better tolerated, and overall 
 

CHAPTER 2: Protozoan Infections   127 

cost-effectivee drug formulation

cost-effectiv f ormulation for cutaneous mostly poor and malnourished children below
and visceral leishmaniasis.  15 years old.  
In India, where sodium pentavalent Leishmaniasis is primarily a disease of
antimony resistance is high, the antineoplastic  poverty. It affects people living in squalid
drug miltefosine was introduced in 2002 to treat conditions, and is associated with poor housing,
VL. Miltefosine
given is the only
to VL patients.   oral drug currently malnutrition, a weak immune system, and
lack of resources. Environmental changes such
s uch 
Pentamidine is another second-line drug as deforestation, new irrigation schemes, and
for cutaneous as well as the visceral form of the urbanization are also linked to changes in the
disease. However, due to side-effects and the  epidemiology of the disease. In urban areas  
development of drug resistance, pentamidine where leishmaniasis occurs, there is a greater
use has been limited. For the cutaneous form of epidemic threat. 
leishmaniasis, topical paromomycin has shown Visceral leishmaniasis is an important
efficacy in certain areas.
certain  areas.  opportunistic infection in AIDS patients. VL/
Combination therapy
therapy using two or more of HIV co-infection is currently a major threat in
the anti-leishmanial drugs is being studied. The the control and prevention of either disease.
 presence of drug resistance especially towards Immunosuppression from HIV predisposes
the pentavalent antimonials, poor treatment to VL, while VL infection accelerates HIV
outcomes of complicated cases (such as HIV replication and progression to AIDS. VL/
coinfection), the potential for greater efficacy, HIV co-infection has been documented in
 better compliance, and fewer side effects are  35 countries, with most cases coming in from  
r easons why com bination ther a py  f or   VL Ethio pia, souther n Eur o pe (S pain, Italy, Fr ance, 
icombinations Amongused
onse sus. being
s the cur r ent ccurrently the or dr uunder
g and PInor the l), and Br azil.there have been
tugaPhilippines,
clinical trials are: sodium stibogluconate plus imported cases of cutaneous lesions referred
 paromomycin, and liposomal amphotericin B to the University of the Philippines — College
College
 plus either miltefosine,
miltefosine, or sodium
sodium stibogluconate.
stibogluconate.  of Public Health, where amastigotes were
identified from the patients.  
Epidemiology 
Prevention and Control 
Leishmaniasis is a global disease distributed
Leishmaniasis
across 88 countries in four continents. It affects Preventive measures against leishmaniasis
more than 12 million people worldwide, and include usage of insect repellants containing
more than 350 million are at risk for the DEET and permethrin, insecticide-treated
disease. New cases of cutaneous leishmaniasis clothing, and fine-mesh bed nets. Use of fine
fine-mesh
number between 1 to 1.5 million per year, the mesh screens and spraying of houses and
an d
majority of which occur in Afghanistan, Brazil,  buildings
 buildin gs are also being done in certain areas.
Iran, Peru, Saudi Arabia, and Syria. American However, interval spraying predisposes to
soldiers deployed in Afghanistan and Iraq have i nsecticides, not
resistance of sandflies to the insecticides,
also demonstrated cases of CL. Mucocutaneous to mention the impact of insecticides on the
leishmaniasis occurs in Bolivia, Brazil, and environment. 
Peru, while half a million new cases annually Regulation of reservoir hosts is another
of visceral leishmaniasis occur primarily in important aspect in the control and prevention
Bangladesh, Brazil, India, Nepal, and Sudan. of leishmaniasis. Insecticide-treated dog collars,
In 2009, there was a noted upsurge
u psurge in VL cases mass testing of domestic dogs, and even
in Sudan compared to previous
pr evious years, affecting  extermination of infected dogs are current  
 

128   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

strategies that address zoonotic transmission Markell EK, Voge M, John DT. Medical
of the disease.    parasitology.
 parasitolo gy. 9th ed.
ed . Philadelphia:
Philad elphia: W. B.
At present, there is no commercially Saunders Company; 1992.  
available form of either active or passive  Nantulyaa VM. TrypTe
 Nantuly TrypTect
ct CIATT a card indirect
chemoprophylaxis against leishmaniasis.   agglutination trypanosomiasis test for
However, in immunocompetent
a form of immunity persists afterindividuals,
resolution 
diagnosis of Trypanosoma
T. rhodesiense infection s. Trans R Socand
infections.
gambiense  
Trop
of active lesions. Certain countries, such as Med Hyg. 1997;9(1):551 – 33..
endemic areas in the Middle East, have been  Neva FA, Brown HW. Basic
B asic clinical parasitology.  
using live parasites either from infected
i nfected insect  6th ed. Connecticut: Appleton & Lange;
vectors, or in recent years, from cultures, to 1994.
inoculate inconspicuous areas (such as the Roberts LS, Janovy J. Foundations of
 buttocks) so as to protect themselves from  parasitology. 5th ed. Dubuque: Wm. C.
disfiguring  facial lesions from future infections. Brown Publishers; 1996.  
Commercial vaccines are currently under Wilson WR, Sande MA. Current diagnosis
development.  and treatment in infectious diseases. USA:
Lange Medical Books,McGraw-Hill;2001.
References 
 p. 842 – 53.
53. 
Beaver PC, Jung RC, Cupp E.W. Clinical World Health Organization. WHO Fact
 parasitology.
 parasitolo gy. 9th ed. Philadelphia: Lea & Sheet no. 116. Geneva: World Health
Febiger; 1984.  Organization; 1999.
Leyr itana,  K T,  Saniel MC,  Car  po BG, Mur r ay Wor ld Heal  h Or ganization . Chagas disease:
HinW .  New wthe
a traveler: or ldfirst a neous leishmcase
cut documented aniasinis nterr u p tionRec.
iEpidemiol ansmission. Wk – 
of  tr 1998;73(1-2):1 ly44.. 
the Philippines. Acta Med Philipp. 2011; World Health Organization. Leishmaniasis:
45(3):73 – 6.
6 .  second generation vaccines. TDR news.
Mahmoud AA. Tropical and geographical 2001;65:13. 
medicine companion handbook. 2nd ed. World Health Organization.
Organizat ion. Miltefosine — 1,200
1,200
Singapore: McGraw-Hill Book Co.; 1993.    patients in Phase IV trial
trial in Inidia. TDR
news. 2002;69:12.
 

CHAPTER 2: Protozoan Infections   129 

CHAPTER 3  

Nematode Infections 
Infections 

Intestinal Nematode s
Vice nte Y. Belizar io, Jr ., Fr anc is Isidor e G. Totañes 

 Ascarislumbricoides two spicules. Females have paired reproductive

organs in the posterior two-thirds, while males

T he most common intestinal nematode of

man is  Ascaris lumbricoides
lumbrico ides or the giant  
round worm, which occurs most frequently
have a single, long, tortuous tubule. The adults
reside in but do not attach to the mucosa of the
small intestines. Larval morphology is similar
in the tropics. It is estimated that more than 1 to the adult. Ascaris has been shown to produce
 Ascaris
 billionn individuals
 billio indivi duals are infected, 70% of whom  pepsin inhibitor 3 (PI-3) that protects worms
are from Asia.  from digestion and phosphorylcholine that
 Ascaris is a soil-transmitted helminth suppresses lymphocyte proliferation. 
(STH), along with Trichuris trichiura and The infertile eggs (Plate 3.1a) measure 88 
hookworms, which means that the soil plays a to 94 µm by 39 to 44 µm, longer and narrower
major role in thedevelopment and transmission  than fertile eggs, with a thin shell
s hell and irregular  
of the parasite. It causes varying degrees of mammilated coating filled with refractile
 patholo gy: (a) tissue
 pathology: ti ssue reaction
reactio n to the invading
i nvading granules. These infertile eggs may be difficult  to
larvae, (b) intestinal irritation to the adult, and  identify and are found not only in the absence
(c) other complications due to heavy infection of males. They are found in about two of five
and extraintestinal migration. STH infections infections. 
are diseases of poverty, and contribute to Fertile eggs measure 45 to 70 µm by
malnutrition and impairment of cognitive 35 to 50 µm (Plate 3.1b). There is an outer,
 performances.
 performan ces. They, likewise,
li kewise, reduce
red uce work coarsely mammilated albuminous covering
capacity and productivity of adults.   which may be absent or lost in “decorticated”
Parasite Biology 
eggs. The egg has a thick, transparent, hyaline
shell with a thick outer layer as a supporting
This worm has a so-called “polymyarian  structure and a delicate vitelline, lipoidal, inner 
i nner  
tcye plles”aor ef  snoummateir com ar rao jnegcetmweenltl iintwohtichhe
ususacnlde  p i pmo bsr itainoen,, w
ove p
m t  heicf ehr tisleheigghslyhaivme p oveoa b
 aenr m idlem.  aAsst
 body cavity. The whitish or pinkish worms are of protoplasm, which will develop into larvae
large, with males measuring 10 to 31 cm and in about 14 days.  
females 22 to 35 cm in length, with smooth The infective stagethese
is the fully embryonated
striated cuticles. The worms have a terminal egg (Plate 3.1c). When eggs are ingested,
mouth with three lips and sensory papillae. they hatch in the lumen of the small intestine,
Males have a ventrally curved posterior end with  releasing the larvae. The larvae then migrate  

129 
 

130   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Plate 3.1. Ascaris unfertilized egg (a), fertilized egg (b), and embryonated egg (c)
(Courtesy of the Department of Parasitology, UP-CPH)  

to the cecum or proximal colon where they of the infection. Ascariasis was estimated
es timated to have
 penetrate the intestinal
intesti nal wall. These larvae enter contributed to a total of 1.85 million disability-
the venules to go to the liver through the portal adjusted life years (DALYs) in 2004.  
vein, on to the heart and pulmonary vessels The varied pathology of ascariasis includes
where they break out of capillaries to enter the the reaction of tissues to invading larvae,
air sacs. In the lungs, larvae undergo molting irritation of the intestine by the mechanical
 before migrating to the larynx and oropharynx and toxic action of the adult, and complications
to be swallowed into the digestive tract. This arising from the parasite’s extraintestinal
hepato-tracheal migration phase takes about
hepato-tracheal migration (Plates 3.2 – 3.4).
3.4). The usual infection
14 days, while the development of egg-laying  of 10 to 20 worms may not show symptoms,  
adult wor ms  takes  a bout 9 to 11  week s af ter hence, may go unnoticed  by  the host unless
eg ingest1ioyear.
is gabout  pan  of  an adult  wor m
n . Th  e lif e s p it is discover edpassing
spontaneous examinain
  by stooofl worms n ostool.
tiothe r  the  
A female  Ascar
 Ascarisis produces about 200,000 During lung migration, the larvae may
eggs per day, but this number decreases with cause host sensitization resulting in allergic
increasing worm load. The eggs are deposited manifestations such as lung infiltration,
in the soil when a person with Ascaris infection asthmatic attacks, and edema of the lips.
defecates indiscriminately.
indiscriminately. In the soil, it takes Symptoms of difficulty of breathing and fever
about 2 to 3 weeks for eggs to develop into the similar to pneumonia may occur as a result
infective stage (embryonation) under favorable of penetration by several larvae through the
conditions with suitable temperature, moisture, lung capillaries as they enter the air sacs.  
and humidity. The larvae undergo two molts to The most frequent complaint of patients is
reach their 3rd stage within the egg and become vague abdominal pain. Eosinophilia is present
embryonated. Only when this infective egg is during larval migration. Moderate infections
i nfections
swallowed can humans become infected with may produce lactose intolerance and vitamin
is (Figure 3.1). The embryonated eggs can
 Ascaris
 Ascar A malabsorption. Heavy infections are likely
survive in moist shaded soil for a few months to cause bowel obstruction (due to bolus
to about two years in tropical and sub-tropical formation), intussusception, or volvulus that
areas, but for much longer in temperate regions.   may result in bowel infarction and intestinal
 perforation. 
Pathogenesis and Clinical Manifestations  
Serious, and at times, fatal effects of
A majority of As ca ri s infections are ascariasis are due to erratic migration of adult
asymptomatic, although an estimated 120 to worms. They may be regurgitated and vomited,
220 million cases exhibit morbidity as a result  may escape through the nostrilsor rarely, inhaled 
 

CHAPTER 3: Nematode Infections   131 

idnutcotsthther tor uacghetah. eTahme p
  wuollr amosf  m
Vatyer inavnaddee b
ntieler at bhesciensstest.inPaelnw
etar alltiionntootf hteh pe ew
r itoor nmesalthcar oviutgyh
the gallbladder or liver. Patients with biliary may occur and result in either acute peritonitis
ascariasis experience severe colicky abdominal or chronic granulomatous peritonitis.  
 pain, which is brought about by the movement
of the worms inside the biliary tract. Worms
Complications brought about by the larvae
and adult worms are a cause for concern. The
may also lodge in the appendix or occlude the continuous biting or pricking of the intestinal
 pancreatic duct and cause acute appendicitis or mucosa for food by a few Ascaris adults may
 pancreatitis, respectively.
respectively. Intestinal
Intestinal bacteria may irritate nerve endings in the mucosa and
 be carried to these migration sites producing  result in intestinal spasm leading to intestinal  
 

132   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Plate 3.2. Ascaris
3.2. Ascarisin
in the liver Plate 3.3. Intestinal obstruction with Ascaris
with Ascaris
(Courtesy of Dr. Benjamin Cabrera) (Courtesy of Dr. Benjamin Cabrera)

In the laboratory, direct fecal smear (DFS),

Kato thick Smear, Kato-Katz techniques, as well
as concentration techniques, such as formalin-
ether/ethyl acetate concentration technique
(FECT), are stool examination techniques
used to diagnose ascariasis by confirming the
 presence of eggs in the
the fece
feces.
s.
DFS is less sensitive compared to the Kato
thick Smear and Kato-Katz techniques. The last 
two methods are useful for both individual and
mass screening in schools or in the community.
Kato-Katz technique also provides quantitative
diagnosis in terms of the intensity of helminth
infection in eggs per gram (epg) of stool
s tool that is
Plate 3.4. Ascaris
3.4. Ascarisin
in the brain useful in monitoring the efficacy  of treatment in
(Courtesy of Dr. Benjamin Cabrera)
clinical trials, as well as public health programs.
A study in China comparing the sensitivity of
obstruction. Hence, a child need not harbor different diagnostic techniques for helminth
hundreds of Ascaris adults to produce intestinal
 Ascaris
infections showed that Kato-Katz had a
obstruction. sensitivity of 98%, while sodium acetate-acetic
Diagnosis  acid-formalin (SAF) concentration technique
had a sensitivity of 93% for the diagnosis of
Clinical diagnosis of ascariasis is rather is infections. In a local study, the
 Ascaris
 Ascar t he sensitivity
inaccurate because
because the signs and symptoms are   for the detection of Ascaris through single and
quite vague and are indistinguishable from those
of other intestinal nematode infections or from double Kato-Katz
and 99.9%, stool sample/s
respectively. were
In addition, in a96.9%
local
non-parasitic infections. Hence, the clinical study comparing the sensitivity of DFS and
diagnosis of ascariasis should be confirmed  FECT for the screening of food handlers, FECT
or established by microscopic examination of was shown to have a higher sensitivity and
a stool sample. The disease should be highly detection rate for intestinal parasite infections
suspected in a child who reportedly passed out compared with DFS. 
the worm with
w ith his feces. 
 

CHAPTER 3: Nematode Infections   133 

Treatment  Integrated Helminth Control Program (IHCP)

of the Department of Health (DOH),
(DOH) , is being
Individual infections are cured by a single conducted in elementary schools every January
dose of any
an y ofthebro
broad-s
ad-spectr
pectrum
um anthelminthc
anthelminthcis
is and July for school-age children through the
such as albendazole, mebendazole,
mebendazole, and pyrantel Department of Education (DepEd). MDA for
 pamoate. A recent
meta-analysis systematic
revealed review and 
that a single-dose  preschool-age
 preschool-age children is being
being conducted
conducted under
the Garantisadong Pamabata program through 
or aaml oaa b
 p l bte nhdaadzocle
ur ,em
r ae b
tees nodf a9z3o.l9e,%a,n9d6 p.5y%
r a,natenld the DOH and the local government units. In
87.9%, respectively. Albendazole is given at filariasis endemic areas, MDA with albendazole
400 mg single dose (200 mg for children 12-23 and diethylcarbamazine every November also 
contribute to the control of STH. The IHCP
IH CP
months), mebendazole at 500 mg single dose,
and pyrantel pamoate at 10 mg/kg (max. 1 g)
targets an MDA coverage of at least 85% of the
target population.
also as a single oral dose. Ivermectin has been
The WHO recommends targeting other
shown to be as effective as albendazole if given
high-risk groups such as women of child-
at a dose of 200 µg/kg single dose. Nitazoxanide
 bearing age and pregnant women. Pregnant
Pregnant
may be given at 500 mg twice a day for 3 days
women in their 2nd or 3rd trimester,
trim ester, as well
(100 mg twice a day for 3 days
d ays for children 1-3
years old; 200 mg twice a day for 3 days for
as lactating women may receive albendazole or
children 4-11 years old). 
mebendazole. Children less than one year old
and pregnant women in their first
first trimester
 trimester
Benzimidazoles,
Benzimidazoles, such as albendazole are ineligible for MDA with albendazole or  
and mebendazole, bind to the
th e parasites’ 
parasites’ 
 b-tubulin
 b-tubul in resulting in the disruption
disrupt ion of parasite mebe n d a z ole .
microtubule polymerization. This binding R e  of
c eregular
 benefits of
 benefits n t studideworming
eshave
hav e rreve
eveale
aledd tha
in thethatt the
school-
eventually results in the death of adult worms age group include improvements in iron
that takes several days. Adverse reactions to these stores, growth and physical fitness, cognitive
anthelminthics are rare, mild, and transient.  performance and school attendance. In
These are epigastric pain, headache, diarrhea, younger children, studies have shown improved
nausea, vomiting, and dizziness, among
nutritional indicators such as reduced wasting,
others. These reactions may be minimized by  
stunting, and improved appetite. 
administering the deworming tablet after a Use of anthelminthics to control helminth
meal. 
infections in livestock resulted in anthelminthic
anthelminthic
In 2001, the World Health Assembly
resistance to all drug classes. Although there
recommended preventive chemotherapy among have been a few reports on the reduced efficacy
high risk groups (e.g., preschool- and school-age of anthelminthics in humans, these reports
children) for morbidity control in communities  were unable to show evidence of genetically  
inhf eecr teiotnhse ics ugm
w anr e2v0a%
r eualtaetr ivteh p len. cPer eovf enStTivHe transmitted drug resistance. Currently, drug
chemotherapy is done through mass drug resistance monitoring involves the identification
administration (MDA) with anthelminthics, of molecular or genetic markers for resistance
specific to each of the anthelminthic drug
either alone or in combination, among target classes.  
 populations,
 populat ions, even without
witho ut the benefit  of stool
examination. The World Health Organization Epidemiology 
(WHO) recommends coverage of at least
 Ascaris has a cosmopolitan distribution
75% of the target populations during MDA.
In the Philippines, MDA, as part of the 
(Figure 3.2). About 1.2 billion people globally  
 

134   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Figure 3.2. Global distribution of soil-transmitted helminth (STH) infections and proportion of children
requiring preventive chemotherapy for STH infections in each countr y
(From World Health Organization. Helminth control in school-age children: a guide for managers of
control programmes. 2nd ed. Geneva: World Health Organization; 2011.)  

are estimated to have ascariasis, and about 2,000 reported an overall prevalence of 27.7%
die annually. The disease remains endemic in among school-age children and 30.9% among
many countries of Southeast Asia, Africa, and  preschool children. Prevalence rates are
are parallel
parallel
Central and South America. Children ages  with those of trichuriasis due to similar modes
5 to 15 years have the highest intensities of of infection and risk factors. 
infection with Ascar is compared with the other
 Ascaris The level of transmission of  Ascaris and
age groups. Children are particularly vulnerable other STH from soil to humans depends on
since they are at risk of ingesting embryonated socio-economic factors more than on physical
is eggs while playing in soil contaminated
 Ascaris
 Ascar factors. The main factors appear to be
b e a high
with human feces.  density of human population, involvement  
Worldwide es timate s reveal that the in agriculture (including use of night-soil as
highest number of cases of ascariasis is found  fertilizer), illiteracy, and poor sanitation. Poor  
in East Asia and the Pacific  Islands, although   health education on personal, family, and
lumbricoides is also known to be able to
 A. lumbricoides community hygiene are also important factors
survive colder temperatures compared with contributing to the transmission of Ascaris . 
Trichuris and hookworm. In many low and
Prevention and Control 
middle income countries like the Philippines,
the prevalence may reach 80 to 90% in certain Surveillance and monitoring are important
high risk groups like public elementary school components of an STH Control Program.
children. Recent local sentinel surveys have  Baseline cumulative prevalence and prevalence 
 

CHAPTER 3: Nematode Infections   135 

of heavy intensity infections should becompared using Kato-Katz method. Monitoring is

with follow-up (pre-treatment) data (Table recommended every 2 years. Reinfection is
3.1). The WHO recommends parasitologic usually observed four months post-treatment
post -treatment
monitoring involving the selection of 5 to 10 and full reinfection appears at 6 or 7 months
schools to represent a district or municipality. after treatment; although in communities with
Stool samples from 50 school children from  poor environmental sanitation (Figure 3.3),
each school will be collected for examination  reinfection may take place immediately after  

Table 3.1. Core indicators of mass drug administration for soil-transmitted helminth infections

Numerator:  of individuals
positive for any STH infection

STH

STH

Source:
Department of Health. Administrative Order no. 2006-28: Strategic and operation framework for establishing Integrated Helminth Control
Program (IHCP). 2006.
World Health Organization. Helminth control in school-age children: A guide f or managers of control programmes. 2nd ed. Geneva: World
Health Organization; 2011.
 

136   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Figure 3.3. Schematic life cycle of soil-transmitted helminths

(From World Health Organization. Prevention and control of schistosomiasis and soil-transmitted
helminthiasis. Geneva: World Health Organization; 2002. p. 145.)

deworming. Nutritional status and school framework (Table 3.2) for the control of STH
 performance
 performan ce may also be monitored
monitore d alongside
alongsid e infections. When mass treatment is being
 parasitologic parameters.  undertaken, submission to the said intervention
Prevention and control measures for  Asca
 Ascaris
ris should be a goal of health education.
and other STH infections involve provision of War on Worms (WOW) approach in
safe water, environmental sanitation, hygiene Biñan, Laguna is a school-based,
school-based, school teacher-
education, and regular deworming, which assisted mass drug administration led by the
are the components of the WASHED (water, Local Government Unit (LGU) which started in
sanitation, hygiene, education, deworming)  1999. The approach was initially supported by 

Table 3.2. The WASHE D framework for a comprehensive control of soil-transmitted helminth infections

Drainage and disposal/re-use/recycling of household wastewater (also referred to as gray

Safe collection, storage, treatment, and disposal (feces and urine)

Management/re-use/recycling of solid waste
STH
Dissemination of key messages
messages to promote the following practices:
 

CHAPTER 3: Nematode Infections   137 

Johnson & Johnson, Inc. (J&J) and eventually

eventual ly do not reach the point of eradication due
du e to
taken over by LGU and the Department of implementation challenges and the limited
Education (DepEd) District of Biñan. Part of  practice of the WASHED strategies in the
the WOW experience was that STH infections   communities (Figure 3.4).

Figure 3.4. Comparison of cumulative prevalence in San Vicente Elementary School (SVES) and sentinel
schools in Biñan, Laguna from 1999 to 2010 (Courtesy of Dr. Vicente Belizario, Jr.)

References  or in combinations against Ascaris and

Trichuris spp. Bull World Health Organ.
Albonico M, Crompton DWT, Savioli L.
2003;81:35 – 442.
2.
Control strategies for human intestinal
Bethony J, Brooker S, Albonico M, Geiger
nematode infections. Adv Parasitol.  
SM, Loukas A, Diemert D, et al . Soil-
1999;42:278 – 341.
341.
transmitted helminth infections: ascariasis,
Belizario VY, Totañes FG, de Leon WU,
trichuriasis, and hookworm. Lancet.  
Lumampao YF, Ciro RT. Sentinel
2006;367:1521 – 32.32.
surveillance of soil-transmitted 
Brooker S, Clements RC, Bundy DA. Global  
ser 
ageelmcihniltdhr iaensisinin p
h lecsctehdoolol-caglegaonvder snchmoeonlt- epidemiology, ecology and control of
soil-transmitted helminth infections. Adv 
units in the Philippines: follow-up
Parasitol. 2006;62:221 – 6
61.
1. 
assessment. Asia Pac J Public Health.  
Forthcoming 2013.
Cabrera BD, Caballero B, Rampal L, de Leon  
W. Control of ascariasis through targeted
Belizario VY, Amarillo ME, de Leon WU,
chemotherapy,
chemotherapy, ascariasis and its prevention
de los Reyes AE, Bugayong MG,
and control. London, New York and
Macatangay BJ. A comparison of the
Philadelphia: Taylor and Francis; 1989.
efficacy of single doses of albendazole,  p. 169 – 83.
83.
ivermectin, and diethylcarbamazine alone 
ivermectin,
 

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Children Without Worms (CWW). A infections: systematic review and meta-

comprehensive strategy for STH control analysis. JAMA. 2008;299(16):1937 – 448.
8. 
[Int
[Internet
ernet].]. 2011
201 1 [cited
[cit ed 2012
201 2 Mar 5]A.vailable  Ng KK, Petersen JF, Cherney MM, Garen C,
from  www.childrenwithoutworms.org. 
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Department of Health. Integrated helminth  basis for
fo r the inhibition
inhibit ion of porcine pepsin
pepsi n
control program. Mass treatment guide,  by Ascaris pepsin inhibitor-3. Nat Struct
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2 006 – 2010
2010  Biol. 2000;7:653 – 7 7..
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O’Lorcain  P, CV Holland. The public health
Department of Health; 2006.  importance of  Asca
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Department of Health. Guidebook for a Parasitol. 2000;121:S51 – 7 72.
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disease prevention and control program for Sinniah B. Daily egg production of  Ascaris
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diarrheal diseases. Manila (Philippines): the faeces and the variability of egg counts.
Department of Health Philippines; 2010.
2010.  Parasitol. 1982;84:167 – 7
75.
5. 
Disease Control Project Priorities. Deworming Sinniah B, Subramaniam K. Factors influencing
children brings huge health and the egg production of Ascar
 Ascaris
is lumbricoides:
lumbricoides
development
development gains in low-income countries relationship to weight, length and diameter
[Internet]. 2008 [cited 2012 Mar 3].  of worms. J Helminthol. 2009;65:141 – 77.. 
Available from http://www.dcp2.org/
from http://www.dcp2.org/ Solon FS, Sarol JN, Bernardo ABI, Solon
file/162/dcpp-helminths-web.pdf
file/162/dcpp -helminths-web.pdf JAA, Mehansho H, Sanchez-Fermin LE,
Dold C, Holland CV.  Ascaris and ascariasis.  et al. Effect of a multiple-micronutrient-  
Micr o bes Inf ect. 2010;13(7):632 – 7.   i  po wder  bever ag o n the
f or  if ied f rr u
E ar ar DG, Belizar io VY, R elos JR . Pr evalence
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of intestinal parasitic infections among food nutr ition status,  physical f itness,  and
cognitive performance of schoolchildren in
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Infect Dis. 2004;33(3):99 – 103.
103.  XZ, Jiang JY, Li LH, et al. Extensive
Evans B. Securing sanitation:
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Geerts S, Gryseel B. Drug resistance in human Tielsch JM, Jape JK, Albonico Metal . Low
helminths: current situation and lessons dose daily iron supplementation improves
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Gilleard JS, Beech RN. Population genetics   improves growth, appetite, and anemia
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Horton J. Albendazole:
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nematodes . Parasitola .review of anthelmintic
2007;134:1133  – 47.  Tarafder MR, Carabin H, Joseph L, Balolong
efficacy and safety in humans. Parasitol.
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2000;121:S113 – 32.
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Keiser J, Utzinger J. Efficacy of current stool examination technique for detection
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Trichuris trichiura infections in humans World Health Organization. Preventi

Preventive
ve
in the absence of a ‘gold
‘gold  standard.’
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 Int J chemotherapy in human helminthiasis:
Parasitol. 2010;40:399 – 404.
404. coordinated use of anthelmintic drugs in
World
World Health Organization. Prevention
Prevention control interventions: a manual for health
and control of schistosomiasis and soil-  professionals
 professio nals and programme
pr ogramme managers.
ma nagers.
transmitted helminthiasis. Geneva: World
World Geneva: World Health Organization;2006.  
Health Organization; 2002. p. 63. World Health
Health Organization. Helminth control  
World Health Organization. The global burden
World in school-age children: a guide for managers
of disease 2004 Update. Geneva: World of control programmes. 2nd ed. Geneva:
Health Organization; 2008.   World Health Organization; 2011.  
 

140   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Trc
i hurs
 i tr ichi 
ura
Vicente Y. Belizario, Jr., Francis Isidore G. Totañes

richuris trichiura or the whipworm is a

soil-transmitted helminth, and is classified
classified  
as holomyarian, based on the
th e arrangement of
somatic muscles in cross-section where the cells
are small, numerous, and closely packed in a
narrow zone. 
Parasite Biology 

The male worm (Plate 3.5a) measures 30

to 45 mm, slightly shorter than
th an the female,
which is 35 to 50 mm long. The female (Plate
Plate 3.6. Trichuris egg 
3.5b) has a blunt posterior end, while the male (Courtesy of the Department of P arasitology,
has a coiled posterior with a single spicule and UP-CPH)
retractilesheath.Thewormshavean attenuated
anterior three-fifths traversed by a narrow yellowish outer and a transparent inner shell.
esophagus resembling a string of beads. The   Fertilized eggs are unsegmented
unsegmented at oviposition 
o us  pos e io wo-fif  hs co ai he i es i e
lays
setr otf r e pr otductivnet on
tsinglte r 
r an bd aapproximately rr  gtans.gs
3,000 to10,000eggs
10,000eg
nAt f etmnale
perday.   andhost
the embryonic
when eggs
development
are deposited
takes
inplace
clayish
outside
soil.  
Compared with  Ascar is eggs, Trichuris eggs in
 Ascaris
soil are more susceptible to desiccation.  
Larvae are not usually described probably
 because soon after the embryonated eggs 
are ingested, the larvae escape and penetrate
intestinal villi where they remain for 3 to 10
days. Trichuris worms inhabit the cecum and
the colon. The worms secrete a pore-forming
 protein, called the TT47 that allows them to
imbed their entire whip-like portion into the
intestinal wall. After copulation, the female
worm lays eggs, which are passed out with the  
il. U
f ceocneds iatniodnds,e ptohseitegdgisn dtheveeslo p er ef caovm
a nd b or ea ble
Plate 3.5. Trichurismale(a) and female (b) embryonated within 2 to 3 weeks. If swallowed,
(Courtesy of the Department of Parasitology, the infective embryonated eggs go to the small
UP-CPH) intestine and undergo four larval stages to
 become adult worms. This process takes about
The approximate measurements of the 12 weeks (Figure 3.5). Unlike  Ascaris, there is
egg are 50 to 54 µm by 23 µm. It is lemon- no heart-lung migration. Each female worm can
or football-shaped with plug-like translucent  produce about 60 million eggs over an average
 polar prominences (Plate 3.6). The egg has a  lifespan of 2 years. 
 

CHAPTER 3: Nematode Infections   141 

Figure 3.5. Life cycle of Trichuristrichiura

Pathogenesis and Clinical Manifestations   is common. The lumen of the appendix may be
filled with worms, and consequent irritation
filled with
The anterior portions of the worms,
and inflammation may lead to appendicitis or
which are embedded in the mucosa, cause granuloma formation. 
 petechial hemorrhages, which may predispose
predispos e The intensity of infection is important in
to amebic dysentery, presumably because the understanding the clinical picture. Infections
ulcers provide a suitable site for tissue invasion with over 5,000 T. trichiura eggs per gram of
 by E. histolytica. The mucosa is hyperemic and
histolytica
feces are usually symptomatic. In patients with
edematous; enterorrhagia
enterorrhagia or intestinal bleeding  heavy intensity infection,
infection, the worms may be 
 

142   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

found throughout the colon and rectum, and  patient suffers from frequent blood-streaked
may result in Trichuris dysentery syndrome diarrhea, abdominal pain and tenderness, and
manifested by chronic dysentery and rectal rectal prolapse where adult worms attached to
 prolapse (Plate 3.7).
3.7). Such cases of heavy chronic
chronic the rectal mucosa can be seen. In light infections
i nfections
trichuriasis are often markedby frequent blood- where symptoms are absent, laboratory diagnosis
streaked diarrheal stools, abdominal pain and is essential. 
tenderness, nausea and vomiting, and weight  Laboratory diagnosis may be done by  
loss. Anemia is strongly correlated to heavy direct fecal smear (DFS) with a drop of saline.
intensity trichuriasis, and blood loss from such An alternative diagnostic technique is the Kato
infections can range from 0.8 to 8.6 ml per day.  thick smear method that uses about 20 to 60  
Furthermore, infection with over 800 worms mg of stool sample. This method is highly
can result in anemia in children. On
O n the other recommended in the diagnosis of trichuriasis.
hand, light infections are moderately
moderately associated The Kato-Katz technique is a quantitative
with anemia, although these infections are method that employs egg counting to determine
usually asymptomatic and the presence of the the intensity of helminth infection. This
 parasite may be discovered
discovere d only in routine stool technique can be used to assess the efficacy
efficacy  o
off
examinations. Trichuriasis has also been shown anthelminthic drugs in terms of cure rate (CR)
to result in poor appetite, wasting, stunting, and egg reduction rate (ERR). This technique
as well as reduced intellectual and cognitive can also be used for epidemiological surveys for
development in children.  the monitoring of a helminth control program.
Both Kato thick and Kato-Katz techniques are  

n p
ie ile
sm  p stfimt thf od sthth  dt ht vt hn hf
s t v tnd nd s p
lei ia yeggs,
a low-as r  e of
i ci eyas eggs
ceocwell igo
eac eio soil-
a eother
Trichuris
transmitted helminths. A single Kato-Katz
examination has a sensitivity and specificity for
the detection of Trichurisof 91.4% and 94.4%,
respectively. 
The acid-ether and the formalin-ether/
ethylacetate concentration techniques can also
 be used for the diagnosis of trichuriasis. The
FLOTAC technique has also been shown
sho wn to be
more sensitive in the diagnosis of trichuriasis
Plate 3.7. Rectal prolapse in a 9-year old female
compared with Kato-Katz and ether/ethyl
seen at the Philippine General Hospital with
heavy Trichurisinfection acetate concentration techniques.
(Courtesy of Dr. Benjamin Cabrera)
Treatment 
The prognosis of trichuriasis is very good. The drug of choice in the treatment of
Because there is no larval migration through the trichuriasis is mebendazole given 100 mg twice
lungs as in Ascar
 Ascaris
lung pathology and hookworm
isoccurs.   infections, no a day
an for 3 days.
alternative Albendazole
drug. may be used as
Both are benzimidazole
Diagnosis 
derivatives and are available as chewable tablets.
Administration of mebendazole 500 mg once o nce a
Clinical diagnosis is possible only in very day for 3 days has beenshown to have the highest
heavy chronic Trichuris infection where the  cure rate (71%) compared with albendazole 400 
 

CHAPTER 3: Nematode Infections   143 

mg given once a day for 3 days (56%).

(56%) . For the Prevention and Control 
 purposes of
o f preventive
prevent ive chemotherapy
chemot herapy through
thr ough
mass drug administration, mebendazole is given Strategies for the prevention and control
of Trichuris infection are similar to those for
as a 500 mg single dose, while albendazole is
 Asca ris infections. The WHO recommends
 Ascaris
given as a 400 mg single dose. In recent local
studies, it has been shown that albendazole in  biannual mass
mebendazole 500drug administration
mg or with
albendazole 400 mg  
combination with ivermectin, a drug that is 
also used to treat filariasis, exhibited better cure  awmheor negtshceh poor el-vaaglenccheilodf r eSnTiH
n  cionm ctiuonnistieis 
f em
and egg reduction rates than
t han albendazole alone.
alone. 
A contraindication for mebendazole
≥ 50%. Treatment of otherhigh-risk groupssuch
and albendazole is hypersensitivity and early as preschool children, women of childbearing
age, including pregnant women in the 2nd
 pregnancy (within
(wit hin the 1st trimester). Adverse
effects of these two drugs are usually mild and and 3rd trimesters as well as lactating women,
transient and may present as headache, nausea, adults in certain high-risk occupations should
also be considered. On the other hand, once a
vomiting, gastrointestinal discomfort, and
itchiness. 
year treatment is recommended in communities
with STH prevalence <50%. Other
O ther strategies
Deworming of children has been
shown to contribute to improved motor and
such as provision of safe water, environmental
sanitation, and hygiene education are also
language development, as well as to reduced 
important in STH control. 
malnutrition. Nutritional status and intellectual
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and tropical countries but is more widely
de los Reyes AE, Bugayong MG,
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Macatangay BJ. A comparison of the
Approximately 604 to 795 million are infected
globally. In tropical and subtropical regions,
efficacy of single doses of albendazole,
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2003;81:35 – 442.
2. 
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SM, Loukas A, Diemert D, et al. Soil-
the highest intensities of infection. In a recent 
sentinel survey in the Philippines, the prevalence transmitted helminth infections: ascariasis, 
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is similar to that
co-infections of  A.the
with lum
lumbri
bricoi
two des. Prevalence
coides
helminths of
is 19.1% entire community and selective treatment
of children alone in the total prevalence
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of soil-transmitted helminthiases in two 
 

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a o -f o i
T r ichur i s is o i   o
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e : 25r 
5
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Province, , Lain -aHRepublic
People’s
vuiallaLg, etoaf l.YEuxntn
enansive
of China,
Bellinger DC, Langdon GC, Manalo DL, revealed by a suite of diagnostic methods.
et al. Helminth infection and cognitive Am J TropMed Hyg. 2008;7
2008;78(5):76
8(5):760
0 – 9
9.. 
impairment among Filipino children. Am Tarafder MR, Carabin H, Joseph L, Balolong
J Trop Med Hyg. 2005;72(5):540 – 8.
8. E, Olveda R, McGarvey ST. Estimating
Glinz D, Silue KD, Knopp S, Lohourignon the sensitivity and specificity of Kato -Katz
LK, Yao KP, Steinmann P, et al. Comparing
Comparin g stool examination technique for detection
diagnostic accuracy of Kato-Katz, Koga of hookworms, Ascaris lumbricoides and
agar plate, ether-concentration, and Trichuris trichiura infections in humans
FLOTAC for Schistosoma
Schistosoma mansoniand soil- in the absence of a ‘gold
‘gold  standard.’
standard.’ Int
 Int J
transmitted helminths. PLoS Negl Trop Parasitol. 2010;40:399 – 404.404.
Dis. 2010;4(7):e754. World Health Organization. Preve Prevention
ntion
Hadju V, Stephenson LS, Mohammed HO,  and control of schistosomiasis and soil-  
Bowman DD, Parker RS. Improvements transmitted helminthiasis. Geneva: World
of growth, appetite, and physical activity Health Organization; 2002. p. 63.
in helminth-infected school boys 6 months
after
Clinsingle
Nutr.dose of albendazole.
1998;7(2):170 6Asia
 – 6.. Pac J  
 

CHAPTER 3: Nematode Infections   145 

Hookworms
Vicente Y. Belizario, Jr., Francis Isidore G. Totañes, John Robert C. Medina

Necatoramericanus has a broad, membranous caudal bursa with

  rib-like rays, which are used for copulation. The 
 Ancyo
l stomaduodenae
l  buccal capsule has a ventral pair of semilunar
semil unar
cutting plates (Plate 3.8a). The head is curved
T  he hookworms that infect humans are  
 Necator americanus and Ancy  An cy los to
toma
duodenale, which are soil-transmitted helminths.
ma opposite to the curvature of the body, which is
like a hook at the anterior end. 
They are blood-sucking nematodes that attach The adult  A. duodenale is slightly larger
to the mucosa of the small intestines. They than N. americanuss. Each adult has single-paired
americanu
are most commonly found in tropical and male or female reproductive organs. Unlike the  
subtropicalcountries where they occur as single americanus, the head of the A. duodenale
 N. americanus duodenale
or mixed infections.  adult continues in the same direction as the
curvature of the body. The buccal capsule has
Parasite Biology 
two pairs of curved ventral teeth (Plate 3.8b).  
Allhookworms have the meromyarian type Rhabditiform larvae of  N. americanus
of somatic muscle with two to five cells arranged and A. duodenale are indistinguishable. They
 per dorsal or ventral half.  resemble those of Strongyloides
Strongyloides stercoralis, but are 

 N. america
americanus
nus
adults
fusiform, grayish-white
grayish-whit are small, cylindrical,
e nematodes. Females (9-  d ehwahvaet alalrr og  ner 
saonm
 primord
 primordium ium is smaller g,em
r   bour eccinaathookworms
hookwor
Tphosetegr ein
ltecnauvaitye.d  ph
ms compared or itllyya,l
11 mm by 0.35 mm) are larger than males (5-9
mm by 0.30 mm). The posterior end of the male  with S. stercoralis. 

Plate  3.8.  Bucc al c apsule s o f hoo kwor ms: N  c  anus (a) and A
.amei r  uod 
 A.d  enal e (b) 
(Courtesy of Dr. Benjamin Cabrera)
 

146   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

The buccal spears of the  N. americanus

filariform larva (Plate 3.9) are conspicuous
filariform larva
and parallel throughout their lengths. There
are conspicuous transverse striations present
on the sheath in the tail region. In contrast,
the filariform larva of  A. du od
oden alee has
enal
inconspicuous buccal spears and transverse 
striations on the sheath in the tail region.

Plate 3.10. Hookworm egg

(Courtesy of the Department of Parasitology,  
UP-CPH)

and transforms into the non-feeding filariform

larva (L3), the infective stage of the parasite. 
Filariform larvae penetrate the skin and
enter venules. They migrate to the heart and
lungs, and then into the alveoli. The larvae then
ascend to the trachea and are finally swallowed,
and passed down to the small intestine where
the worms become sexually mature and the
female will start laying eggs. 
Plate 3.9. Hookworm filariform larvae
(Courtesy of the Department of Parasitology, Pathogenesis and Clinical Manifestations  
UP-CPH)
The pathology of hookworm infection
It is quite difficult to distinguish the eggs of   involves: (a) the skin at the site of entry of the
 A. duodenale from those of N. americanus . The filariform larvae,
filariform  larvae, (b) the lung during larval
eggs have bluntly rounded ends and a single thin migration, and (c) the small intestine, the
transparenthyaline shell. They are unsegmented habitat of the adult worms. 
at oviposition, and are in the two- to eight-cell Penetration of thefilariform larvae through
stage of division when passed out withw ith fresh the skin produces maculopapular lesions and
feces (Plate 3.10).   localized erythema. Itching is often severe, and 
The hookworm life cycle (Figure 3.6)
is d irect and begins with the adult worms   it is known as “ground
“ground  itch” 
itch” or “dew
“dew  itch,”
itch,”  as
it is related to contact with soil, especially on  
copulating while attached to the mucosa of the a dewy morning. Itching, edema, erythema,
small intestines. Female worms oviposit into and later papulovesicular eruptions can last for
the intestinal lumen and the eggs are passed out 2 weeks. If the larvae migrating through the
with human feces. In the soil, the embryo within lungs are abundant, bronchitis or pneumonitis
the egg develops rapidly and hatches after 1 to 2 may result. In the course of migration, these
days into the rhabditiform larva. After 7 to 10 larvae produce minute hemorrhages with
days, the larva undergoes two stages of molting,  eosinophilic and leukocytic infiltration,
infiltration,  but 
 

CHAPTER 3: Nematode Infections   147 

Figure 3.6. Life cycle of hookworms

these manifestations seem to be rare in the lymph, and protein. Other symptoms are
tropics. In the stage of maturation of the exertional dyspnea, weakness, dizziness, and
worm in the intestine, there is abdominal pain, lassitude, while signs include rapid pulse,
steatorrhea, or sometimes diarrhea with blood
steatorrhea, edema, and albuminuria. Unlike in ascariasis,
ascariasis,
and mucus, as well as eosinophilia.   the complications in hookworm infection are
Hookworm infection is usually chronic, quite mild, and remedial measures are readily
hence patients often show no acute symptoms.   applied. In general, the prognosis of hookworm  
Studies have shown greater blood loss per worm infection is good.  
 per day in A. duodenale infection compared with 
duodenale During the migration of the larva in the
 N. americanus infection. Chronic moderate human body,the
body,t he parasite continuously presents
or heavy hookworm infection results in a diverse immunogenic challenges to the host.
 progressive, secondary, microcytic,
microcytic, hypochromic
hypochromic Extensive humoral responses are produced
anemia of the iron-deficient type, due primarily against the larva and the adult hookworm,
to continuous loss of blood. which share many antigens. Cellular immune
Hypoalbuminemia is another manifestation response is primarily mediated by eosinophils,
of hookworm infection. There is low level   mast cells, and Th2 cells. Despite all of these,
of albumin due to combined loss of blood,   there has been no clear evidence that the  
 

148   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

host develops perpetual immunity against one end immersed in water. Culture
hookworm infection; however, polyvalent IgE methods are recommended for species
antibodies have been suggested to provide some identification.  
identification.
 protective roles. 
Molecular approaches, which include
Diagnosis  PCR-based detection dofimmunosorbent
feces and enzyme-linked
enzyme-linke hookworm DNA in 
assay
The clinical picture, though characteristic, 
is not pathognomonic to permit differentiation (cEo pLr IoSaAn)tif goer ntsh,ehdaevteecatlsi on boeef nsedcr eevteolor  p
y/eedx.cr etor y 
from other helminth infections. Final diagnosis
depends on the identification of parasite Treatment 
ova in the feces. The following techniques
are inexpensive and can be applied to both
All diagnosed cases of hookworm infections
should be treated; however, where the risk
r isk
individual and mass screening: 
of reinfection is high, mass screening before
1.  Direct fecal smear is of value only when treatment may be impractical. As with other
the infection is
i s quite heavy. It may not soil-transmitted helminth infection control, the
detect the parasite in light infections WHO recommends mass drug administration
(i.e., egg count of <400 eggs per gram among school-age children at least once a
feces).  year for communities with cumulative STH
2.  The Kato thick or Kato-Katz method  prevalence greater than or equal to 20%.
20%.  
may increase detection rates since Treatment of other high-risk groups such as
more stools are examined using these  preschool children,
children, women
women of childbearing
childbearing age,
including pregnant women in the second and
techniques.
also provideThe latter technique
quantitative diagnosismay
by third trimesters and lactating women, should
determining the intensity of infection also be considered. 
in terms of number of helminth eggs Albendazole, the drug of choice, is
 per gram of feces. The disadvantage
disadvan tage of larvicidal and ovicidal against N. americanus
these methods is the rapid clearance of and A. duodenale . It is given as a 400 mg single
hookworm eggs after 30 to 60 minutes dose for adults and children over 2 years old.
with the use of glycerine as a clearing Chewable tablets or suspension
s uspension preparations
preparations are
agent.  available. Mebendazole for children and adults
3.  Concentration methods like zinc is given as a 500 mg single dose. These drugs are
sulfate centrifugal flotation and    both benzimidazol
ben zimidazolee derivatives
derivati ves that block the
the formalin-ether/ethyl acetate uptake of glucose by most intestinal and tissue
concentration method use greater nematodes. Adverse effects for both drugs are
quantity of stool that may contribute   rare, and are usually mild and transient. These 
to the increase
i ncrease in sensitivi
se nsitivity.
ty. FLOTAC,
FLOTAC,
which is also a centrifugal flotation 
include epigastric pain, diarrhea, headache, and
dizziness, among others.  
method, has been shown to have a Anemia and hypoproteinemia should also
higher sensitivity for the diagnosis of  be addressed
address ed by giving
gi ving iron
i ron supplementati
supp lementation
on
soil-transmitted helminths compared and adequate diet. 
with multiple examinations of Kato- In recent years, tolerance and resistance of
Katz smears.  human hookworms to these drugs had been
4.  Culture methods like the Harada- reported in countries where regular deworming
Mori allow hatching of larvae from is the main control strategy. Studies had shown
eggs on strips of filter paper with   that the use of the recommended single dose 
 

CHAPTER 3: Nematode Infections   149 

of the drugs led to low cure rate. Monitoring high. Among pregnant women and adolescent
the efficacy of
efficacy of and drug resistance to these females, the prevalence rates are 5.5% and
 benzimidazole derivatives has
 benzimidazole has not yetbeen
yetbeen done 2.8%, respectively. A study among military
in the local setting. Baseline data are necessary and para-military personnel showed that
for the evaluation and adjustment of the 46.9% had the infection. In indigenous people
treatment regimen. Cure rates, egg reduction communities in Davao del Norte, 13.6% of
rates, and reinfection rates are important   the school children were found to be infected. 
 parameters in drug monitoring. Among food handlers, 22.7% in Metro Manila  
and 14.8% in Cebu had hookworm infection.  
Epidemiology 
Factors that contribute to the distribution
About 576 to 740 million people in and transmission of hookworms are: (a)
tropical and subtropical countries are estimated suitability of the environment for eggs or
to be infected with either A. duodenale or N. larvae:damp, sandy or friable soilwith decaying
americanus. Associated anemia causes at least vegetation, and temperature of 24 to 32°C,
32°C , (b)
50,000 deaths annually. mode and extent of fecal pollution of the soil
Geographical distribution of the two (through open defecation or the use of night soil
human hookworms used to be relatively as fertilizer), and (c) mode and extent of contact
distinct. A. duodenale was prevalent in Europe
duodenale  between infected
infected soil and skin or mouth. 
and Southwestern Asia, while N. americanus Whereas the method of human infection
was prevalent in tropical Africa and the in necatoriasis is purely percutaneous, in
Americas. But now, both species have become  ancylostomiasis, it is both percutaneous and  

w  ibdter loy p
su b  pd  nbudtr eidgitdhdr oem
dici st,r ai b hes atr eo pniocsloanngder
ugahr ocauttiotn tehatrr i onughr atwhevoer 
gaeltarr  bo and
ule cTonhteam
letse.probablylatitnear also
teodccccuwr isthupon
 present. infective larvae through
In the Philippines, local studies on ingestion of raw or insufficiently cooked infected
speciation of human hookworms revealed that meat, although it is not clear whether infection
out of 1,958 samples positive for hookworm in through eating raw meat occurs in humans. A.
cultures, 97% were identified as N. americanus
americanus, duodenale may remain dormant in the
t he intestines
1% as A. duode nale , and 2% were mixed
du odenale or in the muscles, resulting in a prolonged
infections.  incubation period and creating problems in
The local distribution of human hookworm treatment. Transmammary transmission has
infection is greater in agricultural
agricultural areas. Farmers
Farmers also been reported.
are prone to the infection because they work
w ork In the Philippines, the first human case of
in rice fields
fields and
 and vegetable gardens, and they  Ancylostoma
 Ancylostoma ceylanicum was
ceylanicum reported in 1968
are not properly protected from contact  from a 53-year old woman from Ilocos Norte
with infective soil. In agricultural areas of where 23 adult worms were collected. There  
Compostela Valley province, infection rates are also animal hookworms like  Ancylos
 Ancylostoma
toma
have been shown to be more than 50% in the braziliense (cat hookworm) and  Ancylostoma
late 1990s. Recent surveillance in sentinel sites caninum (dog hookworm) that can infect

in the
of Philippinesinfection
hookworm revealed an
at overall
1.1% andprevalence
1.9% humans
known ascausing “creeping
cutaneous eruption,”
larva migrans also  
(CLM)
for preschool children and school children, (Plate 3.11). 
respectively.  Much of the necessary information about
In other high-risk groups, the prevalence hookworm infection and the disease, i.e,
of hookworm infection remains relatively   morbidity and mortality rates, are still lacking 
 

150   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

of vaccines has been initiated by the Human

Hookworm Vaccine Initiative — Sabin
Sabin Vaccine
Institute. In fact, a vaccine against a secretory
antigen of hookworm had undergone a Phase
I clinical trial on human volunteers. There
were also on-going feasibility studies on the
 possibility
 possibil ity of administering
administ ering the vaccine along  
with anthelminthic drugs, Vitamin A, and
micronutrients, as an intervention package for
school children.
References 
Plate 3.11. Cutaneous larva migrans
(Courtesy of Dr. Vicente Y. Belizario, Jr.) Alboni co M, Bickle Q, Ramsan M, MontresorA,
Albonico
Savioli L, Taylor M. Efficacy of mebendazole
and levamisole alone or in combination
in the Philippines. These are grounds for further against intestinal nematode infections after
local studies on the epidemiology of hookworm repeated targeted mebendazole treatment
infection.  in Zanzibar. Bull World Health Organ.
Prevention and Control  2003;81(5):343 – 52.
52.
Belizario VY, Totañes FIG, de Leon WU,
Regular mass drug administration in   Lumampao YF Ciro RNT. Sentinel  

oor r el sualst p cnr aetaisoenianl ctoamong

edar t of athdehelminths hnet p
r or le p legnr caem
arr  ole
ager  children in selected
shcahdsoil-transmitted
of  pd  pvschool shuelm lltahnicaesisoif n  pspor iels-ctr haonoslm
veinll -aigteteadnd school-
local government
children in a number of areas in the Philippines; units in the Philippines: follow-up
however, coverage of deworming is limited to assessment. Asia Pac J Public Health.  
 preschool-- and school-age
 preschool sch ool-age children ch ildren,, leaving Forthcoming 2013.
other high-risk groups vulnerable.  Belizario VY, Totañes FIG, de Leon WU,
In the Philippines,the
P hilippines,the WASHED
WASHED approach Lumampao
Luma mpao YF,
YF,Ciro
Cir o RNT.
RNT. Soil-transmitted
Soil-transmit ted
is being advocated for a more comprehensive helminth and other intestinal parasitic
control of STH infections. This approach refers infections among school children in
to improvement in access to clean water and indigenous people communities in Davao
sanitation, promotion of hygiene education, del Norte, Philippines.
Philipp ines. ActaTrop.
ActaTrop.2011;120
and regular deworming. Highlighting behavior Suppl 1:S12 – 88..
change among the people and promotion of Belizario VY, Totañes FIG, de Leon WU,
sustainable sanitation through community-led   Naig JR. Baseline Prevalence Survey of
total sanitation may result in greater impact on soil-transmitted helminth infections in
helminth control. Open defecation should be  adolescent females and pregnant women
discouraged and sanitary disposal of human in selected local government units in the
feces, as well as wearing of shoes, slippers, and
 boots should be advised.  Philippines. Final report
of Health-National 2011.for
Center Department
Disease
Because of the reported high rates of post- Prevention and Control. 2011. 
treatment reinfection, diminished efficacy of Belizario VY, Velasco
Velasco JM, de Leon WU, Esparar
 benizimidazole
 benizimid azole drugs,
dr ugs, and concerns for drug
dru g DG, Bugayong PG. Hookworm in the
resistance in many countries, development  military: a parasitologic survey of military  
 

CHAPTER 3: Nematode Infections   151 

and para-military personnel in a Philippine faecal specimens. Acta Trop. 2011;20:206 –  

Military Camp in Northern Luzon. Phil J 10.
Intern Med. 2005;43:169 – 74.
74. Knopp S, Rinaldi L, Khamis S, Stothard JR,
Blaxter M. Genes and genomes of  Necator Rollinson D, Maurelli MP, et al. A single
americanus and related hookworms. Int J FLOTAC is more sensitive than triplicate
Parasitol. 2000;30:347 – 55.
55. Kato-Katz for the diagnosis of low-intensity
low-intensity
Bungiro RD, Cappello M. Detection of   soil-transmitted helminth infections. Trans  
excretory/secretory coproantigens in R Soc Trop Med Hyg. 2009;103:347 – 54. 54.
experimental hookworm infection. Am J Knopps S, Glkinz D, Rinaldi L, Mohammed KA,
Trop Med Hyg. 2005;73(5):915 – 2
20.0.   N’Goran,  EK, Stothard JR, et al.FLOTAC:
Cabrera BD. Species determination of human A promising technique for detecting
hookworm using the polyethylene-tube helminth eggs in human faeces. Trans R
culture technique in selected areas in the Soc Trop Med Hyg. 2009;103:1190 – 4 4.. 
Philippines. Acta Med Philipp. 1981;12(1).  Loukas A, Prociv P. Immune Responses in
Flohr C, Tuyen LN, Lewis S, Minh TT, Hookworm Infections. ClinMicrobiol Rev.
Campbell J, Britton J, et al. Low efficacy 2001;14(4):689 – 703.
703. 
of mebendazole against hookworm in Loukas A. Bethony J. Brooker S. Hotez P.
Vietnam: two randomized controlled trials.
t rials. Hookworm vaccines: past, present, and
Am J Tr
Trop
op Med Hyg. 2007;76(4):732 – 6.
6 .  future. Lancet Infect Dis. 2006;6:733 – 441.
1.  
Gasser RB, Cantacessi C, Loukas A. DNA Mitreva M, McCarter JP, Arasu P, Hawdon J,
technological progress toward advanced   Martin J, Dante M, et al. Investigating

hioaogknwosotr im
d on45.
c  tco – lstr tol. sBu p  pteocr ht nhoul m
io p Aadnv. noaolkyw
sisor om
aGenomics.
h geon Aom
f   tw
ge esl o b
nc y  s
s  peacr iaetsi.v B
t yomcaom e  M 
M C
2008;26:35 45. 2005;6:58.
Gazzinelli MF, Lobato L, Matoso L, Avila R, Soukhathammavong PA, Sayasone S, Phongluxa
Marques RdC, Brown S, et al. Health K, Xayaseng
Xayasen g V, Utzinger J, Vounatsou P,
P, et
education through analogies: preparation al. Low efficacy of single-dose albendazole
a lbendazole
of a community for clinical trials of a and mebendazole against hookworm and
vaccine against hookworm in an endemic effect on concomitant helminth infection
area of Brazil. PLoS Negl Trop Dis.   in Lao PDR. PLoS Negl Trop Dis. 2012;
2010;4(7):e749. 6(1):e1417. 
Hotez PJ, Bethony J, Bottazzi ME, Brooker S, Utzinger J, Rinaldi L, Lohourignonc LK,
Diemert D, Loukas A.New technologies for Rohnerd F,ZimmermannMD,
Zimmerma nnMD, Tschannene,
Tschannene,
the control of human hookworm infection. et al. FLOTAC: a new sensitive technique
Trends
Trends Parasitol. 2006; 22(7):327 – 31.
31.  for the diagnosis of hookworm infections
in fections
Hotez PJ, Brown AS. Neglected tropical disease in humans. Trans R Soc Trop Med Hyg.  
vaccines. Biologicals. 2009;37:160 – 4.
4.  2008;102:84 – 90.
90.
Hotez PJ, Ferris MT.The antipoverty
antipovert y vaccines.   Velasquez CC,
C C, Cabrera BD.  Anc ylo sto ma
Vaccine. 2006;24:5787 – 99.
99.  ceylanicum in a Filipino woman. J Parasitol.

InêsSantos
Ed, Souza JN, Santos
FL, Silva ML, etRC,
al. Souza ES,of
Efficacy 1968;54:430
World  – 43.
43.
Health Organization. Bench aids for the
 parasitolo gical methods
 parasitological meth ods for the
th e diagnosis
diagnosi s diagnosis of intestinal parasites. Geneva:
Geneva:
of Strongyloides stercoralisand hookworm in  World Health Organization; 1994.  
 

152   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Strongy o
ld
i esstercoras
i 
i l 
Vicente Y. Belizario, Jr., Percy G. Balderia

his group of nematodes is characterized than the parasitic female. It has a muscular
 by free-living
free-li ving rhabditif
rh abditiform
orm and parasitic
parasit ic  double-bulbed esophagus, and the intestine is 
filariform stages. Strongyloides stercoralis or a straight cylindrical tube. The free-living male,
T 
threadworm is the only species of this genus
which is naturally pathogenic to humans.  
measuring 0.7 mm by 0.04 mm, is smaller
than the female, and has a ventrally curved tail,
Several species have been reported in mammals two copulatory spicules, a gubernaculum, but  
and in birds.  no caudal alae. Parasitic males have not been
reliably identified. 
Parasite Biology 
The rhabditiform larva measures 225 µm
The parasitic or filariform female is 2.2 mm  by 16 µm. It has an elongated
elongate d esophagus with
 by 0.04 mm, colorless,
colorless , semi-transparent,
semi-tran sparent, with a a pyriform posterior bulb. This species differs
finely striated cuticle. It has a slender tapering from the hookworm in being slightly smaller
anterior end and a short conical pointed tail. and less attenuated posteriorly. It also has a
The short buccal cavity has four indistinct shorter buccal capsule and a larger genital
lips. The long slender esophagus extends to the  primordium.  
anterior fourth of the body, and the intestine is   The infective filariform larva is non-  

cisolnotciantuedouosnteo-tthhier r dsut bhetelr em
nginthaloaf ntuhse. b
 bTohdeyvf rr u olvma f Iet eids insigm,  isllaer ntdoer t,haenhdoa b
 but is usually smaller, with  obkowuotar distinct
5m50filµam
distinc oinr mlenatlagthe
r tif cleft r tvha.
the posterior end. The uteri contain a single file
of 8 to 12 thin-shelled, transparent, segmented tip of the tail.  
ova, 50 to 58 µm by 30 to 34 µm. Eggs have a clear thin shell and are similar
The free-living female (Plate 3.12) to those of hookworms except that they measure
measures 1 mm by 0.06 mm and is smaller   only about 50 to 58 µm by 30 to 34 µm. 
Free-living forms
forms of Strongyloides are found
in the soil. The female worm lays embryonated
eggs, which develop into rhabditiform larvae
after a few hours. These larvae feed on
organic matter and transform into free-living
adults. When conditions in the soil become
unfavorable, rhabditiform larvae develop into
filariform larvae, which are infective tohumans.  
The parasitic life cycle begins when
filariform larvae infect humans through the
filariform larvae
skin. The parasites enter the circulation, pass
through thearelungs,
where they and migrate
subsequently to the Larvae
swallowed. larynx
develop into adults in about a month while in
Plate 3.12. Srt ongy loides stercoralis
srhabditiform
rhabditiform larva
the duodenum. Females generally reproduce
(Courtesy of the
the Department of Parasitology, UP-
 by parthenogenesis.
partheno genesis. They invade the intestinal
intesti nal 
CPH) mucosa where they deposit their eggs. Eggs  
 

CHAPTER 3: Nematode Infections   153 

Figure 3.7. Life cycle of Strongyo

 ld
i esstercoras
i 
i l 
 

hatch into rhabditiform larvae, migrate into the intestinal mucosa by adult females may occur
lumen, and pass out in the feces. simultaneously,
simultaneou sly, particularly in hyperinfection.
hyperinfection. 
Autoinfection occurs when rhabditiform In the first phase of acute infection,
larvae pass down the large intestine and develop larval invasion of the skin produces erythema,
into filariform larvae. Being the infective stage, and pruritic elevated hemorrhagic papules.
these filariform larvae may invade the mucosa During the larval migration phase, the lungs
and enter the circulation to start another   are destroyed causing
causing lobar pneumonia with 
 parasitic cycle without leaving the body of the
host (Figure 3.7).  
hemorrhage. Cough andbronchitis.
also occur, mimicking tracheal irritation may 
In the third
 phase, adult
adult female worms may be found in
Pathogenesis and Clinical Manifestations 
the intestinal mucosa from the pylorus to the
There are three phases of acute infection rectum, but the greatest numbers are found in
in strongyloidiasis: (a) invasion of the skin by the duodenal and upper jejunal regions.
filariform larvae, (b) migration of larvae through Light infection does not cause intestinal
the body, and (c) penetration of the intestinal symptoms. Moderate infection causes diarrhea
mucosa by adult female worms. The migration alternating with constipation. Heavy infection
of larvae through the body and penetration of    produces intractable, painless, intermittent 
 

154   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

diarrhea (Cochin China diarrhea)

di arrhea) characterized The culture technique is practical, low-
 by numerous episodes of watery and bloody cost, and suited for mass screening as well as
stools. Hyperinfection is a syndrome of individual diagnosis. The modified
modified Harada-
 Harada-
accelerated autoinfection which usually, but not Mori culture method makes use of polyethylene
invariably, occurs inthe immunocompromised.  plastic bags or tubes instead of
of glass tubes. 
It manifests with exacerbation of gastrointestinal
gastrointestinal Plastic bags and tubes are unbreakable, lighter
and pulmonary symptoms and increased  to transport, and do not occupy much space. 
numbers of larvae in the stool and/or sputum.   These are therefore recommended for use in the
Chronic strongyloidiasis is often   field. On
field.  On the other hand, the main
m ain advantage
asymptomatic . Howeve
asymptomatic. However,r, intermittentvomiting,
intermittentvomiti ng, of serologic testing is the rapidity and ease of  
diarrhea, constipation, and borborygmi may  performance of the procedure.  
 be observed. Anal pruritus, urticaria, and larva Treatment 
currens rashes are also common. Recurrent
asthma and nephritic syndrome have also been All infected individuals should be treated.
reported in cases of chronic infection with S. Treatment was previously based on albendazole
 stercoralis. or thiabendazole. However,
However, recent studies show
Complicationsinclude edema,emaciation, that ivermectin also provides the best results in
loss of appetite, anemia, lobar pneumonia, ileus, chronic uncomplicated strongyloidiasis with
intestinal obstruction, gastrointestinal bleeding, regard to efficacy and tolerability. Higher doses
and malabsorption leading to cachexia.   given for longer periods may be necessary.
Prognosis is good in light infections,   Strongyloides stercoralis is quite sensitive to the  

 bmutr tm
aloitdye rby
ofotissues
nud htoavtyheinm
atesad
adultse eand
f eacstsiiovnes inhvaavseiohnigh
larvae. Disseminated  cbidenald azctoiloen, sanof d thiveer dmr uegctsi.n
 biceindadlazaonlde, latr hviia b
oAvl b
have been used to treat hyperinfection or
infection occurs among patients with cancer, disseminated disease singly or in combination,
malnutrition, HIV/AIDS, HTLV-1, or those  but data are limited to case reports or case series.  
using immunosuppressive drugs after organ Albendazole and thiabendazole are
transplantation.  contraindicated in pregnant women and in
those with known hypersensitivity to the
Diagnosis 
drugs. Thiabendazole
Thiabendazole may give rise to dizziness,
The finding
finding of
 of unexplained eosinophilia gastrointestinall irritation, drowsiness, pruritus,
gastrointestina
in a patient may be a clue pointing to and headache lasting for several hours. Adverse
strongyloidiasis. The application of repeated reactions with albendazole are transient
concentration techniques, like the Baermann gastrointestinal discomfort and headache.  
funnel gauze method, usually leads to detection Egg reduction rate cannot be determined
of the infection. Harada-Mori culture is  because eggs are not passed out in the feces
considered one of the most successful methods  but are oviposited in the intestine and other
in parasite identification. At present, using the tissues of the host. Reinfection rate is difficult
nutrient agar plates is also recommended. Other to calculate because of autoinfection.

laboratory methods that

string test, duodenal can be done
aspiration, are Beale’s
and small bowel Epidemiology 

 biopsy. In disseminated
dissemin ated strongyloidi
strong yloidiasis,
asis, larvae Strongyloides stercoralisis found throughout
may be found in sputum or urine. Serology may the world and follows a distribution pattern
not be useful in filariasis
filariasis endemic
 endemic areas since similar to hookworm in the tropics and
there are cross-reactions between Strongyloides subtropics, as well as in Europe and the USA.
worm  antigens. 
and filarial worm antigens. Some 50 to 100 million people are estimated 
 

CHAPTER 3: Nematode Infections   155 

to be infected with this parasite. Strongyloides

Strongyloides   and mortality. People with cancer, debilitating
is a soil-transmitted helminth.   diseases like pulmonary tuberculosis, and
In the Philippines, strongyloidiasis is malnutrition, and those about to undergo
relatively rare. Local data on the prevalence of organ transplantation should be cleared of
Strongyloides stercoralis reveal that out of 4,208 Strongyloides infection. This important step is
stools examined using Harada-Mori culture, taken to prevent the occurrence of disseminated
only 50 samples or 1.2% were found positive  strongyloidiasis, which is almost always fatal 
for the worm. If all studies on prevalence were  because larvae invade vital organs. 
included, out of 294,176 stools examined, only References 
148 or 0.05% were found positive. Prevalence 
rates have been described to fluctuate between Bon B, Houze S, Talaba
Talabani
ni H, Magne D, Belkadi
Belkad i
0 to 2.3%, depending on the area selected. This G, develoux M, et al. Evaluation of a rapid
infection is more frequent in male children 7 to enzyme-linked immunosorbent assay 
14 years old, than among females and adults.  for diagnosis of strongyloidiasis. J Clin
Infection and disease rates as well as Microbiol. 2010;48(5):1716 – 9
9.. 
morbidity and mortality figures are not Cabrera BD. Prevalence of Strongyloides
well documented. The factors that affect ralis infection in selected areas in the
 stercoralis
 sterco
transmission include poor sanitation and Philippines using a modified Harada-Mori
indiscriminate disposal of human feces that  culture technique. Acta Med
M ed Philipp.
Philipp. 
may contain Strongyloides larvae. Autoinfection
Autoinfection 1981;17(3):19 – 26.
26.
explains how some people remain infected   Gann PH, Neva FA, Gam AA. A randomized  
 
f eonr demoir  ypehar esnoevmeen aof ntehr alse baveiengsethene
rc eatr hean.  T3h0is  p asluos f thsiina bgleen-daanzdoletwf or -dtor eseatimver nmt ectin
tvr eir 
in American veterans who returned from the of strongyloidiasis. J Infect Dis.  
Korean and Vietnam wars.   1994;169(5):1076 – 9 9..
Prevention and Control 
Igual-Adell R, Oltra-Alcaraz C, Soler-Company
Soler-Company
E , Sánchez-Sánchez P, Matogo-Oyana J,
Prevention and control measures for this Rodríguez-CalabuigD. Efficacy and safety
disease are similar to those for hookworm of ivermectin and thiabendazole in the
infection. Both worms use the soil for further treatment of strongyloidiasis. Expert Opin
development and maintain their endemicity in Pharmacother. 2004;5(12):2615 – 9
9..
areas where environmental sanitation is poor and Keiser P, Nutman T. Strongyloides stercoralis
human feces is deposited indiscriminately in the in the immunocompromised population.
soil by infected people. Infection is acquired by Clin Microbiol Rev.2004;17(1):208 – 117.
7. 
individuals who usually walk barefoot. There is Segarra-Newnham M. Manifestations,
a need to provide health education on personal, diagnosis, and treatment of Strongyloides
family and community hygiene to change ralis infection. Ann
 stercoralis
 sterco Pharmacother.
 behavior and practices. Infected individuals 2007;41(12):1992 – 2001.
2001.
should be treated in order to prevent morbidity 
 

156   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Enterob iusverm c
iua
l rs
i 
i 
Vicente Y. Belizario, Jr., Percy G. Balderia

nterobius vermicularis or human pinworm  posterior esophageal bulb. The small adult
causes enterobiasis or oxyuriasis. The   female worm measures 8 to 13 mm by 0.4 mm  
infection is typically characterized by perianal and has a long pointed tail. The uteri of gravid
g ravid
itching or pruritus ani. Although not a usual females are distended with eggs. The male,
cause of significant
significant morbidity
 morbidity or mortality,   measuring 2 to 5 mm by 0.1 to 0.2 mm has a  
migrating worms may go beyond the perianal curved tailand a single spicule. Males are rarely
region and can occasionally cause complications
complications seen because they usually die after copulation. 
in ectopic areas.   The rhabditiform larva, measuring 140
This intestinal nematode is classified
classified  as to 150 µm by 10 µm, has the characteristic
meromyarian, based on the arrangement of the esophageal bulb, but has no cuticular expansion
somatic muscles where there are two to five cells on the anterior end.
 per dorsal or ventral half.  Eggs (Plate 3.14) are asymmetrical, with
The human pinworm is the most common one side flattened
flattened and
 and the other side convex,
helminth parasite identified in temperate and range from 50 to 60 µm by 20 to 30 µm
regions, where environmental sanitation is in size averaging 55 by 36 µm. The translucent
in place. Less attention is given to pinworm   shell consists of an outer triple albuminous  

inr f f escetniocceen oinf f  ottr rho  per i,caml oare acsl,inl ikcealyllyydsuigentifioctahnet

 p  beryinognf ifc or l p
ceomv b poeicdhalnm
 im  p br or 
icaelm
 protection. Inside the egg is a tadpole like
r atneeccetif f onr  acnhdemanicianl ner
 parasites. 
embryo that becomes fully mature outside the
Parasite Biology 
host within 4 to 6 hours.  
Adult worms have cuticular alar expansions Adult worms are found in the cecum
(Plate 3.13)
3.1 3) at the anterior end
en d and a pr
promi
ominen
nentt  and adjacent portions of the small and large  

Plate  3.13.  E  obi us c e phalic alae

er 
nt  Plate 3.14. D-shaped eggs of Enterobius
(Courtesy of the Department of Parasitology
Parasitology,, vermicularis(Courtesy of the Department of
vermicularis(Courtesy
UP-CPH)  Parasitology, UP-CPH)
 

CHAPTER 3: Nematode Infections   157 

intestines. Gravid female worms migrate down usually dies. Eggs on the
th e perianal region become
the intestinal tract and exit through the anus to fully embryonated within 6 hours. When
deposit eggs on the perianal skin. Adult female ingested, eggs containing the 3rd stage larvae
worms migrate to the perianal area, usually in hatch in the duodenum, pass down the small
the evening hours. A single female lays from intestines to the cecum, and develop into adults
4,672 to 16,888 eggs per day with an average (Figure 3.8). Eggs are resistant to disinfectants
d isinfectants
of 11,105 eggs. After egg deposition, the female   but succumb to dehydration in dry air within 
 

158   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

a day.
day. However,
However, in moist conditions,
condit ions, these eggs
eg gs relieved only by vigorous scratching. Diagnosis
can remain viable for up to 13 days. The eggs is confirmed by finding adult worms or eggs on
remain viable longest under conditions of fairly microscopic examinations. Adult worms may
high humidity and moderate temperature. The  be seen in the feces or in the perianal region.
eggs may survive for some days in dry dust, and Eggs are found in the feces in only about 5%
airborne eggs can infect persons at a distance of infected persons. The method of laboratory
via inhalation. diagnosis is the Graham’s scotch adhesive tape 
Pathogenesis and Clinical Manifestations  
swab (perianal cellulose tape swab), which gives
the highest percentage of positive results, and
 Enterobius vermicularis is a relatively the greatest number of eggs seen. This low-cost 
innocuous parasite and rarely produces any diagnostic method is easy to perform and is very
serious lesions. Mild catarrhal inflammation sensitive and specific. 
of the intestinal mucosa may result from
Treatment 
the attachment of the worms. Mechanical
irritation and secondary bacterial invasion The drugs of choice are mebendazole 100
may lead to inflammation of the deeper layers mg PO single dose or albendazole 400 mg PO
of the intestines. Invasion of the appendix is single dose. Pyrantel pamoate 11 mg/kg base
not unusual, but whether this invasion is a PO single dose (max. of 1 g) is considered a
significant cause of appendicitis is not known. secondary drug of choice.  E. vermicularis
vermicul aris is
Migration of egg-laying females to the anus quite susceptible to these drugs, with reported
causes irritation of the perineal region. Intense   cure rates of over 90%. Moreover, since family  

sitecchoinndgalr eya b
das cttoer 
sia d hmiladyr egnivienr 
ciar laitncf heicntgio, nan. C f eiscetetod tmheme bnetirr r s e ahr eouusseuhaolldy  ins f r  ede.nC
re ecctoedm, mtr eenadtm t  uof r e
with this parasite may suffer from insomnia due can only be considered after seven perianal
to the pruritus. Other signs of infection are smears, on consecutive days using scotch-tape
 poor appetite,
appetit e, weight loss, irritability,
irritabi lity, grinding
grindin g swab method, are all found to be negative.
of teeth, and abdominal pain.  The egg reduction rate is difficult to determine
Complications such as appendicitis,  because eggs are collected from theth e perianal
vaginitis, endometritis, salpingitis, and area instead of from the feces using Kato-Katz.
 peritonitis are all due to aberrant adult worm Mebendazole, albendazole, and pyrantel are
migration. Entry into the peritoneal cavity via contraindicated in individuals with known
the female reproductive system may result in the hypersensitivity. Adverse effects of these
formation of granuloma around eggs or worms. drugs include mild, transient gastrointestinal
gastrointestinal
Pinworms or their eggs have occasionally been disturbance, and headache. 
reported from other ectopic sites such as the
Epidemiology 
liver and lung. 
The prognosis of enterobiasis or oxyuriasis Enterobiasis occurs in both temperate and
is good. This parasitic disease is extremely tropical regions of the world, and has a high
contagious and can easily spread among  prevalence in both developed
develo ped and developing
members
it has beenofdescribed
a family orasin
i nainstitutions.
familial or aHence,
group
countries. It is the only intestinal nematode
infection that cannot be controlled through
disease.  sanitary disposal of human feces, because
Diagnosis 
the eggs are deposited in the perianal region
instead of the intestinal lumen. Eggs usually
Enterobiasis should be suspected in contaminate underwear and beddings. The
children and adults who show perianal itching   route of infection is through the mouth, the  
 

CHAPTER 3: Nematode Infections   159 

respiratory system (by inhalation of dust opportunities for health education of teachers
containing Enterobius eggs), and through the and school children regarding measures on
anus (wherein the hatched larvae enter the anus control and prevention of intestinal helminth
and cause retroinfection when they go back into infections, including pinworm infections.  
the large intestine). Risk factors for infection
include overcrowding, thumb-sucking, nail- References 
 biting, and lack of parental knowledge on  Cabrera BD, Garcia EG, Cruz TA, Salazar NP,  
 pinworms.   Jueco NL. Studies on enterobiasis in the
There are around 208.8 million infected   Philippines. I: Frequency of enterobiasis
 persons in the world, with 18 million in among schoolchildren in the city of Manila.
Canada and the United States of America. J Philipp Med Assoc. 1961;37(12):1032 –  
Prevalence is 12 to 41% in Washington, D.C. 45.
In the Philippines, prevalence levels have been Cabrera BD, Garcia EG, Cruz TA, Salazar
found to be 29% among schoolchildren from  NP, Jueco NL. Studies on enterobiasis
exclusive private schools, and 56% among in the Philippines. II: The occurrence
those from public
publi c schools. Localy,prevalence is of  Enterobius ova in the fingertips and
consistently higher in females (16%) compared fingernails of infected schoolchildren.  J 
to males (9%). Eggs were found in nail
n ail clippings Philipp Med Assoc. 1961;37(12):1032 – 445.
5.
of school children.   Crompton DW, Montresor A, Neishem MC,  
Local data on infection and disease rates, Savioli L. Controlling disease due to
as well as morbidity and mortality figures are   helminth infections.Genev
infecti ons.Geneva:
a: World
WorldHealth  

inadequate.
Prevention and Control  ovrr i gcanAiz, aTtiao p
D jakO  pn p . ietl J. Diagnosis of
 p;e20D0,3D
and anthelminthic therapy for  Enter
 Enterobius
obius
Personal cleanliness and personal hygiene vermicularis infections during pregnancy:
are essential. Fingernails should be cut short review of the literature and case report. Z
and hand washing should be done after using Geburtshilfe Neonatol. 2006;210(4):147 –  
the toilet, as well as before and after meals. 52.
The use of showers rather than bathtubs is Jong EC, Sanford C, editors. The travel and
suggested, and infected persons should sleep tropical medicine manual. Philadelphia:
alone until adequately treated. Underwear, Saunders Elsevier; 2008. 
night clothes, blankets, and bed sheets should Kim DH, Son H, Kim JY, Cho MK, Park
 be handled with care and washed in hot soapy MK, Kang SY. Parents’ knowledge about
water. Vacuum cleaning around beds and enterobiasis might be one of the most
contaminated areas will be useful. Being a important risk factors for enterobiasis  
familial disease, chemotherapy of the entire in children. Korean J Parasitol.
family is recommended, and will help in the 2010;48(2):121 – 66.. 
control of the disease. Markell EK, John DT, Krotoski WA. Medical  
The implementation of mass drug Parasitology. 8th ed. Philadelphia: W. B.
administration targeting soil-transmitted Saunders Company; 1999.  
helminthiases is expected to have an impact St. Georgiev V. Chemotherapy of enterobiasis
on the prevalence of enterobiasis as well. (oxyuriasis). Expert Opin Pharmacother.
Pharmacother.
Control efforts in elementary schools provide   2001;2(2):267 – 75.
75.
 

160   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Sung JC, Lin RS, Huang KC, Wang SY, Lu http://www.dpd.cdc.gov/dpdx/HTML/

YJ. Pinworm control and risk factors of PDF_Files/MedLetter/Enterobius_
 pinworm infection among primary-school
primary-scho ol vermicularisInfection.pdf.
children in Taiwan. Am J Trop Med Hyg. World Health Organization. First WHO
2001;65(5):558 – 62.
62. report on neglected tropical diseases 2010:
The Medical Letter. The medical letter
l etter report working to overcome the global impact
i mpact of
for drugs for parasitic infections [Internet]. neglected tropical diseases. Geneva: World 
2010 [cited 2012 Mar 3]. Available from   Health Organization; 2010.
 

CHAPTER 3: Nematode Infections   161 

Cap ia
l 
l ra
i ph
 p
 i 
l 
li pn
i enss
 i
Vicente Y. Belizario, Jr., Francis Isidore G. Totañes

apillaria philippine nsis is one of four

philippinensis intestinal malabsorption. Severe disease can
Capillaria species that are known to result in death. Fish-eating birds are the natural
n atural
infect humans. Human infection with C. hosts of the nematode.  
 philippinen
 philip sis was first reported by Chitwood et
pinensis
Parasite Biology 
al. in 1963 in a 29 year old male from Northern  
Luzon. Intestinal capillariasis, a zoonotic Capillaria philippinensis is a nematode
disease, is characterized by abdominal pain, from the superfamily Trichinelloidea, to which
chronic diarrhea, and gurgling stomach. The Trichuris and Trichinella belong. The
Th e parasites
disease may also be associated with protein- in this superfamily characteristically have a thin
losing enteropathy, electrolyte imbalance, and  filamentous anterior end and a slightly thicker
and shorter posterior end. The male worms
(Plate 3.15) are about 1.5 to 3.9 mm in length,
while females (Plate 3.16) are 2.3 to 5.3 mm
long. The male spicule is 230 to 300 µm long
and has an unspined sheath. The esophagus
has rows of secretory cells called stichocytes,  

enet.ir Teheesoa p
satnicdhtohseom  pnhuasgiesalsus btr tuecr 
r m rne  ails,  acnaldledthae
tuir 
vulva in females is located at the junction of
anterior and middle thirds. 
Female worms produce characteristic
eggs, which are peanut-shaped with striated
shells and flattened  bipolar plugs (Plate 3.17).
Plate 3.15. Male Cap ia
ll  ra
i ph
 p
 ill 
i  pi 
nenss
 i These eggs, which measure 36 to 45 µm by 20  
(Courtesy of Dr. John Cross)
µm, are passed in the feces and embryonate in  

Plate 3.17. Cap liara

i ph ip i ens isegg
ll  pn
Plate 3.16. Female Capillariaphilippinensis   (Courtesy of the Department of Parasittology, ology,
(Courtesy of Dr. John Cross) UP-CPH) 
 

162   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

the soil or water. They must reach the water The eggs hatch in the intestines of the fish
fish  and
in order to be ingested by small species of grow into the infective larvae. When the fish
freshwater or brackish water fish (Figure 3.9).  is eaten uncooked, the larvae escape from the 
 

CHAPTER 3: Nematode Infections   163 

fish intestines and develop into adult worms in Endoscopic finding may reveal non -specific
human intestines. segmental erythematous inflammation in the
The first generation of female worms small bowel with superficial erosions with
 produces larvae to build up the population. exudation. 
Subsequent generations predominantly produce Histologically, the intestines also show
eggs, although there are always a few female flattened and denuded villi, and dilated mucosal
worms that produce both larvae and eggs, or   glands. The lamina propria is infiltrated
infiltrated with
 with 
larvae only. Some of these larvae are retained  plasma cells,
cells , lymphocytes,
lympho cytes, macrophages,
macro phages, and
in the gut lumen and develop into adults. This neutrophils. 
leads to hyperinfection and autoinfection,  
Diagnosis 
which result in the production of very large
numbers of worms.
wor ms. In one autopsy, as many as Diagnosis is based on findingc  haracteristic
200,000 worms were recovered from one liter eggs in the feces by direct smear or wet mount,
mo unt,
of bowel fluid.  as well as by stool concentration methods. There
Fish-eating birds are believed to be the may also be various larval stages of the parasites,
natural hosts of C. philippinensis, and humans as well as adult worms in the feces. The uterus
are considered incidental hosts. of the female worms may contain developing
eggs and sometimes larvae (Plate 3.18). The
Pathogenesis and Clinical Manifestations  
 parasites can also be recovered from the small
Persons with C. philippinensis usually have intestines by duodenal aspiration. 
abdominal pain and borborygmi. Patients 

inr iotia
 p giar lelyss ieanscseinigntoeur m
ssesx ptoer  p 10diavr or lhuema,inwohuisch
tttteont10
t  8itt
stools per day. After a few weeks, there is
noticeable weight loss, malaise, anorexia,
vomiting, and edema. Laboratory findings
show severe protein-losing enteropathy and
hypoalbuminemia; malabsorption of fats and
sugars; decreased excretion of xylose; low serum
 potassium,
 potassiu m, sodium and calcium; and high levels
of immunoglobulin E. If the disease is not
treated soon after the symptoms occur, severe Plate 3.18. Capilariaphilppinensissecond sta
stage
ge larva
from the feces of a person with intestinal
manifestations of the disease develop with a capillariasis (Courtesy of Dr. John Cross)  
 potentially fatal outcome.  
The large number of worms that A study done in Egypt demonstrated
develop in humans is responsible for the high specificity
specificity of
 of sandwich enzyme-linked
severe pathology. The parasites do not invade immunosorbent assay (ELISA) in the detection
intestinal tissue, but they are responsible   of coproantigen prepared from stool samples of
for micro-ulcers in the epithelium, and the  patients with capillariasis.
capil lariasis. This
T his technique
techni que did
compressive degeneration and mechanical not showwith
cross-reaction withica
coproantigen from
compression of cells. Homogeneous material is  patients  Fasciola
 Fascio la gigant
gigantica and Schistosoma
seen at the anterior end of the worm by electron mansoni. Another study demonstrated cross-
microscopy. The ulcerative and degenerative reaction of capillariasis patient antibodies with
lesions in the intestinal mucosa may account for Trichinella spiralis antigen in immunoblot
malabsorption of fluid, protein, and electrolytes.  assay, suggesting the prospective use of T.
 

164   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 spiralis antigen for the immunodiagnosis of towns and resulted in more than 1,000 cases
capillariasis.. ELISA using T. spiralis antigen
capillariasis and 77 deaths.
death s. Cases of human
h uman capillariass
capillariassii have
has been tested and shown to have a sensitivity  been subsequently
subse quently reported
r eported in
i n Thailand,
Thailan d, Iran,
of 100% in the diagnosis of capillariasis (43
( 43 Japan, Indonesia, United Arab Emirates, South
 positive cases) and a specificity
specificity of
 of 100% (57 Korea, India, Taiwan, Egypt, and Lao People’s
negative cases).  Democratic Republic. A review of data from
local hospitals throughout Taiwan from 1983  
Treatment  to 2003 revealed a total of 30 capillariasis cases,
In severe cases with electrolyte and protein 21 of whom were from two major Taiwanese
loss, patients should be given electrolyte absrcinal tribes. 
replacement and a high protein diet (Plate In the Philippines, nearly 2,000 cases have
3.19). Anthelminthic drugs should also be  been documented from the Northern Luzon
given. The drug of choice for the
th e treatment  provinces
 provin ces from 1967 to 1990. Cases have also
of intestinal capillariasis is mebendazole, 200  been documented in Zambales and and Southern
mg twice a day for 20 days. Alternatively, Leyte. Infections are acquired by eating
albendazole 400 mg may be given once daily uncooked small freshwater/brackish water
for 10 days. Relapses may occur if the treatment fish. Ilocano people enjoy eating bagsit and
regimen is not followed and completed.   other fishes found in the lagoons. In Monkayo,
Compostela Valley Province, an outbreak
described as a “mystery disease”  in 1998 resulted
in the death of villagers due to misdiagnosis. 

oInf  ttehsteincalsecsapr ilelsaer niiaatsiinsgwaisthdicahgr nonsiecddinarr 1h7e%
a.
A more recently described endemic area in the
Philippines involved Zamboanga del Norte,
where more than 70 deaths were recorded and
4.9% of those examined in a parasitologic survey
were confirmed to have capillariasis. A few cases
have also been confirmed  in Zamboanga del
confirmed in
Sur, Agusan del Sur, and Misamis Occidental.
Occident al. 
Prevention and Control 

It is believed that the 1967 to 1968

Philippine epidemic was due to washing of
fecally contaminated bed sheets in lagoons in the
Plate 3.19. 31-year old female with intestinal Tagudin area of Ilocos Sur. Efforts to improve
i mprove
capillariasis before treatment (left) sanitation and health educational programs to
and 1 year after treatment (right)  prevent indiscriminate
indiscri minate disposal of human waste
(Courtesy of Dr. Vicente Belizario, Jr.)
and to discourage eating raw fish  are important
Epidemiology  in controlling the spread of infection (Plate
3.20). Capacity building for health personnel in
Intestinal capillariasis
capillariasis was first recorded in the field, including laboratory staff, for early and
 Northern Luzon in the the Philippines. IIn
n 1966, accurate diagnosis and treatment is important in
an epidemic in Pudoc West, Tagudin, Ilocos  preventing
 preventi ng mortality.
mortali ty. Health education can also
Sur was reported, that spread to neighboring   help improve patient health-seeking behaviors. 
 

CHAPTER 3: Nematode Infections   165 

infectious diseases. New York: Academic

Press; 1983. 103 – 3
36.
6. 
Cross JH, Basaca-Sevilla V. Biomedical
Biomedical surveys
in the Philippines. Manila (Philippines): US
 Naval Medical Research Unit No. 2; 1984.  
Cross JH. Intestinal capillariasis. Clin Microbiol
Rev. 1992;5:120 – 9
9.. 
The Medical Letter. Drugs for Parasitic
Infections [Internet]. 2010 [cited 2012 Mar
3]. Available from 
from www.medicalletter.org.
www.medicalletter.org. 
El Dib NA, Sabry MA, Ahmed JA, El-
Plate 3.20. Proper excreta disposal is i mportant Basiouni SO, El-Badry AA. Evaluation
for prevention and control of intestinal of Capillaria philippinensis coproantigen
helminthiases including capillariasis
(Courtesy of Dr. Vicente Belizario, Jr.)
in the diagnosis of infection. J Egypt Soc
Parasitol. 2004;34:97 – 106.
106.
Intapan PM, Maleewong W, Sukeepaisarnjaroen
References 
W, Morakote
Morakote N. An enzyme-link ed
immunosorbent assay as screening  
Bair MJ, Hwang
Hwan g KP,
KP, Wang
Wang TE Liou
Lio u TC, Lin
Lin SC, tool for human intestinal capillariasis.
Kao CR, et al. Clinical features of human Southeast Asian J Trop
Trop Med Public Health.
Health .
intestinal capillariasis
capillariasis in Taiwan. World J  2010;41(2):298 – 305.
305.

BelizG VoYe,ndter Loel.oJ,2nVerdadero
ar aisotr Fantone 04U;1,  0E( p
0W 1 – , 3G.  alang
s16a)r a:2r 3D9G Inta pW
an, Mor a, kMotaele New. PontgenW
PM tia, lSuskeeoe par isiachr nin
f T  ner 
i ja ll oaen
JM, C. Compostela lis antigen for serodiagnosis of human
 spiralis
 spira
Valley: a new endemic
endemic focus for capillariasis
capillar iasis capillariasis philippinensis by immunoblot
 philippi nensis. Southeast Asian
 philippinensis. Asian J Tr
Trop
opMed analysis. Parasitol Res. 2006;98:227 – 331.
1.  
Public Health. 2
2000;31(3):478
000;31(3):478 – 81.
81.  Lu LH, Lin MR, Choi WM, Hwang KP, Hsu
Belizario VY, Totañ
Totañes
es FI, de Leon WU, Migriño
Migri ño YH, Bair MJ, et al. Human intestinal
JR, Macasaet LY. Intestinal capillariasis, capillariasis ( Capillaria philippinensis )
Western Mindanao, the Philippines. Emerg in Taiwan. Am J Trop Med Hyg.
Infect Dis. 2010;16(4):736 – 8.8 .  2006;74(5):810 – 3 3..
Canlas BC, Cabrera BD, Dauz U. Human Sangchan A, Wongsaensook A, KularbkaewC,
intestinal capillariasis, II. Pathological Sawanyawisuth K, Sukeepaisarnjaroen W,
features. Acta Med Philipp. 1967;4:84 – 91.
91.   Mairiang P. The endoscopic pathologic
Chitwood MB, Velasquez C, Salazar NG. findings in
findings  in intestinal capillariais: a case
Capillaria philippine nsis . (Nematoda:
philippinensis report. J Med Assoc Thai. 2007;90:175 – 88.. 
Trichinellida) from intestine of man in the Singson CM. Recurrences in human intestinal
Philippines. J Parasitol. 1968; 54:368 – 71.
71.  capillariasis.. Phil J Microbiol Infect Dis.
capillariasis
Cross JH, Banzon TC, Singson CM. Further 1974;3:7 – 13.
13. 
on Capillaria philippinensis : Soukhathammavong
studies
development of the parasite in the AN. Case report:P,three
Sayasone
casesS,ofHarimanana
intestinal
Mongolian gerbil. J Parasitol. 1978; capillariasis in Lao People’s Democratic
64:208 – 13.
13. Republic. Am J Trop Med Hyg. 
Cross JH, Bhaibulaya M. Intestinal capillariasis 2008;79(5):735 – 8 8..
in the Philippines and Thailand. In: Whalen GE. Intestinal capillariasis — a new
Croll N, Cross JH. Human ecology and   disease in man. Lancet. 1969;1:13 – 6 6.. 
 

166   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Tissue Nematodes
Vicente Y. Belizario, Jr., Timothy M. Ting

LymphaticFilariasis Parasite Biology 

long,Adanudlt filif or m in wshoar  pmes. aTr ehcer emam e,
aley whoir tm
Wucherer iabancrotfi Brugiamalayi  W ucher er ia

measures 20 to 40 mm in length, while the

T  here are eight known species of filarial
nematodes that use humans as their  
definitive host. These are subdivided into three
female measures 80 to 100 mm. Microfilariae
in fresh specimens appear as minute snake-like
groups based on the anatomic location from
organisms constantly moving among the red
 blood cells. A microfilaria
microfilaria measures
 measures 270 to
which they cause pathology: subcutaneous,
290 µm and is enclosed in a hyaline sheath
s heath
serous cavity,and lymphatic filariasi. Mansonella
 Mansonella
which is much longer than the microfilaria
causes serous cavity filariasis in the abdomen.
Filarial worms that live in the subcutaneous
su bcutaneous
itself (Figure 3.22). When stained, the central
fat under the skin include Loa loa (African eye axis shows dark-staining nuclei, which serve as
worm), Mansonella streptocerca , and Onchocerca an important identifying feature. The column
of nuclei is arranged in two or three rows and
volvulus . Lymphatic filariasis is caused by  
is distinctly conspicuous. Microfilariae have
malayi , and 
Wuchereria bancrofti ,  Brugia malayi several curvatures and a graceful appearance. 
timorii. With adults that become lodged  
 Brugia timor
 Brugia
in the lymphatic system, these worms cause The Brugia male measures 13 to 23 mm
lymphedema, lymphangitis, and in chronic in length while the female measures 43 to
cases, elephantiasis. Disease is transmitted 55 mm. Adult females of  B. malayi and W.
bancrofti are indistinguishable. The  Brugia
 by blood-feeding
blood -feeding arthropod
arthropo d vectors,
vector s, mainly
microfilariae measure 111 to 230 µm in length
mosquitoes and black flies.  
Lymphatic filariasis (LF) is one of the most (Plate 3.21). In stained blood smears, they can 
debilitating diseases plaguing many tropical
countries. Next to psychiatric illness, LF is the
second leading cause of permanent and long-
term disability, affecting both physical and
 psycholo gical aspects of the victim.
 psychological victim . The social
stigma and associated economic consequences
result in a poor quality of life to the afflicted.
The two most common mosquito-borne
causative agents of LF are Wuchereria bancrofti
or Bancroft’s filarial worm, which is the
causative agent of Bancroftian filariasis; and
 Brugia malayi or the Malayan filarial
filarial worm,
 worm,
which causes Malayanfilariasis.
Malayan filariasis. 
Plate 3.21. Brugiamalayi mi
microfilaria
(Courtesy of the Department of Parasitology
Parasitology,,
UP-CPH) 
 

CHAPTER 3: Nematode Infections   167 

 be seen enclosed in a sheath, and having angular damage, and migrate towards the mosquito’s
curvatures with secondary kinks, and two nuclei head and proboscis. During a blood meal, larvae
at the tip of the tail. The column of indistinct emerge from the proboscis onto the skin of the
and confluent nuclei is composed of two rows.   susceptible host and actively penetrate the skin
Adult male and female W.bancrofti
bancrof ti worms through the bite wound to reach the lymphatic
are found tightly coiled in nodular dilated vessels and nodes where they develop into adult
nests (lymphangiectasia) in lymph vessels and   worms. They are usually localized in the lymph  
in sinuses of lymph glands. Adult females vessels of the lower extremities, inguinal lymph
 produce microfilariae, which gain entrance to nodes, epididymis of males, and labia of females.
the peripheral blood circulation where they are   Microfilariae migrate from the parent worm,  
Microfilariae migrate
 picked up by the appropriate
appropr iate mosquito
mosquit o vector through the walls of the lymphatics, and into
during a blood meal (Plate 3.22). Mosquitoes the neighboring blood vessels. 
 belonging to the genera  Aede s, Culex , and The life cycle of B.malayigenerallyfollows
 Anophe les have been shown to be biologic the same pattern as that of W. bancroftiwith a
vectors of Wuchereria. Microfilariae ingested few exceptions (Figure 3.10). Mosquito vectors
 by the mosquito migrate
mig rate to its muscles where of  B. malayi  belong to the genus  Mansonia.
they develop into first (L1), second (L2), and Development of the microfilariae to the
third (L3) stage larvae. After 6 to 20 days infective stage in the mosquito takes about 2
of development, 3rd stage larvae force their
th eir weeks. Maturation time for the 3rd stage larvae
way out of the muscles, causing considerable  to become adults takes about 3 to 9 months.
Thereafter, microfilariae are produced and  may 

 be seen in the and

Pathogenesis circulation.
Clinical  Manifestations  

LF is characterized by a wide spectrum

of clinical manifestations, with signs and
symptoms different from one host to another.
The infection is usually acquired in childhood
 but may take years to manifest
manifest itself. The clinical
course may be divided into asymptomatic,
acute, and chronic stages, generally progressing
in that order. In an endemic community, the
th e
different stages of the disease frequently overlap,
and in certain groups of people from non-
endemic areas, the disease may be characterized
 by an initial acute stage followed directly by a
chronic stage in a relatively short period of time. 
Individuals who grew up outside
o utside regions 
endemic for these filarial parasites and who get
infected by them
regions may after migration
clinically to “Expatriate
present with the endemic
Syndrome.” The syndrome is characterized by
Plate 3.22. Wuchereriabancroftimi
  crofilaria clinical and immunologic
immunologic hyper-responsiveness
hyper-responsiveness
(Courtesy of the Department of Parasitology, to the mature or maturingw
mat uringworms.
orms. Together
Together with
UP-CPH) the usual acute manifestations of lymphadenitis  
 

168   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

and lymphangitis, individuals with this lymphatic endothelial cell proliferation and
syndrome also present with allergic reactions differentiation leading to collateralization.
such as hives, rashes, and blood eosinophilia.   These lymphatic dysfunctions have been shown
Lymphatic localization is important to predispose infected individuals to secondary
in parasite survival because lymph is a less    bacterial infection
i nfectionss and tri
trigger
gger inflammatory
infla mmatory
aggressive medium than blood: no platelets, no reactions in the skin and subcutaneous tissue,
complement system, incomplete coagulation leading to lymphedema and elephantiasis.  
system, and no granulocytes; in addition, its A characteristic feature of chronic LF
flow is much less violent. Filarial adult worms
wor ms infection is fibrosis and cellular hyperplasia
cause parasite-induced lymphatic dilatation in and around the lymphatic walls; these
(lymphangiectasia);); this is a common feature
(lymphangiectasia feature changes are postulated to render lymphatic
of patent infection, though clinically apparent endothelial cells less effective at transporting
lymphedema is rarely seen. Another cardinal interstitial fluid, thereby contributing to the
feature of LF is lymphangiogenesis, where edema and collagen accumulation. Dead
live filarial parasites or filarial antigens induce  and decalcifying adult worms elicit immune  
 

CHAPTER 3: Nematode Infections   169 

responses leading to lymphatic blockage  by several immune

immune regulatory
regulatory processes driven
driven
and gross pathological lesions; it invokes    by living parasites to ensure their long-term
lymphangitis and lymphadenitis with localized survival. Co-infection with other parasites
 pain and swelling. The amount of exposure and infectious disease is common, and the
to secondary bacterial infections and the suppressive immunomodulatory mechanisms
magnitude of host immunity to infective or  by the worm can modulate
modulat e protective
protecti ve immune
developing larvae, or to Wolbachia increase  responses for malaria and tuberculosis. Though 
the risk of development of chronic disease. no clinical manifestations are seen and they
Lymphatic insufficiency leads to increase appear outwardly healthy, these individuals
susceptibility to opportunistic infections, and   may actually have hidden lymphatic pathology 
result in acute dermatolymphangioadenitis and kidney damage. Recent studies in animals
(ADLA) (Plate 3.23). Another potent inducer show direct evidence that infection with Brug
 Brugia
ia
of inflammation is exposure to Wolbachia that can selectively induce CD4+ lymphocyte
is released by dead or dying worms.  apoptosis, which may contribute to immune
unresponsiveness
unresponsiveness to filariasis. The asymptomatic
asymptomatic
stage may also be seen in those individuals who
are called “endemic
“endemic  normals,”
normals,” who
 who harbor in
their blood the parasite antigen instead of the
microfilariae. 
ADLA is the most common acute
manifestation of LF, defined as localized pain,  

lcyem  uplhitaisdeanidtisloacnadl /woar 
ll p r r rm th p, hwainthgitoisr   w
 llyym anitdh/our t
systemic manifestations of fever, nausea, and
vomiting. Clinical descriptions are remarkably
Plate 3.23. Dermatolymphangioadenitis similar to those of erysipelas and cellulitis. The
(acute lymphatic filariasis)  attacks are recurrent, and among patients in
(Courtesy of Dr. Vicente Belizario, Jr.) LF-endemic areas, the mean annual reported
incidence ranges from 1.5 to more than 7
The clinical spectrum of LF includes   episodes per patient. The duration of symptoms,
(a) asymptomatic microfilaremia, (b) acute  based on patient self reporting, ranges from 1
dermatolymphangioadenitis
dermatolymphangioaden itis (ADLA) also to 16 days, which result in significant short
 previously called
called adenolymphangitis
adenolymphangitis (ADL),
(ADL),  term disability, where the number of workdays
(c) acute filarial lymphangitis (AFL), (d) lost may exceed the duration of the ADLA
lymphedema and elephantiasis, (e) genito- episode itself. Studies indicate that the rate
urinary lesions (e.g., hydrocele), and (f) tropical of ADLA is higher in persons with chronic  
 pulmonary eosinophilia (TPE).   disease, particularly lymphedema. Among those
One of the most striking features of LF is  with lymphedema, the risk factors for ADLA
that individuals with thousands to millions of include increasing patient age, poor hygiene,
vigorously
vigorous ly motile microfilariae in the peripheral and illiteracy. Studies from Brazil, India, and  
 blood often show no obvious clinical signs of Guyana show that the presence and number
disease, known as asymptomatic microfilaremia. of interdigital skin lesions are very strong risk
These individuals serve as the main reservoir for factors for attacks of ADLA.  
mosquito vectors which acquire microfilariae Current evidence shows that ADLA is
during a blood meal. This stage is characterized
characterized  of bacterial etiology, based on clinical signs 
 

170   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

and symptoms (erysipelas or cellulitis-like),

and isolation of bacteria at the time of the
acute episode. The bacteria most frequently
associated with ADLA episodes are Group A
Streptococcus, although other bacteria are often
found in cultures, including non-pathogenic
strains. Thus, secondary bacterial infections  
from neglected skin lesions (reduced sensation
 predisposes to trauma, and poor hygiene)
 precipitate attacks of ADLA, and repeated 
ADLA episodes are deemed the most important
factor in lymphedema progression.  
AFL is a rare manifestation
manifestation directly caused
 by adult worms that died spontaneously, or
commonly observed following treatment
with diethylcarbamazine (DEC), the latter is
considered evi
eviden
dence
ce of the drugs’ macrofilaricidal
efficacy.  AFL is characterized by lymphangitis
that progresses distally along the lymphatic Plate 3.24. Elephantiasis
vessel, producing a palpable “cord.” AFL may (Courtesy of Dr. Vicente Belizario, Jr.)
 be accompanied by mild fever, headache, and  

is aulsauisael.ly
m istiladl laynmd pr hevdeerr m
lyDm s  i b r, p
 balem. aTyhoeccsyum   b
ptuotmits acrr ue  stenactetaockf f  s.hTalhloe wmaskininf ef aotludr se, otf hsetsaegaer 3e if sotlhdes
 p
are self-limited or generally subside without where the base can still be seen when the patient
treatment.  moves the leg or foot and the fold“opens
fold “opens  up.”
up.”
The most common chronic manifestation Lines or creases not seen in the normal
n ormal leg are
of LF is lymphedema, which on progression already considered shallow folds. In stage 4,
leads to elephantiasis (Plate 3.24). The lower
low er there are knobs present in the affected area;
limbs are commonly affected, but upper limb these are lumps or protrusions in the skin that
and male genitalia may be involved.
in volved. In females,  predispose the area to trauma. A patient in
 breasts and genitalia
genitali a may be affected, but this is stage 5, has deep skin folds, where the base
relatively uncommon. Repeated ADLA episodes
episodes can no longer be seen when the patient moves
are responsible for lymphedema progression the leg, but only when the folds are actively
and elephantiasis. Literature on lymphedema in “opened” by
“opened”  by hand. In stage 6, mossy lesions
filariasis-endemic areas lack standardization in are present, brought about by the clustering
clus tering
terms of terminology, agreed-upon criteria for   of small elongated or rounded growths. These 
diagnosis, and case definition. Many authors usually leak translucent fluid, putting the area
use the term ‘elephantiasis’ for
fo r all forms of at risk for secondary bacterial infection. In  
lymphedema.   stage 7, the patient is unable to
t o adequately or
Dreyer et al. in 2002 proposed a staging independe
independently
system for chronic lymphedema. In stage 1, due to the ntly perform
extent of theactivities
patholgy.ofThe
daily living
infected
the swelling increases during the day but is area is foul-smelling and the affected individual
reversible once the patient lies flat
flat in
 in bed. In frequently experiences acute attacks. 
stage 2, the swelling is no longer reversible Hydrocele or chylocele results in the
overnight, and the patient may still experience  obstruction of the lymphatics of the tunica  
 

CHAPTER 3: Nematode Infections   171 

vaginalis (Plates 3.25 – 3.26).

3.26). Clear or straw- Although Malayan filariasis occasi onally
colored hydrocele fluid typically accumulates  presents with
wi th groin involvement,
involv ement, hydroceles
hydr oceles
in the closed sac of the testis, and rarely, the are rare. Deformities resulting from Malayan
fluid may have a milky appearance caused filariasis are not as severe as in Bancroftian
the presence of lymph — a condition known filariasis. There may be enlargement of the
as chylocele. Hydrocele is a common chronic epitrochlear, inguinal, and axillary lymph
disease manifestation of Bancroftian filariasis  nodes. More advanced cases may either  
since W. bancrofti worms have been shown  be asymptomatic, or may manifest with
ultrasonographically to prefer localization in
ultrasonographically elephantiasis of one or more limbs, usually
scrotal lymphatics. These cases usually occur   involving the area below the knee or below  
after puberty, and the prevalence increases the elbow.
with age. Chronic epididymitis, funiculitis, Rupture of lymphatics in the kidney
lymphedematous thickening of the scrotal skin, may produce chyluria. This results from the
and thickening of the spermatic cord are also  blockage of retroperitoneal lymph nodes
genital manifestations of chronic Bancroftian  below the
th e cisterna chyli.
ch yli. There is
i s consequent
filariasis. The thickened cord can usually be
filariasis. The reflux and flow of the intestinal lymph directly
 palpated during physical examination. In into the renal lymphatics,
ly mphatics, which may rupture
females, lymphedema of the vulva may occur.  and allow the flow
flow of
 of chyle into the urinary
tract. The “milky urine” contains considerable
quantities of lymph srcinating from the 
gastrointestinal tract. There are several reports of  

gfiloar miaesr ius.loMnie p  spiinc  p
cr hor sictoi p ieanttusr w
phaetm iiai ayanalcsr of of tciacnur
thB
aim
in microfilaremic persons.  
Tropicall pulmonaryeosinop
Tropica pulmonary eosinophilia
hilia (TPE) is a
classic example of occult filariasis in which the
typical clinical manifestations are not present,
and microfilaria are not found in the blood but
may be found in the tissues. The syndrome,
which is brought about by immunologic
Plate 3.25. Hydrocele
hyper-responsiveness to filarial infection, is
(Courtesy of Dr. Vicente Belizario, Jr.) characterized by paroxysmal nocturnal cough,
characterized
hypereosinophilia (3,000-5,000 cells per mm3
of blood, levels unrelated to the severity of
symptoms), elevated erythrocyte
erythrocyte sedimentation
rate, evidence of diffuse miliary lesions or  
increased bronchovascular markings, extremely
high titers of filarial antibody (IgE), and good
therapeutic response to DEC. In most cases,
lung function istotal
vital capacity, impaired, with a reduction
lung capacity, in  
and residual
volume. It is commonly misdiagnosed as asthma
or tuberculosis. Chronic symptoms may delay
Plate 3.26. Small and big hydroceles in two diagnosis, and if untreated, TPE progresses to
patients suffering from filariasis  
(Courtesy of Dr. Vicente Belizario, Jr.)
chronic pulmonary fibrosis and respiratory
failure. 
 

172   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Diagnosis  microfilariae into coming out to the peripheral

circulation, allowing blood smear collection
The microscopic finding of characteristic even during daytime.
microfilaria in the blood is the traditionally
microfilaria in
Although these methods are still widely
accepted procedure. Due to the nocturnal
used, their low sensitivity and poor acceptability
 periodicity of most W. bancrofti strains, wet necessitate alternative approaches
approaches that fulfill the
smears or thick blood smears are taken between  requirements for control program mapping,  
8m pic.r mofi. laanr diae4 m
a.m
ay. nInotm
 baenydecmhr oonnsitcr a b
inlf eecitniotnhse, monitoring and assessment, and endpoint
 peripheral blood. This may be brought about decision criteria and surveillance. Detection
Detection
of circulating filarial antigens (CFA) is  nnow
ow  
 by the following factors: (a) low inte
intensity
nsity o
off
the preferred method since it also detects
infection, (b) dead worms, and (c) obstructed
latent infections. This is mainly done with
lymphatics. In cases of low intensity infections,
immunochromatographic card tests. These
filtration using a nucleopore filter  or
 or the Knott’s
simple card tests that detect CFAs are very
method for concentration may be used. Table 
sensitive and specific, thus eliminating the
3.3 summarizes the main distinguishing features
features need for laboratory facilities. Other diagnostic
of themicrofilariae
the microfilariae  of 
of W.bancrofti and B. malayi
approaches include molecular xenomonitoring
which may be appreciated microscopically
microscopically in of parasites in pools of mosquitoes, and
stained thick blood films. The DEC provocative detection of exposure to transmission in
test (3 mg /kg DEC single dose) stimulates  
children with antibody detection.

Table 3.3. Comparison of microfilaria of Wuchereria bancrofti and Brugia malayi  

Mean length (μm)

Pink

Kinky

Innenkôrper length ( μm)

Source: World Health Organization. Control of lymphatic filariasis: a manual for health personnel. Genev a: World Health Organization; 1987.

Treatment  tive chemother a py f or

athnediinsttehrr eu b patsiiosnof o pf  r tr eavnesnm ission in elimination
DEC has been the drug of choice for
 programs.. A single optimum
 programs optimu m dose of DEC does
the treatment
discovery of lymphatic
in 1948. filariasis
It is effective since
against its
both not clear all microfilariae and does not kill all
adult worms. A regimen of 6 mg/kg for 12
microfilaria and adult worms; however, some
consecutive days is better than the single
s ingle dose,
strains of adult worms may not be sensitive to and can be given to individuals if supervised
sup ervised
the drug. It markedly lowers blood microfilaria  by a medical practitioner,
practiti oner, preferably
preferabl y in divided
even in single once-a-year doses of 6 mg/kg. doses after meals.  
This reduction is sustained for about one year, 
 

CHAPTER 3: Nematode Infections   173 

The drug’s mechanism of action is not well ivermectin alone. There is probably no added
understood, but it is clear that host components effect against adult worms in LF. DEC or
are necessary, such as the arachidonic acid ivermectin in combination with albendazole
 pathway and the 5-lipoxygenase pathway.   used in LF elimination programs has the added
Recent trials show that DEC has no role in the  benefit of clearing so il -transmitted helminth
soil
treatment and prevention of ADLA attacks in (STH) infections. 
lymphedema. DEC is the treatment of choice   Doxycycline and related antibiotics kill the 
Doxycycline
for the treatment of TPE and is given for 3 to endosymbiont Wolbachia, which is essential
4 weeks. for growth, development, embryogenesis, and
Adverse events (AEs) include fever, myalgia, survivalof filarial worms. Treatment of LF with  
headache, and sore throat or cough lasting 24 a course of doxycycline at 200 mg daily for 4 to 6
to 48 hours. These are mild and self-limiting, weeks results in long-term sterility and eventual
and may be treated symptomatically. These death of adult worms. Anti-Wolbachia therapy
AEs represent an immune response that is showed significant improvements in lymphatic
mainly due to the destruction of microfilaria  pathology and a decrease in the severity of
that is similar to the Mazzotti reaction seen lymphedema and hydroceles. Studies have also
in onchocerciasis. There may also be AEs shown that prior treatment with doxycycline
associated with rapid killing of adult worms reduces the frequency and severity of AEs to
(AFL), which can lead to scrotal pain in men, DEC-albendazole. This relatively good safety
and systemic inflammation due to t he release  profile is due to the avoidance of parasite-
of Wolbachia. Direct adverse events due to the  mediated or Wolbachia-mediatedinflammatory
inflammatory  

eer r mr aer cet.in  is  a  dr ug  pr imar ily  used  in

dr ugIavr  achdvem  cptiyonhsa.s Amltahnoyu bgehnaefi
er soethr er a p ntsi- es peocl ibaallcyhiian
W 
the treatment of onchocerciasis, loiasis, and the treatment of individual patients, its use
strongyloidiasis. It is also effective against in community-based control and elimination
ectoparasitess such as lice and scabies. Used in
ectoparasite  programs is hindered by the logistics of tthe
he
LF, it is highly effective and well tolerated at length of treatment and contraindications in
doses of 100 to 200 µg/kg for the reduction children and pregnant
p regnant women.  
of microfilaremia
microfilaremia for for up to 1 year. Ivermectin The treatment recommendations for
leads to hyperpolarization
hyperpolarization of glutamate-sensitive ADLA include bed rest, cooling the affected area
channels and immobilization of microfilaria. to relieve the pain, analgesics and antipyretics
AEs are similar to DEC but milder due to its for pain and fever, topical antibiotics and
relatively slower parasite clearance. It has no antifungals for superficial bacterial and fungal
 proven action against adult worms and TPE.   infections, systemic antibiotics (e.g., penicillin)
Albendazo le i s a broad- spectrum for moderate to severe cases, and elevation of
anthelminthic given orally that is effective   the involved extremity. Enrollment in a hygiene  
against nematodes, cestodes, and flatworms. education program dramatically reduces the
Its mechanism of action is via inhibition of incidence of ADLA and the progression of
 polymerization of -tubulin and microtubule
 polymerization lymphedema to elephantiasis. A proper “foot
formation. A low dose of 400 mg used for   care progra
 program”
m” includes: (a) washing the affected 
the treatment of most intestinal helminth limb twice a day with soap and water especially
infections decreases W. bancrofti microfilaremia the webs of toes and skin folds, and drying
 progressively for 6 to 12 months. Based on with a clean cloth to remove moisture; (b)
current studies, combination with DEC or clipping nails often and keeping them clean; (c)
ivermectin reduces microfilarial loads in the  preventing
 preventi ng and promptly
prompt ly treating
treatin g local injuries
 periphery longer than
t han treatment
treat ment with
wit h DEC or   and infections with topical agents; (d) regular  
 

174   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

use of properly fitting footwear; and (e) raising  effects, and have not been adequately evaluated
the affected limb at night to
t o reduce the
t he sweliln
swelilng.
g. in filariasis-endemic areas. Current WHO
In the setting of severe lymphedema and  guidelines call for the complete surgical removal
elephantiasis,, the hygiene education program 
elephantiasis of the tunica vaginalis to minimize or prevent
recurrence. 
stated above may bandages,
use of compressive be supplemented
bandage s, stockings,with the
manual
Epidemiology 
lymphatic drainage (massage), heat therapy, 
and, in refractory cases, surgical procedures.  About 120 million people worldwide
An estimated 27 million males suffer   are affected by the disease, and more
m ore than  
from hydroceles, and the prevalence is strongly 1 billion people are at risk (one-fifth
(one- fifth of
 of the
associated with the intensity of parasite world’s population), mostly in the poorest
transmission (microfilaremia prevalence).
pr evalence).  areas. Bancroftian filariasis accounts for 90%
Recent observations from Brazil, Egypt, and of cases in 83 endemic countries while the
Haiti indicate that many acute hydroceles Malayan filarial
filarial worm
 worm (and B. timori) causes
resolve spontaneously, and about 24%
24 % persist
persist to the remainder. W. bancrofti affects more than
 become chronic. Surgery is the recommended l00 million people in the tropical areas of India,
treatment for hydrocele, and if done
don e properly, Southeast Asia, the Pacific  Islands, Africa, and
is deemed curative. Other methods such as South and Central America. India has the largest
aspiration of fluid and injection of sclerosing number of cases. B. malayi and B. timori affect 
substances are less effective, are associated with 12.5 million people in Southeast Asia (Figure
hydrocele recurrence, have unacceptable side  3.11). The prevalence of infection continues to  
 

CHAPTER 3: Nematode Infections   175 

rise in tropical and subtropical countries due

to rapid growth of cities. This creates more
 breeding sites
s ites for mosquitoes
mosquito es to transmit
trans mit the
disease in areas where Culex is the vector. 

In rural is
W. bancrofti areas, particularly
transmitted in  Anopheles
by the Africa,  
mosquito, which includes species that transmit
malaria. In urban areas, the major vectors are 
Culex mosquitoes which can breed in latrines, 
sewage, and ditches. In the Pacific region,
mosquito vectors belonging to the genus Aedes
can breed in tiny areas of clean water in the axils
of plants (Plates 3.27 – 3.28),
3.28), empty containers, Plate 3.28. An axil of abaca: 
or old tires.  a breeding site of  Aedespoecilus
 Aedespoecilus  
(Courtesy of Dr. Vicente Belizario, Jr.)
In the Philippines, 45 provinces are
endemic for LF: (Region IV) Quezon Province, Leyte, Southern Leyte, and Western Samar;
Marinduque, Oriental Mindoro, Occidental (Region IX) Zamboanga del Norte, Zamboanga
Mindoro, Palawan, and Romblon; (Region  
V)  Albay, Camarines Norte, Camarines Sur,
Sibugay, and Zamboanga del Sur; (Region X)
Catanduanes, Masbate,
Masbate, and Sorsogon; (Region 
Bukidnon, Misamis Occidental, and Misamis
Oriental; (Region XI) Compostela Valley,
VI) Aklan, Antique, Capiz, and Iloilo; (Region Davao del Norte, Davao del Sur, and Davao  

r neSgr aoms aO
EaIsIt)e N
V r ienotr ra thll;e;er (nR 
r,r,  N IIIo)r tBhielirnan, 
R eSgaiomnar V,  N Oriental; (Region XII) North Cotabato,
Saranggani, South Cotabato, and Sultan
Kudarat; (CARAGA) Agusan del Norte,  
Agusan del Sur, Dinagat Islands, Surigao del
 Norte, and Surigao del Sur; (ARMM)
(ARM M) Basilan,
Maguindanao, and Sulu (Figure 3.12). 
 Aedes
 Aed es p oec ilus , which breeds in water
oecilus
accumulated in the axils of abaca and banana
 plants, is the mosquito vector in most provinces
of the Philippines.  Anophe les minim
minimusus var .
 flavirostris , the principal vector for malaria in
the Philippines is also the vector of W. bancrofti
in Sulu and Palawan.
Palawan. Malayan filariasis has been
described in Palawan, Eastern Samar, Agusan  
coel-eSxuisr t,saw
d . Ianlat yhie. sTe p
ul.um
ndithS B ceos,sqW 
 helam uito vector s,
. bancr o f tt  i
are Mans oniabonnae which breeds in freshwater
 Mansonia
swamps, and Manso
 Mansonia
nia uniformis which breeds
uniformis
in rice fields. These mosquitoes are night biters
and they usually start biting as early as 5 p.m.
until 11 p.m. The reported prevalence is less
than 3%. Cats are important reservoir hosts
Plate 3.27. Farmer in abaca plantation and may transmit the infection to humans by
(Courtesy of Dr. Vicente Belizario, Jr.) means of the cat-mosquito-man cycle.
 

176   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

infected males than females. This may be due

to economic activities (e.g., abaca farming) that
increase exposure of adult males to mosquito
vectors. In the Bicol region, hydroceles are more
frequently
the encountered
extremities.   than elephantiasis of

Prevention and Control 

The World Health Organization (WHO)
in the 50th WorldHealth Assembly
Asse mbly has targeted
targete d
LF for elimination by the year 2020. The Global
Programme to Eliminate Lymphatic Filariasis
(GPELF) has two major goals: to interrupt
transmission of the parasite via preventive
chemotherapy, and to provide care for those
who suffer from the clinical manifestations  
of LF through hygiene education programs.
The development of safe, effective, and well-
Figure 3.12. Map of lymphatic filariasis-endemic
tolerated single dose microfilaricidal regimens
provinces in the Philippines, distribution in the has resulted in effective and sustainable drug
three major island groups, and provinces delivery in endemic areas. DEC-medicated table 
dec lar e dDly
em a teicntff iil loaf r iH
ae tr hee  by the
(Adapted from 
papr h
tm
from  www.doh.gov.ph/content/
s-lf 
sia
eolrr i mcoinoaktingg LsaFltinhasso b
el cecaes.sf Buellllsyidiens
meeennduesemdicsuar 
national-filariasis-elimination-program)   the commonly used filaricidal drugs, drug
development is continuously being undertaken.
The national microfilaria rate (MFR) Moxidectin has been proven in recent animal
in 1998 was 9.7%. Although the reported   trials to be
to be a very effective macrofilaricide. 
 prevalence rates
rat es appear to
t o be generally
gener ally low —   The goal for endemic communities is to
 below 3%, studies in Sorsogon have shown eliminate the presence of microfilariae in the
that microfilaria
microfilaria rates
 rates may be as high as 15%  blood in order to prevent transmission of the
in endemic villages. In a village in Sorsogon, disease by vectors. According to the WHO,
hydrocele was present in 4% of males, while single doses of DEC in combination with
incidence of ADLA over a 1-year follow-up another drug such as albendazole or ivermectin
 period was 100 cases per 1.000 population. is 99% effective in removing microfilariae
Recent studies show that Romblon province has  from the blood for up to one year from
treatment. Proper control of transmission in
heinhdiogr 
tM hoeshtaC 18
18i.c8r o%fi,lar niad pOr er viaelnetnacl e
s tFhAe hr aigteheosf t m communitiess therefore entails the identification
communitie
rate of 12.6%.   of endemic areas and implementation of mass
In the Philippines,
Phili ppines, areas
ar eas endemic
endemicfor LF are treatment programs using an albendazole/
in regions with
wi th the highest
highest incidence of poverty.
poverty . DEC combination; or a DEC/ivermectin
combination in areas where onchocerciasis or
Out of a total of 80 provinces, 39 have a higher
 poverty incidence than the national average and loiasis is prevalent. The use of albendazole/
30 of these 39 provinces are endemic for LF.  DEC or albendazole/ivermectin combinations
In general, adults are more frequently offers opportunities for integrated control of
infected than children, and there are more   STH and LF. 
 

CHAPTER 3: Nematode Infections   177 

In the Philippines, the four provinces in Anitha K, Shenoy R. Treatment of lymphatic

Panay Island as well as the province of Quezon filariasis: current trends. Indian J Dermatol
were recently found to be endemic. The Venereol Leprol. 2001;67:60 – 5
Venereol 5..
Department of Health (DOH) is currently Bain O, Babayan S. Behaviour of filariae:

implementing
 provinces. MDA activities
According in those
to the DOH, nine morphological
of their life styleand anatomical
within signatures
the arthropod and
 provinces have reached elimination level:  vertebrate hosts. Filaria J. 2003;2:16. 
SouthernLeyte,Sorsogon,Biliran,Compostela Belizario V, Lariosa T, Pesigan A, Leonardia
Valley, Bukidnon, Romblon, Agusan del Sur, W, Llanto R. The clinical epidemiology
epidemio logy of
Dinagat Islands, and North Cotabato. The  lymphatic filariasis in an endemic village  
criteria for a province to be declared LF-free in Sorsogon. Acta Med Philipp. 1995;
are: (a) MFR of <1%; (b) no true positives in 31(2):61 – 9.
9.
children ages 2 to 4 years old; and (3) no true Belizario V, Reyes L, Solon J. Rapid
R apid assessment
 positives among new school entrants. MDA methods for lymphatic filariasis in two
coverage rates for the monitoring and evaluation municipalities in Sorsogon, Philippines.
of elimination programs should be used with Final report 1998. Geneva: Special
caution. A study by Amarillo, et al . in 2008 Programme for Research and Training
revealed over-reporting, where the proportion in Tropical Diseases, World Health
of the sampled population that received and Organization.  
ingested the antifilarial drugs was much lower Bennuru S, Nutman T. Lymphatics in human
than the reported coverage.
coverage.  lymphatic filariasis: in vitro models of  

 pr evePnetr  cptr wotitehctm
rs conatla  p queiatsouvr ecstomr sa.yThe p
ivoe sm  lpuse Layr ma p
 p Rine  ds uBcieodl. 2llyy0m09
sithe-R   p;h(a4t)i:c221r  m9o.deling. 
1r 5e – 
of mosquito nets as well as insecticide residual Bennuru S, Nutman T.Lymphangiogenesi Lymphan giogenesisand sand
spraying may help decrease the number of lymphatic remodeling induced by filarial
mosquito vectors at home. In addition, advances  parasites: implicatio
i mplications ns for pathogenesis.
path ogenesis.
in vector control include the development of PLoS Pathogens. 2009;5(12):e1000688. 
 Bacillus
 Bacillus sphaericussprays and polystyrene beads
sphaericus Bockarie M. Deb R. Elimination of lymphatic
to seal latrines in order to eliminate or reduce filariasis: do we have the drugs to complete
Culex vector populations. Health education the job? Curr Opin Infect Dis. 2010;3:617 –  
may also benefit
also benefit  those who, living in endemic 20.
areas which may lack awareness on the etiology, Cabrera B, Arambulo P. Human filariasis
 prevention, and control of LF.  in the Philippines. Acta Med Philipp.
1973;9(2):160 – 73.
73.
References 
Das PK, Ramaiah KD, Vanamail P, Pani SP,
Adiss D, Brady M. Morbidity management Yuvaraj J, Balarajan K, et al . Placebo- 
in the global programme to eliminate controlled community trial of four cycles
lymphatic filariasis: a review of the scientific of single-dose diethylcarbamazine or
literature. Filaria J. 2007;6:2.   ivermectin against Wuchereria bancrofti
Amarillo M, Belizario V, Sadiang-abay J, Sison infection
R and transmission
Soc Trop trans
Medmission in India.
Indi a. Trans
Hyg. 2001;5(3):336Trans  – 441.
1.
S, Dayag A. Factors associated with the
acceptance of mass drug administration
acceptance Department of Health. National filariasis
for the elimination of lymphatic filariasis in elimination program [Internet]. 2011 [cited
Agusan del Sur, Philippines.
Philippines . Parasit
Parasi t Vectors.
Vectors. 2012 Mar 3]. Available from http://www.
from http://www.
2008;1:14.  doh.gov.ph/content/national-filariasis-
elimination-program
 

178   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Dreyer G, Addiss D, Dreyer P, Noroes L. Basic compression for filarial lymphoedema. Nat
lymphedema management: treatment and Med J India. 2002;15(4):192 – 4 4..
 prevention of problems associated with Taylor M, Hoerauf A, Bockarie
Bockari e M. Lymphatic
lymphatic filariasis. New Hampshire: filariasis and onchocerciasis. Lancet.  

Hollis
Galvez Tan,Publishing Company;
J. The elimination of 2002.
lymph  atic
lymphatic The 2010;376:1175
Global Alliance  – 
to85.
8Eliminate
5. Lymphatic
filariasis: a strategy for poverty  alleviation  Filariasis. Lymphatic filariasis [Internet]. 
[Internet].  
and sustainable development
development — 
 —  perspectives 2010 [cited 2012 Mar 3]. Available from
from the Philippines. Filaria J. 2003; 2:12.   http ://www.filariasis. org/index.pl
org/in dex.pl 
Hernandez L. Current status of filariasis in the World Health Organization. Control of
Philippines. Southeast Asian J Trop Med lymphatic filariasis: a manual for health
Pub Health. 1993;24:8-9.  personnel. Geneva: World Health
Hoerauf A. Filariasis: new drugs and new Organization; 1987.  
opportunities for lymphatic filariasis and World Health Organization. WHO technical 
onchocerciasis. Curr Opin Infect Dis.   report series 821, lymphatic filariasis: the  
2008;21:673 – 81. 81. rep ort of the 
disease and its control, fifth report
Houston R. Salt fortified with diethylcarbamazine WHO expert committee on filariasis.  
(DEC) as an effective intervention for Geneva: World Health Organization;1992.  
lymphatic filariasis, with lessons learned World Health Organization. Tropical disease
from salt iodization programmes. Parasitol. research progress 1975 – 94,
94, Highlights
2000;121(suppl):S161 – 73.
73.  1993 – 1994,
1994, Twelfth programme report of  
’

eecctCi onnwoir thR ,  BBOr us b g ioar nm
JensoEn. IJn, f O e iJc,rr  oDf ielavr ainae y tPhr eogU
r   N
aN
mDmPe/W
f f or or R  ndHTOr ai
ldeseBar nchk. aW npin
aiS  p iaiiln
ecgia
induces the apoptosis of CD4+ T Tropical Diseases (TDR). Geneva: World
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Or ganization; 1995.
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7. on lymphatic filariasis. Geneva: World
Kron M, Walker J, Hernandez L, Torres E, Health Organization;
Or ganization; 2000.
Libranda-Ramirez B. Lymphatic filariasis
fi lariasis World Health Organization. The global
in the Philippines. Parasitol Today.   elimination of lymphatic filariasis: the
2000;16(8):329 – 33.
33. story of Egypt. global elimination of
Manjula Y, KateV, Ananthakrisnan N.Evaluation lymphatic filariasis. Geneva: World Health
of sequential intermittent pneumatic   Organization; 2003.  
 

CHAPTER 3: Nematode Infections   179 

Parastrongy u
l scanto
 nens s
i
Vicente Y. Belizario, Jr., Francis Isidore G. Totañes

reviously classified under the genus   intestine. This arrangement

arrangement is usually described
 Angiostron
 Angio gylus, Paras
strongylus  Parastrongy
trongylus
lus can
cantonensis,
tonensis asthe “barber’s pole”
   pattern. The morphologic  

P 
or the rat lungworm, was first described
 by Chen in 1935 from domestic rats in
Canton, China. The nematode, which normally
features may be observed through the worm’s
transparent cuticle. The posterior end of the
female worm is blunt shaped. A single female
lives in rat lungs, has been known to cause worm can lay up to 15,000 eggs daily.
eosinophilic meningoencephalitis in man.  The elongated ovoidal eggs have delicate
Human infection was first reported in Taiwan hyaline shells. They measure 46 to 48 µm by
in 1945. Parastrongyliasis outbreaks in the 68 to 74 µm and are unembryonated when
Pacific islands have been documented since oviposited. The 1st stage larva, found in the
then, and more than 2,800 cases have already lungs of the rodent host, has a distinct small
 been reported worldwide.   knob near the tip of
o f the tail. Two
Twowell-developed
well-dev eloped
chitinous rods below its buccal cavity identify
Parasite Biology 
the third stage larva. These rods have expanded
The adult worm, which is pale and filiform, knob-like tips.
has a length of 17 to 25 mm (Plate 3.29). Male   Rats are the definitive hosts of  P. cantonensis . 

0w.o2r 5mtos  0m.3e5asm
0. e  1in6 dtioam2e2tem
ur m Thieny hle
r. m leanvgetahwaenlld- stagtsealr aer vinaef f e. cTtehdetlhar ovu
R  aeg p satitoenthoef   tshtoem
h ei ngeetr  thaicr hd
developed caudal bursa, which is kidney-shaped wall and travel in the bloodstream until they
and single-lobed. Female worms measure 19 reach the central nervous system. They undergo
to 33 mm in length and 0.28 to 0.50 mm two molts, which take about 2 weeks, before
in diameter. The female worms have uterine they reach maturity. Early development occurs
tubules that are wound spirally around the in the brain. After the final
final molt
 molt in rats, the
young adults migrate to the pulmonary arteries
to complete their development. After 2 weeks,
the adult females start laying eggs.  
Adult worms live in the two main branches
of the pulmonary arteries of the rat. In the
 bloodstream, gravid
 bloodstream, gravid females
females lay eggs, which
which are
are
transported into the smaller vessels of the lungs.
After 6 days, eggs hatch and release the first 
stage larvae that penetrate into the respiratory
tract. The larvae then migrate up to the trachea
and reach the oropharynx where they are then
swallowed and eventually expelled in the feces.
It takes about
abou t 6 to 8 weeks from infection
inf ection befor
beforee
the rat excretes 1st stage larvae (Figure 3.13). 
The first stage larva is the infective stage
Plate 3.29. Parastrongylusadults for the molluscan intermediate host. In the
(Courtesy of the Department of Parasitolog
Parasitology,
y, 
UP-CPH)
Philippines, the known intermediate hosts  
 

180   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

include the following slugs and snails: Achat

 Achatina
ina Although the mechanism by which humans
 fuli ca (Plate 3.30) or giant African snail,
 fulica get infected is not yet
y et entirely clear, transmission
 Hemiplecta sagittifera, Helicostyla macrostoma, is usually attributed to: (a) ingestion of the raw
Vaginilus plebeiu,  ssand Veronicellaaltae. Its mode
plebeiu mollusk intermediate host infected with the
of infection is by ingestion or active penetration. third stage larva; (b) ingestion of leafy vegetables
In the mollusk, larva eventually develops into contaminated with mucus secretions of the
the 3rd larval stage in about 12 days. mollusk carrying the infective stage (3rd larval 
 

CHAPTER 3: Nematode Infections   181 

worms may also be seen in the cerebrum and

cerebellum. Eosinophils, monocytes, and
foreign body giant cells in the spinal cord or
in the cerebrospinal fluid
fluid (CSF)
 (CSF) are usually

associated
contains with
100 the infection.
to 1,000 Theper
leukocytes CSFµL.usually
Adult
worms have also been recovered from the eyes  
and pulmonary arteries of patients. Large
numbers of Charcot-Leyden crystals have also
 been demonstrated in the meninges. Dead 
worms can also result in inflammatory reaction
and local tissue necrosis. 
Plate 3.30.  Achatn l a, the intermediate
ii  afu ii 
c intermediate host of
Prognosis is usually good. In most cases,
Parasrtongy luscantonens is the disease is mild and no hospitalization is
(Courtesy of the Department of Parasitology, necessary. The infection is self-limited and
UP-CPH) symptoms gradually disappear with recovery.
Meningeal symptoms are often the first to
stage) of the parasite; (c) ingestion of a paratenic subside, followed by improvements in vision,
host, such as freshwater prawn or crab harboring and relief from paresthesia. Cranial nerve
the infective stage of the parasite; or (d) drinking involvement is the last to recover. Permanent
of contaminated water. neurologic deficits have been documented, and  

gh etnhehhuustmom
thr ouW anascghetinintof f ec
etcht edi,nthtestlianr ev,a e pnatesr s in rare cases, the disease may result in death.  
Diagnosis 
the circulatory system and migrate to the brain
or spinal cord, or occasionally migrate into the Diagnosis of parastrongyliasis in humans
eye chamber. In humans, however, the larvae is relatively difficult, since the primary site of
 probably remain in the brain for a longer period infection is the brain. Presumptive diagnosis
of time and do not develop to the adult stage.   may be made based on travel and exposure
history, correlated with clinical symptoms,
Pathogenesis and Clinical Manifestations  
medical history, laboratory findings, brain
In most cases, the incubation period is imaging results, and serological tests.  
around 6 to 15 days, but may vary
varyfrom 12 to 47 Examination of blood may reveal a high
days. The chief complaint in many cases is acute,  proportion of eosinophils, comprising 7 to
severe, intermittent occipital or bitemporal 36% of the white blood cell (WBC) count.
headache. Other common symptoms include ExaminationofCSF maycontributetoincreased
stiffness of the neck, paresthesia, vomiting, sensitivity in the diagnosis of parastrongyliasis.
fever, nausea, blurred vision or diplopia,   CSF eosinophilia of greater than 10% in
 body or muscle pain, and fatigue.
fati gue. Confusion,
Confus ion,    proport ion to WBC will exclude other common
 proportion
incoherence, disorientation, memory lapses, causes of meningitis. The CSF protein level in
or coma have also been observed during most patients is mildly elevated, while the CSF
illness. Intraocular hemorrhage and retinal glucose is normal. However, other infections
detachment as associated complications have (e.g., cysticercosis, trichinosis, visceral larva
also been reported. Postmortem examination migrans, schistosomiasis, paragonimiasis, and
may show leptomeningitis, encephalomalacia gnathostomiasis) involving the central nervous
and moderate ventricular dilation.
dilation. Immature  system must first  be ruled out. 
first be
 

182   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Meningeal lesions may be appreciated Further studies showed that its prevalence
with the use of computed tomography (CT) in rats is less than 7%. The presence of  P.  P.
scan. CT scans may also reveal non- specific cantonensis as a parasite of rats and/or snails
cerebral edema and ventricular dilatation.   has been reported in the following provinces
Magnetic
lesions resonance
with imaging
hyperintense (MRI) may
T2 signal. show
Although of Luzon:
 Norte, Batangas,
Laguna, Bulacan,
Mountain P Cavite, Nueva
Province,
rovince, Ilocos
enzyme-linked
enzyme-link ed immunosorbent
immunosorbent assay (ELISA)  Ecija, Pampanga, Pangasinan, Quezon, Rizal,  
for the diagnosis of parastrongyliasis is still not Sorsogon,
Sorsogo n, Tarlac, and Metro Manila. Two
Two cases
commercially available, a dot-blot ELISA that of ocular parastrongyliasis have been reported
tests blood has been demonstrated to be 100%   from the East Avenue Medical Center. The  
sensitive and specific for use in epidemiological  patients were blood relatives coming from
surveys. In addition, serum antigens from P. Isabela who have eating history of improperly
cantonensis can also be detected by immuno- cooked snails. The worms were identified
identified  at
 polymerase chain reaction (PCR).  the College of Public Health, University of the
Philippines Manila. 
Treatment 
Prevention and Control 
 No anthelminthic treatment is
recommended at present, although mebendazole The main preventive strategy against
and albendazole have been demonstrated to  parastrongyliasi
 parastron gyliasiss is through awareness and
effectively treat parastrongyliasis in China, education on proper eating habits and safe
Taiwan, and Thailand. Anthelminthic therapy   food preparation. The
T he public should be 

eetnheshdouwr natitoon r oeelf fli etvhee sdyim
r headsu bccee se p s caunldar
 pastoe.mO d waaesahteidngvr eagwetao b
misocloluusr kasgeodr  f ur onm
w  br   p r llyyancdook
lpeso.oH ooked
 parastrongyliasis
 parastron gyliasis may require surgical removal washing after gardening should also be advised.
of worms from the eyes. Symptomatic treatment Farmers occasionally use molluscicides, such
with the use of analgesics and lumbar puncture as metaldehyde or iron phosphate food bait
can relieve the headaches experienced by the  pellets to
t o control intermediate
intermedi ate hosts.
host s. Copper
 patient with eosinophilic
eosinophilic meningitis.
meningitis. Prednisone
Prednisone  barriers against snails and slugs are also
30 mg daily is recommended, particularly in utilized by farmers to prevent contamination
severe cases with cranial nerve involvement. of vegetable and fruit crops. Health workers in
The anti-inflammatory and immunosuppressive endemic areas should also be educated on the
effects of steroids are helpful in mitigating the diagnosis, treatment, control, and prevention
disease process.  of parastrongyliasis.  
Epidemiology  References 

Human infection with  P. cantonensis was

cantonensis Chen ER. Angiostrongyliasis and eosinophilic
first reported
first  reported in 1945 by Nomura and Lin in meningitis in Taiwan: a review.. In: Cross
Taiwan.As a human parasite,
parasit e, P. cantonensis
cantonensishas JH, editor. Studies on angiostrongyliasis
also been documented in approximately 30 in East Asia and Australia. Taipei, Taiwan: 
countries including Thailand, China, Tahiti, U.S. Naval Medical Research Unit No. 2,;
French Polynesia, USA, Cuba, New Caledonia, 1979. p. 57 – 73.
73.
Japan, Australia, Vanuatu, India, and the Cross JH. Public health importance of
Philippines.  Angiostrongylus cantonensis and its relations.
In the Philippines, Nishimura and Yogore Parasitol Today. 1987;367 – 9
9.. 
reported the presence of Paras
 Parastrongylus in rats. 
trongylus
 

CHAPTER 3: Nematode Infections   183 

Eamsobhana P, Yoolek A, Kreethapon N. meningitis. J Clin Microbiol. 1979;9:629 –  

Blinded multi-laboratory evaluation of an 30. 
in-house dot-blot ELISA kit for diagnosis of Lu S, Zhang Y, Steinmann P, Zhou XN.
human parastrongyliasis.
parastrongyliasis. Southeast Asian J Emerging angiostrongyliasis in Mainland
Trop JR,
Hollyer Med Troegner
Public Health.
VA,2003;34(1):1
Cowie RH, – 6.  China.
4. Emer Infect Dis. 2008;14(1):161 –  
Hollingsworth RG, Nakamura-Tengan  Manson-Bahr
Manson- Bahr PE, Bell DR. Manson’s tropical  
LC, Castro LC, et al. Best on-farm food diseases. 19th ed.London: Bailliere Tindall;
safety practices: reducing risks associated 1987. p. 564 – 7
7..
with rat lungworm infection and human  Peters W, Pasvol G. Atlas of Tropical Medicine
eosinophilic meningitis. Honolulu and Parasitology. 6th ed. Philadephia:
(Hawaii): College of Tropical Agriculture Elsevier Ltd.; 2007. p. 242 – 4
4.. 
and Human Resources, University of Punyagupta S. Angiostrongyliasis: clinical
Hawaii; 2010.  features and human pathology. In: Cross
Jitpimolmard S, Sawanyawisuth K, Morakote JH, editor. Studies on angystrongylosis in
 N, Vejjajiva A, Puntumetakul M, East Asia Australia. Taipei (Taiwan): US
Sanchaisuriya
Sanchaisuriya K, et al. Albendazole therapy  Naval Medical Research Unit No.2; 1979.
for eosinophilic meningitis caused by  p. 138 – 50.
50. 
 Angiostron
 Angiostrongylus
gylus cantonensis.
cantonensis Parasitol Res. Theravanij S. Immmunology of
2007;100:1293 – 6.6. angiostrongyliasis. In: Cross JH, editor.
Koo J, Pien F, Keiks MM. Angi
 Angiostr
ostrongy
ongylus
lus   Studies on angiostrongyliasis in Eastern 

1p0h:i1l1ic55m – e6n2in. gitis.  R ev  Inf ec

e1o9s8in8o;  p ect  Dis. Asaivaala n
 N MdedAiucasltr R 
aelisae.ar Tcah  p  TNaiow. a2n; )1:97U9S.
ipUeni i(t N
Kuberski T, Bart RD, Briley JM, Rosen L.   p. 151 – 64.64. 
Recovery of  Angiostrongylus cantonensi
cantonensiss  Wang QP,
QP, Lai DH, Zhu XQ, Chen XG, Lun
from spinal fluid of a child with eosiniphilic   ZR. Human angiostrongyliasis. Lancet
Infect Dis. 2008;8:621 – 30.
30.
 

184   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Trc
i hi 
nel 
asp rial 
i 
s
Vicente Y. Belizario, Jr., Francis Isidore G. Totañes

richinella was first described by Tiedemann  the body.In addition, the female wworm
orm has an
in 1822. In 1835, James Paget and Richard   oviduct, a seminal receptacle, a coiled uterus, 
Owen demonstrated Trichinella in human  a vagina, and a vulva. The vulva is situated in
cadavers in London. Before the turn of the   the anterior 5th on the ventral side of the body.
century, German investigators were able to The viviparous female lives for 30 days and is
 prove that raw or insufficiently
insufficiently cooked
 cooked meat capable of producing more than 1,500 larvae 
(i.e., pork) was responsible for trichinellosis in in its lifetime. 
humans. Trichinellosis wasinitially attributedto The larva measures 80 to 120 µm by  
a single species, T. spiralis, but the discovery of 5.6 µm at birth, but reaches the size of 0.65
marked strain differences in Trichinellaisolates to 1.45 mm in length and 0.026 to 0.040
have led to the identification
identification  of new species.   mm in width after it enters a muscle fiber.
fiber.  It
There are eight recognized species and has a spear-like, burrowing anterior tip. TheTh e
three genotypes under the genus Trichinella. digestive tract of a mature larva encysted in a
Trichinella spiralisis the most
important cause muscle fiber  resembles
 resembles that of the adult worm.
of trichinellosis in humans, and is the species The reproductive organs, at this stage, are not
that is most adapted to domestic and wild   yet fully developed but even then, it is already  

isigtsh.e T 
 p mr iocshtinweil d  bountedthes p
l aelbyr idt iosvtir ,i b etchiesr  ahmanodn,g
 poec  iIbnleT 
 poss b tor 
ri  cideinnetl il f ay tihnef fe  scetxioonf , tthhee  ph
hin oasstit(ei.e.,
phar 
wild animals in Asia, Europe, Northern humans, rats, dogs, cats, pigs, bears, foxes,
Africa, and Western Africa, although it can walruses, or any other carnivore or omnivore)
also infect domestic pigs. T. britoviis the 2nd serves as both the final and intermediate host by
most common Trichinella species affecting harboring both the adult and the larval stages.
humans. Trichinella nativa infects primarily Infective larvae are usually encysted in the
wild carnivores in the frigid zones of Asia, North muscle fibers
fibers of
 of the host (Plate 3.31).  
America, and North Eastern Europe. Other
species that have been known to cause human
hum an
trichinellosis include T. murrelli, T. nelsoni, T.
 papuae, and T. pseudospiralis
pseudospirali s.
Parasite Biology 

The adult male, which measures 0.62 to  

1.58 mm by 0.025 to 0.033 mm, has a single
testis located near the posterior end of the body,
and is joined in the mid-body by the genital
tube which, in turn, extends back to the cloaca.
The posteriorly-located cloaca has a pair of
caudal appendages and two pairs of papillae.
The adult female measures about 1.26 to 3.35 Plate 3.31. Trichinellaspiralislarvae in musc
mu scle
le
(Courtesy of the Department of Parasitology,
mm by 0.029 to 0.038 mm, and has a single
UP-CPH)
ovary which is situated in the posterior part of  
 

CHAPTER 3: Nematode Infections   185 

The infective encysted larvae enter the After a few days, the female worm deposits
host through ingestion of raw or insufficiently larvae in the mucosa. The larvae penetrate the
cooked meat. The cysts are digested in the mucosa, pass through the lymphatic system into
stomach, and the larvae excyst either in the the circulation, and finally into striated muscles
stomach or in
then burrow thethe
into small intestine. The
subepithelium larvae
of the villi (Figure 3.14).After
and develop. In theabout
muscles, the larvae
3 weeks, theygrow
start
where they undergo four molts. Maturation  to coil into individual cysts. Encapsulation is  
takes about 2 days, and adult worms begin
beg in to completed 4 to 5 weeks after infection. The larva
mate 5 to 7 days post infection. The female in the cyst remains viable for many years. The
 produceseggs that grow into larvae in its uterus.   average lifespan of the encysted larva is about 5  

Figure 3.14. Life cycle of Trichinellaspiralis

 

186   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

to 10 years, and can survive for up to 40 years in dyspnea, dysphagia, and difficulty in chewing.
humans. In humans, calcification of the collagen Occasionally, there is paralysis of the extremities
capsule in the infected muscle cell and the larva and splenomegaly. In severe cases, there may be
may occur. This process may be observed 6 to gastric and intestinal hemorrhages.  

12 months after
destruction infection
or death andlarva.
of the may lead to the Larval
can result inmigration
pericardialinto
pain,the heart muscle
tachycardia, and
electrocardiogram
electrocardiog ram abnormalities. Pericardial 
Pathogenesis and Clinical Manifestations   effusion, congestive heart failure, and other
The severity of symptoms depends on chronic heart abnormalities have also been
the intensity of infection. Patients with light observed. Neurological complications, which  
infection, i.e., harboring up to 10 larvae, are are caused by small subacute cortical infarcts,
usually asymptomatic, while patients with may occur in chronic infections. Meningitis
moderate infection (50-500 larvae) show and meningoencephalitis may also develop.
symptoms. Infection with a few hundred In heavy infections, ocular disturbances,
larvae can result in gastroenteritis, diarrhea, diplegia, deafness, epileptiform attacks, and
and abdominal pain approximately two days coma may occur. In the convalescent phase,
 post infection.
infection . Infection
Infectio n with 100 to 300 larvae fever, weakness, pain, and other symptoms
may lead to symptomatic trichinellosis, while start to abate. Full recovery is expected since
since
more than 1,000 to 3,000 larvae can result in trichinellosis is a self-limiting disease. However,
However,
severe disease.   protean neurologic signs arising from brain
Clinical manifestations vary depending on   damage may persist. 

tahr e  sdtiavgiedeodf  tihnet p
o atr har seitee p alecloyy:n: denittieor nics
. Thhaseecs,li niacm ecPtirr o  ngsn. oD
inf ec siseaitshgiosoudn, ceos  p
pem
m lyeeixnce p
ciaolnly mtildin
 phase, invasion phase, and convalescent
convales cent phase. cases of heart failure, encephalitis, or other
These correspond to the stages of: (a) incubation complications
complications such as pneumonia or septicemia.
and intestinal invasion, (b) larval migration Low-grade or absent peripheral blood
and muscle invasion, and (c) encystment and eosinophilia is indicative of poor prognosis.  
encapsulation. 
Diagnosis 
Symptoms in the enteric phase may
resemble those of an attack of acute food The most definitive diagnostic examination
 poisoning,
 poisoni ng, including
inclu ding diarrhea
di arrhea or constipati
co nstipation,
on, is the demonstration of the larva through
vomiting, abdominal cramps, malaise, and muscle biopsy. Muscle biopsy is done through
nausea. During the invasion phase, the histological examination of 0.2 to 0.5 g of
migrating larvae and resulting metabolites lead muscle tissue. Digestion of muscle samples with
to immunological, pathological, and metabolic  pepsin and hydrochloric
hydrochlo ric acid can also be done
reactions.Inflammatory reaction to the infection to determine the number of larvae per gram
results in eosinophilia, which results in the
th e of muscle, or to isolate larvae for molecular
release of histamines. Histamines, serotonins, characterization. The digestion technique,
 bradykinins,
 bradykin ins, and prostagland
pr ostaglandins
ins contribute
cont ribute to
to however, is limited to muscle larvae that are
an increase in vascular permeability, resulting about 10 to 12 days old (about 2-3 weeks post
in tissue edema. The cardinal signs and infection) since younger larvae may bedestroyed
symptoms of trichinellosis include severe  by the digestion fluid. 
myalgia, periorbital edema, and eosinophilia.  Non-specific
 Non-speci fic laboratory
labor atory tests
test s to detect
Other typical signs and symptoms include eosinophilia, muscle enzymes (creatine
high remittent fever and chills, headache,   phosphokinase,
 phosph okinase, lactate
lact ate dehydrogenase,
dehyd rogenase, and
an d  
 

CHAPTER 3: Nematode Infections   187 

myokinase), and total IgE in serum may be children 2 years and older, albendazole should
useful in diagnosis. An algorithm for the  be given at 10 mg/kg body weight. A treatment
diagnosis of individual cases is shown in Table cycle may be repeated five days after the initial
3.4.  cycle in case of severe infection. Thiabendazole
Thiabendazole

Table 3.4. Algorithm for the diagnosis of the

is no longer
drug used  due to its associated adverse
reactions.
probability of acute trichinellosis in humans   Supportive treatment through analgesics  
and antipyretics is commonly used to control
symptoms. Corticosteroids may be given with
anthelminthics to control hypersensitivity
conjunctivitis, subungual hemorrhages,
reactions to the larvae, and may also be given 
to treat acute vasculitis and myositis.  
Epidemiology 

Trichinella infections in humans have

already been documented in 55 countries
worldwide. There are about 10,000 cases
reported each year, 0.2% resulting in mortality.
The diagnosis of trichinellosis is very Human trichinellosis occurs wherever meat
unlikely in the occurrence of only one symptom is a part of the diet. Outbreaks have been
from group A, B or C. Trichinellosis may be   reported in Argentina, Bosnia-Herzegovina,
Bosnia-Herzegovina, 
r uo s pmecgtr eodupinAthoer   ptwr r eosef nr coemogf f  r onu p 
f fsr   p one
 pntdom
e   sBy,ma p C
Thainila,nFdr ,anTcuer ,kLeayo, s,UR  ainane,iiaaU
kor m
ai  bpaeikni,stSawn,edaennd,
, Sz  p
from group C, while a diagnosis is probable Vietnam. Trichinella infection has never been
when there are three group A and one group documented in a small number of island
C symptoms. Diagnosis is highly probable in countries, including the Philippines.  
the presence of three group A and two group Trichinellosis is primarily a zoonosis.
C symptoms. A diagnosis is confirmed in case Humans get infected after ingestion of raw
of three group A, two group C, and one
on e group or insufficiently
insufficiently cooked
 cooked meat from infected
D symptoms; or any of symptom from group animals. The infection is usually maintained in
A or B, and one from group C and one from a pig-to-pig or pig-to-rat-to-pig cycle. 
group D. 
Prevention and Control 
Currently, enzyme-linked immunosorbent
Currently,
assay (ELISA) is recommended
recommended for the diagnosis Health education is an important
of trichinellosis. Confirmation of ELISA- component of prevention and control
 positivee samples may be done through
 positiv throug h Western   measures against this parasitic infection. It
 blot technique.
techn ique. Latex agglutinatio
aggluti nationn technique
techniqu e is recommended that meat be cooked at a  
may be utilized for rapid (<1 hour) confirmation minimum of 77°C (170°F). Freezing is another
of trichinellosis.  way to kill larvae. Storage at – 15°C
15°C for 20 days
Treatment  or – 
or – 30°C
30°C for six days is suggested. Smoking,
salting, or drying meat is not effective. Other
The treatment of choice for trichinellosis control measures include regular animal
is mebendazole 5 mg/kg body weight daily, or monitoring (meat inspection or detection of
albendazole 15 mg/kg body weight per day circulating antibodies), keeping pigs in rat-free
in two divided doses, for 10 to 15 days. For    pens, and
and proper
proper disposal
disposal of suspected carcasses. 
 

188   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

References  Gottstein B, Pozio E, Nockler K. Epidemiology,

diagnosis, treatment, and control of
Beaver PC, Jung RC, Cupp EW. Clinical
trichinellosis. Clin Microbiol Rev. 
 parasitology.
 parasitology. 9th ed. Philadelphia:
Philadelphia: Lea and 2009;22(1):127 – 45.
45.
Febiger; 1984. 
Blaga R, Durand B, Antoniu S, Gherman C, Murrell
PozioKD,
E. Lichtenfels RJ, Zarlenga
The systematics DS,
of the genus
Cretu CM, Cozma V, et al. A dramatic
Trichinella with a key to species. Vet 
itnr iccr heiansellionsitshien iR 
ncoim hean
deannciea  of vehr utm  past 25
Parasitol. 2000;93(3-4):293 – 307.
307. 
 Nockler K, Kapel CM. Detection and
years: impact of political changes and surveillance for Trichinella
Trichinella: Meat inspection
regional food fo od habits. Am A m J TropTrop Med Hyg. and hygiene, and legislation. In: Dupouy-
2007;76(5):983 – 6.
6.  
Camet J, Murrell KD, editors. FAO/
Dupouy-Camet, J, Bruschi F. Management
WHO/OIE guidelines for the surveillance,
and diagnosis of human trichinellosis. In: management, prevention and control
control 
Dupouy-Camet J, Murrell KD, editors.
of trichinellosis. Paris (France): World
FAO/WHO/OIE guidelines for the
Organisation for Animal Health Press;
surveillance, management, prevention and 2007. p. 69 – 9
98.8. 
control of trichinellosis. Paris (France): Pozio E. World distribution of Trichinella spp.
World Organisation for Animal Health
infections in animals and humans. Vet
Press; 2007. p. 37 – 68.
68.
Parasitol. 2007;149:3 – 21.
21.
Goldsmi th R, Heyneman D. Tropical
Goldsmith Tropical medicine
medicine
and parasitology. Connecticut: Appleton
and Lange; 1989.
 

CHAPTER 3: Nematode Infections   189 

 Ani 
sak isspp.
Winifreda U. de Leon  

nisakids are nematode parasites of whales, ingestion by marine mammals, the 3rd stage
dolphins, porpoises, walruses, seals,   larvae molt twice and develop into adult worms.  
sea lions, and other deep marine mammals. Pathogenesis and Clinical Manifestations  
Like any nematode, anisakids have elongated
vermiform bodies without segmentation. They Humans may ingest the 3rd stage larvae
have a complete digestive tract, and the sexes are  from raw or improperly cooked infected fish.
separate. Although they are parasites of marine The 3rd stage larvae, however, do not develop
mammals, they can cause gastrointestinal into the adults in the human gut. Larval
infections and allergic reactions in humans infection with anisakids is called anisakiasis
with the consumption of raw and undercooked or, more recently, anisakidosis. It may result
squid and fish containing the 3rd stage larvae in gastric and intestinal pathology. A second
of the parasite. Commonly involved
involv ed infective manifestation of morbidity brought about  
species are Anisa
 Anisakis
kis simplex and Pseudo
simplex  Pseudoterran
terranova
ova  by the
the parasites is an alle
allergic
rgic reaction
reaction to the
decipiens. Related species include Contracaecum chemicals secreted by the worms. 
sp. and  Hysterothylaci um sp. 
 Hysterothylacium Ingested larvae invade the submucosa  
of the stomach or the intestines, resulting in
Parasite Biology 

The adult worms embedded in the gastric dieemaonr dr hdaegteacahn.dH

h inoflwam er a, tiif fo  tnh.eT pheenleatr r vaateiom
evm n aiys
wall of the marine mammal host discharge deep, a tumor-like granuloma surrounded by
unembryonated eggs into the sea. The 1st stage inflammatory cells and eosinophils will develop.
larvae that develop inside the eggs molt into the Gastric anisakidosis is usually less acute and less
2nd stage larvae that hatch out of the egg. The
T he exudative than the intestinal form.  
free swimming 2nd stage larvae are ingested by Gastric anisakidosis has an acute
micro-crustaceans,
micro-crustaceans, where the 3rd stage larvae  presentation, occurring within 1 to 12 hours
develop. Going up the predatory food chain, after ingestion of infective larvae. Most
the third stage larvae are transported to various  patients complain of severe abdominal pain
 paratenic hosts,
h osts, like squid and
an d several species
speci es accompanied by nausea and vomiting. The
of fish.
fish. Usually,
 Usually, the 3rd stage larvae are more acute symptoms may eventually subside, with
concentratedd in fish viscera but may occasionally
concentrate vague but persistent abdominal pain and
 be found in the fish
fish muscles
 muscles (Figure 3.15).  intermittent bouts of nausea and vomiting.
The 3rd stage larvae of Anisa
 Anisakis simplexx are
kis simple Occasionally, the larvae may be regurgitated.
milky white in color, measuring 19 to 36 mm Symptoms may be mistaken for peptic ulcer
in length, with a long stomach, and a blunt disease, cholecystitis, or even gastroenteritis. 
tail with mucron, and are referred to as Type I When the larvae pass into the intestines, a
larvae. Other species of Anisakis have third stage
 Anisakis severe eosinophilic granulomatous response may
larvae with shorter stomachs and blunt tails, and occur 1 to 2 weeks following infection. Intestinal
are called Type II larvae. The 3rd stage
s tage larvae anisakidosis usually mimics appendicitis,
of Pseudo
 Pseudoterranovaare yellowish brown in color
terranova Crohn’s disease, intestinal obstruction, or
measuring 25 to 50 mm in length. Following   diverticulitis. 
 

190   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Outside of these more common locations, When the oropharynx is involved,

involved, the
the larvae have been found invading the  presentation
 presentati on is commonly known as “tingling
oropharynx, esophagus, and colon. This throat syndrome.” 
condition is referred to as ectopic anisakidosis. 
 

CHAPTER 3: Nematode Infections   191 

Acute allergic reactions have been reported There have been reported cases from Egypt as
in anisakidosis, when biochemical substances well. The condition is more common in the
are released by the parasites into the flesh of the coastal population of these countries due to the
host fish. Urticaria, asthma, conjunctivitis, and consumption of raw and inadequately cooked
contact
workersdermatitis have been
in fish and marine observed
products among
processing fish. Indocumented.
 been the Philippines,
  anisakidosis has not yet
factories and are forms of occupational  Considered to be high risk for anisakidosis  
hypersensitivity.  are fish dishes such as Japanese sushi and an d
Diagnosis 
sashimi, pickled anchovies, gravlax, salted and
smoked herring, and possibly fish bagoong as 
Anisakidosis should be highly suspected well as fish
fish  kinilaw
kinilaw in the Philippines. Salting,
if there is a recent history of eating raw  marinating, pickling, smoking, and other curing
or improperly cooked fish or squid prior techniques are effective against some foodborne
foodborne
to the acute onset of symptoms. Through   pathogens, but not for anisakid
anisakid larvae. 
gastroscopic/endoscopic
gastroscopic/endoscopic examination, the larvae Several species of marine fish and
can be visualized and removed for identification. cephalophods (squid) have been found to be
Intestinal anisakidosis is more difficult to infected with anisakid larvae. Mostly involved
establish, and may be diagnosed only after are the Pacific/Atlantic cod, Pacific  halibut, red
surgery. Serological procedures
procedures to detect specific snapper, mackerel, eels, salmon, and anchovies.
antibodies have been employed with good In the Philippines, anisakid larvae have been
results, such as enzyme-linked immunosorbent   found in blue mackerel scad ( galunggong 
 galunggong ),
), but 

ayST(E).LISA),  and  r adioaller gosorbent  test 

ssA
(aR 
(R  tohe b per esevasloe ncael. aIndf edctendsietyeellsof (  ppthal 
 b p al eo sl)ar hvavees b
e em
ens
found in Cebu, Mactan, and Leyte.  
Treatment 
The increasing number of cases is believed
The main approach is to mechanically to be due to multi-factorial causes. Deep
remove the larva using endoscopic forceps. sea marine mammals are currently being
It is strongly recommended that endoscopic  protected. Therefore, there has been an
removal be done early to avoid invasion of increase in the population of the definitive
the gastric submucosa. Corticosteroids have  hosts. The worldwide distribution of the
 been used in cases of allergic anisakidosis but anisakid nematodes may result in widespread
clinical trials have not been performed. A contamination of marine fish  and squid. The
fish and
 possible therapeutic
therape utic benefit  from albendazole increasing popularity of the consumption of
for intestinal anisakidosis has been reported sushi and sashimi globally may also contribute
in Spain.  to the increase in cases. 

Epidemiology  Control and Prevention 

Human anisakidosis is not a very common In order to best control and prevent
infection, but it has been reported from all anisakidosis, marine fish, squid, and
over the world. In Asia, the majority of reports shellfish must be thoroughly cooked prior
have come from Japan and Korea, while in to consumption. For raw or undercooked  
Europe, human cases have been identified    preparati ons, fish an
 preparations, andd shellfish must undergo
und ergo
in the Netherlands, France, Germany, Italy,  blast freezing atat – 
 – 35°C
35°C for at least 15 hours.
Spain, and the United Kingdom. It has also Freezing at – 
at – 20°C
20°C for 7 days has also been
b een
 been reported in North and South America.   found to be effective. Furthermore, raising the 
 

192   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

awareness of both producers and consumers of Kliks MM. Anisakiasis in the western United
 potentially
 potential ly infectious products
pro ducts through
throug h health States: four new case reports in Calufornia.
education may be helpful.  Am J Tr
Trop
op Med Hyg. 1983;32:526.  
Oshima T. Anisakiasis — is
is sushi bar guilty? 
References 
Parasitol
Pacios Today.J,1987;3:44.
E, Arias-Diaz Zuloaga J,  Gonzalez-
Amato Neto V,Amato JG, Amato
Amat o VS. Probable
recognition of human anisakiasis in  Armengol J, Vil larroel P, Balibr ea JL.  
Brazil. Rev Inst Med Trop Sao Paulo.
Pau lo. Albendazole for the treatment of anisakiasis
Albendazole
2007;49(4):261 – 2.
2.   ileus. Clin Infect Dis. 2005;41(12):1825 –  
Audicana TM, Kennedy MW. Anisak
 Anisakis
is sim
simplex
plex 6. 
from obscure infectious worm to inducer Petersen F, Palm H, Cuzi MA. Flesh parasites
of immune hypersensitivity. Clin Microbiol of fish
fish in
 in Central Philippine Waters. Dis
Rev.. 2008;21(2):360 – 7
Rev 79.
9. Aquat Org. 1993;15:81 – 6 6..
Jueco NL, Bobis TA , Ramirez LM. Seasonal Sakanari JA, Mckerrow JH. Anisakiasis. Clin
 prevalence and density of Anisakis larvae Micro Rev. 1989;2:278.  
in fish (galunggong) sold in public Velasquez CC. Resume of findings on  Anisakis
 Anisakis  
markets in Manila. J Philipp Med Assoc. larvae. Philipp Zool Soc. 1976;4:17.  
1971;47:467 – 76.
76. 
 

CHAPTER 3: Nematode Infections   193 

Toxocaracan s
i Toxocaracat i
Ernesto C. Balolong, Jr., Winifreda U. de Leon  

oxocariasis is a zoonotic disease which may Parasite Biology 

 present as a public health problem with  
stray dogs and
an d cats common in urban
urban areas. The T o xocar a cani s c m pletes  its lif e cycle in
dogs (Figur e 3.16). Following ingestion by the
disease is caused by larvae of Toxocara canis and canine hosts, the larvae emerge from the eggs,
Toxocaracati , roundworms found in dogs and
cats, respectively. When infective eggs of these
these 
 penetrate the gut wall, and migrate into various
tissues, where they encyst. In younger dogs,
roundworms are ingested by humans, larvae the larvae, after hatching, migrate through the
are released and penetrate the intestinal wall
circulatory system to the lungs and trachea.
then migrate via the veins into the
th e liver and the They eventually are coughed out,
o ut, swallowed,
rest of the body, where they remain as larvae.
and then develop into the adult stage in the
Toxocaraspp. belong
belo ng to the
t he Family
Fami ly Toxocaridae
Toxocaridae
small intestine in about 60 to 90 days after
and Order Ascaridida.
 

194   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

hatching. The female nematode produces Pathogenesis and Clinical Manifestations  

about 200,000 eggs per day which are shed
in an unembryonated form but become
At least three clinical forms of TC had been
infective after 2 weeks to several months.
reported in humans; these include visceral larva
migrants (VLM), ocular larva migrants (OLM),
These
optimalnon-infective eggsconditions
environmental need several weeks of
of
(10-35°C, and covert toxocariasis (CoTOX). VLM and
OLM, although presented as independent  
high soil humidity) to develop into infective 
embryonated eggs. The embryonated eggs are f estiastitohnes,r ecsaunltcoef xm
clinicTahl emVanLiM isti.gr ation
resistant to freezing, moisture, and extreme pH and subsequent death of the larvae in the
levels for at least a year. Meanwhile in older  
female dogs, the encysted stages are reactivated different tissues and organs, producing an
during pregnancy, and infect their puppies
intense inflammatory response manifested
through the transplacental and transmammary as eosinophilic granulomas. It is observed  
that the liver, lungs, central nervous system,
routes, with the adult worms establishing in the
t he
and eyes are the most sensitive. Wheezing is
small intestine. Eggs therefore are excreted both
a common sign of VLM, along with other
 by infected
infecte d lactating
lactatin g females and
an d puppies.
puppies . In
most adult dogs with some degree of acquired lower respiratory symptoms, more commonly,
immunity, the larvae undergo larval migration  broncho spasm. Progression
 bronchospasm. Pro gression to eosinophilic
eosino philic
 pneumonia and respiratory failure has been
to tissues and remain encysted. These encysted reported. Isolated reports describe diffused
larvae may then be released after predation.
Toxocaracanis can also be transmitted to non-  
non-cavitating pulmonary nodules and pleural
effusions. VLM is usually associated with liver  
cshaneeeei pd)mor am rr iaelds  b(ey.ge.a, r r rtha  bw boir tsm, sc,haincktse,na,ncdaot tlhe,er
cam enlargement and necrosis. Histopathology
soil-dwelling invertebrates through ingestion studies usually reveal granulomatous
granulomatous hepatitis.
The spleen is enlarged less often than the
of organs and muscle tissue of paratenic hosts
liver. Generalized lymphadenopathy is an
containing parasite egg or larvae.  
infrequent manifestation of toxocariasis.  
The cat roundworm, T. cati, follows a
life cycle similar to that of T. canis except that
Although infrequently involved, the heart
vertical transmission is attributed more to
can be affected, with myocarditis as the most
common problem. Loeffler endomyocarditis
lactation than transplacental transmission.
t ransmission. T. has also been reported. 
cati causes fewer cases of human infection than 
The OLM is expressed with signs and
T. canis, most likely because of the defecation
defecation
 patterns of cats, which make environmental
symptoms manifested in the eyes, and occurs
contamination less frequent. 
usually in children 5 to 10 years old. Unilateral
Humans are accidental hosts and become visual impairment sometimes with strabismus
is common. It is considered to be the result 
infected by ingesting infective eggs from  
contaminated soil. After ingestion, the eggs onoasltlya,llontheelaor cvualaisr
oa bf  lae vtoer yinf veawdelaar nvade.af Of eccctaasilm
hatch and release larvae that penetrate the structures. The most serious consequence is
intestinal wall and are carried by the circulation
to different organs (e.g., liver, heart, lungs,   the invasion
include of thepole
posterior retina. Other ocular
granuloma, lesions
peripheral
 brain, muscle,
mu scle, and eyes). While
Whi le the larvae do granuloma, or a condition similar to chronic
not develop into adult worms in the human
host, they can cause severe local reactions that endophthalmitis. Blindness is also common.  
may result in significant  damage. 
significant damage.
CoTOX is the medical term used to
t o identify
a less specific syndrome where most patients are 
 

CHAPTER 3: Nematode Infections   195 

asymptomatic
asymptomatic and eosinophilia is less frequent. In addition to the blood test, diagnosis of
Usual symptoms may include: coughing, toxocariasis includes identifying the presence
wheezing, chronic or recurrent abdominal pain, of typical clinical signs of OLM or VLM and a
hepatomegaly, sleep disturbances, headache,
headache, history of exposure to cats and dogs.  

malaise, and anorexia.

as polyarthralgias, Manifestations
monoarthritis, such
migratory Medical
to detect and imaging techniques can lesions
localize granulomatous be used
cutaneous lesions, and small-vessel vasculitis   due to Toxocara larvae. Abdominal ultrasound  
may coincide with VLM.   had shown multiple hypoechoic areas in
Another recognized syndrome i s   livers of patients who initially pre sented with
neurological toxocariasis, which is also one of hepatomegaly, eosinophilia, and a positive  
the causes of encephalitis. Larvae may migrate Toxocaraserology. Using computed tomography
to the brain, meninges, and may be found (CT), hepatic lesions appear as low-density
 present in the cerebrospinal
cerebrospi nal fluid (CSF). Solitary areas. In the CNS, more sensitive magnetic
mass lesions may be observed in the brain resonance imaging (MRI) may reveal granulomas
tissue causing seizures, static encephalopathy, appearing as hyper-intense areas. 
arachnoiditis,spinalcordlesions,optic neuritis, Treatment 
and eosinophilic meningitis, a form of aseptic
meningitis in which the WBCs in the CSF Visceral toxocariasis can be treated with
mainly consist of eosi
eosinophils.
nophils.  antiparasitic drugs such as albendazole or
mebendazole, usually in combination with
Diagnosis 
anti-inflammatory medications. Although  

diagnToosxeo b iaussies tihnehsuympantom
 bceacr ra ia is sdoif f f itcouxlotctaor iiaasis thoer sat p
m pya,tif ef onr tstw
  p oxaoticeanr tisasw
hoitshe t p isir tehconveeur r rwo  liothgoicuatl
are similar to the symptoms of other infections. toxocariasis or lung or cardiac complications,
Fecalysis cannot be utilized in the evaluation of anthelminthic treatment is mandatory. Patients
human toxocariasis as eggs are not produced or nflammatoryy reaction due  to
 presentingg with iinflammator
 presentin to
excreted. Definitive diagnosis of toxocariasis
to xocariasis is higher doses of praziquantel or albendazole
 based on the detection of larvae
larvae from biopsy were found to respond very well
w ell to steroids.
tissues, but this test is time-consuming and Treatment of oculartoxocariasis is morediffic
moredifficult
ult
difficult to
difficult  to perform. Currently, diagnosis is and usually consists of measures to prevent
commonly based on clinical and serologic  progressive damage to the eye. 
tests. Commercial immunoglobulin G (IgG)
Epidemiology 
enzyme-linked immunosorbent assay (ELISA)
kits are available wherein Toxocara excretory- Human toxocariasis is primarily a soil-
secretory (TES) antigens are used to detectd etect transmitted zoonosis with the infection
IgG antibodies against the larvae. In general, more commonly found in children than
however, these assays do not have adequate adults. Children are more at risk because  
specificity for use in countries where other soil- of their tendency to play in soil and exhibit  
transmitted helminths are endemic. Western geophagia or soil eating, thus increasing the
 blot is more specific but is unable to differentiate risk of toxocariasis. Cases are more frequently
 between new and old infections. Polymerase seen in children living in homes and in
chain reaction (PCR) has good results in the neighborhoods where dogs and puppies are not
Toxocaraspecies in tissues using
identification of Toxocara dewormed. Poor personal hygiene as well as
animal models.  consumptionn of inadequately washed vegetables 
consumptio
 

196   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

grown in contaminated gardens may result in minimize environmental contamination with

chronic low-dose infections. Less commonly, eggs. Adult cats and dogs should be treated
zoonotic toxocariasis infection is associated every 6 months. Treatment of female dogs is
with consumption of raw meat from potential also indicated after each estrus cycle.
 paratenic
rabbits. Thehosts, such chickens,
seroprevalence lambs or
of toxocariasis was Gardens should
contamination be fenced
by dogs to prevent
and cats. fecal
Vegetables
significantly higher among persons frequently   gathered from possibly contaminated gardens  
eating raw or undercooked liver than in persons should be thoroughly washed, and the
who ate their meat that has been sufficiently consumption of raw or undercooked meat that
cooked. This suggests that infective larvae can   could harbor Toxocaralarvae should be avoided. 
 be released
released from
from animal
animal tissues
tissues during
during digestion
digestion Hand washing, especially prior to eating, should
and subsequently cause human toxocariasis.   be encouraged, while hand to mouth activity
A number of surveys around the world should be discouraged at all times. Municipal
demonstrated high rates of contamination of ordinances to prevent pet dogs from entering
soil with the parasite eggs in parks, playground,  parks and playgrounds and to require owners
and other public places (10-30%). In western to remove their pets’
their pets’ feces
 feces from public areas
countries, the prevalence of infection in dogs should be considered.  
was reported to be about 25%, but may be
References 
as high as 30 to 60%. The prevalence of
infection tends to be lower in older animals Despommier D. Toxocariasis: clinical aspects,
in addition to well-cared pet dogs, and higher   epidemiology, medical ecology, and  

ipthoutnhed hdioghs.f eTchuinsdhitiygho pf  r T 
itnogsettr rha  eyr owr   p lecnaar r cae,
eov  xxaole 20
mo0l3ec
ec;1u6la(r 2)a:s2 p ts7.2C
 p6e5c  – 
–  .  lin  Micr o biol  R ev. 
and the increasing number of pet animals in Foyaca-Sibat H, Ibañez-Valdés L, Moré-
western countries explain the high level of soil Rodríguez J. Parasitic zoonoses of the
contamination with Toxocara eggs. Studies  brain: another challenger [Internet].
have also demonstrated contamination of soil Internet J Neurol. 2010 [cited 2012
samples taken from gardens of homes where a Jun 5];12 (2 ). A vailable from http://
clinical case of toxocariasis is found. Toxocara www.ispub.com/journal/the-internet-
eggs have been recovered from salads and other  journal-of-neurolog
 journal-of -neurology/volume-12
y/volume-12-number
-number
raw vegetables taken from such gardens.  2/parasitic-zoonoses-of-the-brain-another-
challenger.html#sthash.Bda
challenger.h tml#sthash.BdaBRnYK.dpbs
BRnYK.dpbs 
Prevention and Control 
Gomez L, Rueda T, Pulido C, Sanchez-Roman  
Toxocaracontrol aims to prevent infection J. Ocular toxocariasis. A case report. Arch
in both man and animals. Contamination of Soc Esp Oftalmol. 2007;83:49 – 5
52.
2. 
soil and environment can be greatly reduced Macpherson C, Meslin F, Wandeler A. Dogs,
with the control and capture of stray dogs and zoonoses and public health. New York:
cats, cleaning up feces from soil and pavements, CABI Publishing; 2000. 
closing of potentially contaminated areas  Magnaval JF, Glickman L, Dorchies P, Morassin  
to animals and children, and implementing B. Highlights of human toxocariasis.
strategic anthelminthic treatment of dogs Korean J Parasitol. 2001;39(1):1 – 111.
1.  
and cats. As dogs and cats are the sources of Mohamad S, Azmi NC, Noordin R.
infection, treatment program starting at 2 to Development and evaluation of a sensitive
3 weeks of age should be implemented, and and specific assay for diagnosis of human
repeated every 2 weeks until 12 weeks of age to   toxocariasis by use of three recombina
recombinant
nt 
 

CHAPTER 3: Nematode Infections   197 

antigens (TES-26,
(TE S-26, TES-30USM,
TES- 30USM, and
andTES- Vidal J, Sztajnbok, Seguroa AC. Eosinophilic
120). J Clin Microbiol. 2009;47(6):1712 –   meningoencephalitis
meningoe ncephalitis due to Toxocaracanis:
17. a case report and review of literature. Am J
Rai SK, Uga S, Kataoka N, Matsumura T. Trop Med Hyg. 2003;69(3):341 – 4
43.
3. 

Atlas of medical
(Japan): parasitology.
Kyokuseisya 1st ed.1996.
Co., Ltd.; Kobe 
 

198   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

CHAPTER 4  

Cestode Infections 

teinsif tr iendaal UC. e
InW destLoed
oen s 

Taenia spp.  
Taeniasaginata  
Taeniasaginata

aenia saginata is known as the beef

tapeworm of humans. It is cosmopolitan  
in distribution. Humans serve only as definitive
host and never as intermediate hosts. Therefore,
Therefore,
human cysticercosis due to this species does
not occur. The epidemiology, prevention, and
control of T. saginatawill be considered jointly
under the section on T. solium. 
Parasite Biology 

The adult worm inhabits the upper

 jejunum and can live for up to 25 years. It
derives nourishment from intestinal contents.
Adults measure 4 to 10 m in length and may
have 1,000 to 4,000 proglottids. There have
h ave
Plate 4.1. Taeniasaginatascolex
 been reports of worms reaching 25 m in (Courtesy of Department of Parasitology, UP-CPH)  
length. The cuboidal scolex measures 1 – 2 mm
in diameter and has four prominent acetabula
(Plate 4.1). vagina of T. saginata has a sphincter. Gravid
It is devoid of hooks or a rostellum.    proglottids are longer that they are wide (16-
Attached to the scolex is a short neck from   20 mm by 5-7 mm) and are most distal from  

which a chain of immature, mature, and gravid eocvka  (aPnldathe a4s.21)5.  T

twhiethnec toh2e 0utlear 
teur sali b
s dr aisntcehnedse.d
 proglottids develop. 
Mature proglottids are approximately The genital pores of proglottids are irregularly
square in shape,
and female and theyorgans.
reproductive containThere
maturearemale
two
alternate.
Taenia spp. ova are spherical or subspherical
subspherical
large lobes of ovaries and a median club-shaped in shape, measuring 30 to 45 µm in diameter
uterus. Follicular testes numbering 300 to 400 (Plate 4.3). The srcinal thin outer membrane
are scattered throughout the proglottid. The   surrounding the egg is rarely retained after  

198 
 

CHAPTER 4: Cestode Infections   199 

 pits. Inside the eggshell is the oncosphere or  

embryo provided with three pairs of hooklets.
The gravid proglottid contains 97,000 to 
124,000 ova. Annually, a worm may pass out 
594,000,000
apolysis ova.
and are Gravid
either proglottids
passed undergo
out with the feces  
or actively crawl out of the bowel to the external 
environment.
environme nt. With apolysis of gravid segments,
eggs are released and they remain viable in the
soil for weeks. 
Upon ingestion of the T. saginata eggs
 by cattle, the oncosphere is released. The
oncosphere actively penetrates the intestinal
mucosa, enters a venule, and is carried to other
 parts of the body. It typically enters a muscle
fiber  and develops into an infective stage called
Cysticercus bovis in 2 months. The cysticercus
is ovoidal, milky white, about 10 mm in
diameter, and has a single scolex invaginated
into a fluid-filled bladder. Humans readily
 become infected when these encysted
encysted larvae
larvae are 
iTnhge sltaer dvaf rr io smdigrr  aewsteodr   oim tpor 
u  p ro f f  ppther elymceoaotk,  eadn b
 dbetehf e.
scolex evaginates to attach to the mucosa of the
small intestines where it will become mature
Plate 4.2. Taeniasaginatagravid segment in about 12 weeks (Figure 4.1). Usually, only
(Courtesy of Department of Parasitology, UP-CPH)   one adult tapeworm is present in T. saginata
infections. The adult seems to be irritated by
alcohol, and passage of proglottids sometimes
results after a drinking bout. While humans are
suitable intermediate hosts for T. solium, they
are not for T. saginata. 
Pathogenesis and Clinical Manifestations  

Among patients seen at the Department

of Parasitology, College of Public Health,
University of the Philippines Manila, the most
common chief complaint is the passage of
 proglot tids or segments in the stool. T.saginata
 proglottids saginat a
Plate 4.3. Taeniaegg  causes mild irritation at the site of attachment.
(Courtesy of Department of Parasitology, UP-CPH)
Patients with taeniasis may experience non-
specific symptoms, such as epigastric pain,
 passage from the proglottid. The ova are vague discomfort, hunger pangs, weakness,
 brownis h in color,
 brownish color , with a thick
t hick embryophore
embry ophore weight loss, loss of appetite, and pruritus ani
which appears striated because of numerous   (perianal itching). Rarely, entangled proglottids  
 

200   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

may result in intestinal obstruction. Individual   Gravid proglottids are pressed or flattened in
T. saginata proglottids are actively motile  between two glass slides and are examined
and they have been documented to cause against the light. This will allow one to have
obstruction in the bile and pancreatic ducts, a rough count of the lateral branches from the
as well as the appendix. The sight of actively main uterus. Injection of India ink through
motile proglottids in the perianal area and in the genital pore will help one make an accurate
the undergarments may result in anxiety and   count of the lateral branches of the uterus 
distress.  (15-20 for T. saginata and 7-13 for T. solium).
Diagnosis 
Mature segments can be stained to demonstrate
the vaginal sphincter for T. saginata and the 
Specific diagnosis rests on identifying the accessory ovarian lobe for T. solium.
characteristic proglottids, eggs or scolex. The
characteristic Examination of the stool can be done for
first  specimen usually brought in by patients are the presence of eggs, but eggs are irregularly
the gravid proglottids, either single or in chains.  passed out with the stools. Concentration
They are passed out with the feces or may techniques like the formalin-ether/ethyl
 be recovered in the pat ient’s  undergarments. 
patient’s acetate concentration technique will be useful 
 

CHAPTER 4: Cestode Infections   201 

in increasing the chance of demonstrating the

eggs. Perianal swabs may also be useful because
eggs are left in the perianal skin as the gravid
segments squeeze out of the anal opening. 
Treatment 

The drug of choice is praziquantel.  

Praziquantel is given at a dose of 5 to 10 mg/
kg as a single dose for both adults and children.
It is not necessary to recover the scolex unless
species-specific diagnosis is needed. Criteria for
the cure include the following: (a) recovery of
the scolex, or (b) a negative stool examination
3 months after treatment. 
Taenia solium   Plate 4.4. Taeniasolium scolex 
(Courtesy of Department of Parasitology, UP-CPH)
Taenia solium is known as the pork
tapeworm of man. It has a cosmopolitan  branches of T. saginata. T . solium proglottids
distribution. Man may serve as both a definitive are relatively less active than the proglottids of  
host and an intermediate host. Therefore, both T. saginata. They have not been observed to
intestinal and tissue infections occur in man.  actively crawl about.
Parasite Biology 
oxhiemagtr ealvyid30, p0r 0o0gglltoott5i0d,0c0o0notavian.sThe gr avid
a ppr T
The adult worm inhabits the upper small  proglottids
 proglot tids also undergo apolysis to eventually eventuall y
intestines. Like other intestinal cestodes, it release eggs, which remain viable for weeks.
derives nourishment from intestinal contents of The eggs of T.solium are indistinguishable from
the host. It is shorter than T. saginata and has that of T. saginata. They measure 30 to 45 µm
less number of proglottids. The adults measure 2 and have a thick brown striated embryophore
to 4 m in length and may have 8,000 to 10,000 surrounding a hexacanth embryo. The eggs
 proglottids. The scolex of T. solium has four are ingested by hogs and the oncospheres are
acetabula, but it is smaller (1 mm) and more released in the intestines (Figure 4.2).
spherical that that of the beef tapeworm (Plate The oncosphere penetrates the intestinal
4.4). The scolex carries a cushion-like rostellum mucosa to typically encyst in muscles as
with a double crown of 25 to 30 large and small cysticercus cellulosae (Plate 4.5). The cysticercus
hooks, which are absent in T. saginata. After may be found in all tissues.Commonly, infected
the scolex, comes the neck from which the are the muscles, tongue, heart, diaphragm,
 proglottids develop. liver, spleen, and mesentery. Infected meat is
The general morphology of the proglottids  often called “measly pork.”
  pork.”  Upon ingestion of
resembles that of T. saginata. The difference improperly cooked infected meat, the larva is
lies in the presence of an accessory ovarian
ov arian liberated and the scolex attaches to the intestinal
lobe, the absence of a vaginal sphincter, and mucosa. Maturity is attained in approximately
the smaller number ofof follicular testes (100-  12 weeks from the time of ingestion of the
200) in the mature proglottid of T.soliu m. The
solium cysticercus. 
gravid proglottid characteristically contains 7 Man may also be an intermediate host of T.
to 13 lateral branches as opposed to 15 to 20    solium. Taeniaeggs are very resistant and when  
 

202   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Figure 4.2. Life cycle of Taeniasolium

Taeniasolium(cysticercosis)
(cysticercosis)
 

CHAPTER 4: Cestode Infections   203 

they are located in striated muscle and in the

 brain, but the subcutaneous tissues, eye, heart,
lung, and peritoneum may be involved. The
living cyst may produce inflammation.  Cysts
may
fluidsurvive up to
increases 5 years.
and Upon
there is death, cystic
a pronounced
tissue response to the parasite. The parasite is 
eventually calcified. 
Symptomatology is dependent on the  
number, size, and location of the lesion.
One of the most serious manifestations is
Plate 4.5. Cysticercus cellulosae from pork
neurocysticercosis
neurocysticercosis (NCC), which is considered
(Courtesy of the Department of Parasitology, as one of the most serious zoonotic diseases  
UP-CPH) worldwide. Cysticerci containing a scolex may be
found in the brain parenchyma or floating freely
in the ventricles. Cysticerci may also appear  
the eggs are ingested, development to cysticerci as large vesicular structures devoid of a scolex
ensues as it does in pigs. The oncosphere hatches and are usually located in the basal cisternal
in the duodenum, and spreads to different
spaces. NCC is divided into two general forms,
organs through the bloodstream. This results in  parenchymal
 parenchym al and extraparenchymal,
extraparen chymal, which, in
human cysticercosis. The mature cysticercus is turn, is further divided into subarachnoid or  
oval, translucent, and has an opaque invaginated  
scolex with four suckers and a circlet of hooks. meanif n
f egsittaitci,oinstr anvdenctor  lapr o,nadnidngs  ppm
r r ircr r  ue  s  p inanl.aCgelimniecnatl
It is usually encapsulated with adventitious
adventitious host depend on the form of NCC present in the
tissue. However, in the vitreous humor and in    patient. Focal neurologic deficits deficits are  are usually
the brain, it may be unencapsulated. A full size encountered in parenchymal NCC. They would
of 5 mm may be attained in 10 weeks.   depend on the location of the cysts. Focal or
Human infection with cysticercus cellulosae generalized seizures are observed when cysts
can be acquired through fecal-oral route by are located in the cortex. The subarachnoid
ingesting Taenia soliumeggs from contaminated form may lead to an aggressive form of NCC
food or drink. Individuals harboring the called racemous cysticercosis. In this form,
adult Taenia solium can infect themselves there is a proliferation of cysts in the base of the
(autoinfection) due to poor hygienic practice.   brain. This form has a poor prognosis. In the
Pathogenesis and Clinical Manifestations   intraventricular form, cysts are usually present
in the third or fourth ventricle and often lead 
 A. Intestinal infection 
infection 
to obstructive hydrocephalus. The spinal form
T.solium intestinal infection results in mild is rare. 
non-specific abdominal complaints. Unlike inT. The death of the larva leads to inflammation
inflammation  
ta infections, proglottids are not as active  
 saginata
 sagina of the affected region. Calcification is the end-
and, therefore, obstruction of the bile duct, result of the cellular reaction. Convulsions
 pancreatic duct, or the appendix is unlikely.   are the most common manifestations of
cerebral cysticercosis. Visual and motor
B. Cysticercosis  
deficits, headache, and vomiting may occur.
The cysticerci are often multiple and can Cerebrospinalfluid (CSF) tap results may show
develop in any organ ortissue. Most commonly,  an increased opening pressure, elevated protein, 
 

204   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

decreased glucose, and increased mononuclea

mononuclearr Ophthalmic cysticercosis can be diagnosed
cells. Half of the cases may present with through the visualization of the cysticerci using
CSF eosinophilia without peripheral blood ophthalmoscopy but the procedure may induce
eosinophilia.  movement and/or evagination of the scolex.
In the eyes, cysticerci are often retinal or Muscular and subcutaneous cysticerci are
subretinal in location. They may float
float freely
 freely usually palpable and can be recovered through
in the vitreous or aqueous humors. Vision   tissue biopsy for histopathologic processing.  
is usually affected due to chorioretinitis and Serologic tests include serum and CSF
vasculitis. Detachment of the retina has also enzyme-linked immunosorbent assay (ELISA)
 been reported. The patient may complain of   and electro-immuno transfer blot (EITB)  
intraorbital pain, photopsia, and blurring or or Western blot for specific IgG and IgM
loss of vision. anticysticercall antibodies. These tests
anticysticerca t ests have  
a sensitivity of 75 to 100% using a partially
par tially
Diagnosis 
 purified glycoprotein antigen to detect
 A. Taeniasis  antibodies. Dot-ELISA test is a very good
Specific diagnosis of taeniasis rests on
screening test for cysticercosis. It uses crude
antigen from the cysticerci obtained from
identifyingg the characteristic proglottids, eggs,
identifyin
or scolex as described in the T. saginata sub-
 pigs. Recent studies are looking
lookin g into the use of
section. 
antigen B of cysticercus cellulosae as a useful
adjunct in diagnosis. 
B. Cysticercosis  
Treatment 

 Neurocysticercosis
 Neurocyst icercosis may be suspected
suspe cted in  A. Taeniasis  
a patient coming from an endemic area with
epileptic seizures without associated systemic   The drugs of choice are praziquantel
symptoms. Concomitant infection with T. and niclosamide. Because of the theoretical
 solium adult occurs only in 25% of cases. If a  possibility of autoinfection and subsequent
 patient has subcutaneous
subcutaneous cysticerci
cysticerci concomitant
concomitant cysticercosis, treatment
treatment should not be delayed.
with neurologic symptoms, this provides Praziquantel is given as 5 to 10 mg/kg, single
 presumpt ive evidence
 presumptive evide nce for neurocysticer
neur ocysticercosis.
cosis. dose for both adults and children. Niclosamide
CSF abnormalities such as an elevated protein, is not available locally. Criteria for cure include
reduced glucose, and increased mononuclear the following: (a) recovery of the scolex, or (b)
cells may be seen. Computed axial tomography
to mography a negative stool examination 3 months after
(CAT) scans and nuclear magnetic resonance treatment. 
imaging (MRI) are useful for localizing
B. Cysticercosis  
cysticerci and evaluating the pathology before  
and aTf hter etr aer aetm
ther neet.main CAT scan p
 patter ns: (a) enattoief  N
ntaninagtehme  p
 pr eseM Cudlteipelen p
nt.CM or am
dsaor en tcheyf m l
a round low-density area without surrounding cystic lesions are treated by giving praziquan
praziquantel
tel
enhancement
dye, afterenhancement
(b) ring-like administration of injection
after contrast at a dose of 50 to 75 mg/kg divided into
three doses for 30 days or albendazole at a
of contrast dye, and (c) a small calcified  area
calcified area dose of 400 mg twice daily for 8 to 30 days.
within a cystic space. The first pattern shows a Corticosteroids are then given (either 80 mg
viable larva with no inflammation; the second, of prednisone or 10 mg of IM
I M dexamethasone)
a dead larva; and the third shows a dead scolex.   4 hours after the
th e last dose. Parenchymal 
 

CHAPTER 4: Cestode Infections   205 

forms presenting as cysticercotic encephalitis Taenia asiatica 

asiatica 
or those with massive parasitic infection are
Taenia asiatica, a third Taeniaspecies, has
given high dose corticosteroid therapy and
mannitol in cases of increased intracranial
 been reported in Taiwan, Korea, Thailand, and
Indonesia. This parasite was initially believed to
 pressure. Many experts do not recommend  be closely related to Taenia saginat
saginataa. In contrast
giving praziquantel or albendazole in these
to Taenia saginata, however, the cysticercus  
cases. For the subarachnoid form, some experts
experts 
recommend surgical removal of the lesions, loaf r  vaer ioa bf T 
leaeinnitaer amieadtiicaatewher oestf soutnhadt inintchlue dliever
 s

while others recommend albendazole therapy  pigs, cattle,

catt le, goats, wild
wil d boars,
boars , and monkeys,
mon keys,
in which albendazole is given at a dose of 10 to   hence the term cysticercus viscerotropica. The
15 mg/kg/day for 8 days. Although albendazole cysticercus has wart-like protuberances on the
therapy has been shown to have several benefits, external surface and contains an invaginated
there are reports of associated meningeal fibrosis scolex armed with vestigial hooklets. 
and hydrocephalus. Ventricular forms are best
treated with surgical removal of the cyst. 
The length of the adult
adu lt may vary
v ary between
between 4
to 8 m with 300 to 1,000 segments. Similar to
Ocular cysticercosis should be treated
Taenia saginata, the scolex is devoid of hooklets
surgically before praziquantel or albendazole  but there is a prominent
promine nt rostellum. The gravid
is given because ocular inflammation cannot
 be controlled
control led with steroids.
steroid s. Symptomatic
Sympto matic cysts  proglottids
 proglot tids have
hav e posterior protuberance
protub erance with
outside the CNS may be surgically removed.   11 to 32 lateral branches arising from the main
uterus. The mature segments, on the other
Epidemiology  hand, were found to carry a vaginal sphincter. 
The distribution of T.
T.solium and T.sagi
saginata
nata Due to the number of uterine branches and the
infections is highly related to the habit of eating  presence of vaginal sphincter,
sphincter , Taenia asiatica
may be misidentified
misidentified  as Taenia saginata. 
raw or improperly cooked meat. Abstinence A collaborative workwith Japanes
Japanesee scientists
from beef as part of the religious beliefs among was undertaken by the College of Public Health,
the Hindus prevent T. saginat a infections, while
saginata
University of the Philippines Manila. Gravid
among the Moslems, prevention of T. solium segments from six patients, identified
identified  earlier  
infections happens because of abstinence from as Taenia saginata were subjected to genetic
 pork. Both tapeworms have a cosmopolitan studies and the mitochondrial RNA of five  out
distribution, although T. solium is especially of the six samples were found compatible with
common in Slavic countries, Latin America, Taenia asiati ca. Further studies of this kind will
asiatica
Southeast Asia, China, and India. T. saginata establish the prevalence and the magnitude of
has high endemicity in Ethiopia and East Africa. the problem regarding this parasite.
It has also been reported in Japan,
J apan, Europe, In the Philippines, T. saginata infection is 
Australia, Canada, and the United States of
America.   of oar neicmoaml m
m inotenr m
theadniT 
at.e sohl iu
osmts ihnof ewcteivoenr . sShuor wv eyds
Maintenance of the life cycle in nature   that pigs are infected more than cows or cattle.
is dependent on the level of environmental
sanitation practiced in the area. Animal The overallareas.
in selected prevalence of taeniasis
In isolated foci, aisprevalence
only 0.56%
intermediate hosts, especially pigs should be of 11 to 15% for T. saginatahas been reported.
kept in pens to avoid access to human feces. Many of the identified  cases were adult males
identified cases
Contamination of the grazing fields with human who came from the Northern Luzon provinces,
feces favors infection of the intermediate hosts.   where eating raw or undercooked meat while 
 

206   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

drinking alcohol isa delicacy. Neurocysticercosis Eom KS, Rim HJ. Morphologic description of
has been reported in local literature. There has Taenia asiatica. Korean J Parasitol. 1993;
 been one report of ocular cysticercosis.  31:1. 
Flisser A. Neurocysticercosis in Mexico.  
Prevention and Control 
Parasitol Today. 1988;4:13l.  
Prevention and control of taeniasis may Garg RK. Medical management of
appear simple but may be difficult to implement.  neurocysticercosis.
neurocysti cercosis. Neuro India.
Thorough cooking of meat is a primary 2001;49:329 – 337.
337. 
measure. Freezing at – 
 – 20°C
20°C for 10 days kills the Mahmoud AA. Tropical and geographical  
cysticerci. Sanitary inspection of all slaughtered medicine companion handbook. 2nd ed.
 pigs, cows,
cows, and cattle should
should be done. Meat Singapore: McGraw Hill Book Co.; 1993.  
inspection should include examination of the McManus DP, Bowles J. Asian (Taiwan)
liver as well.  Taenia species or strain? Parasitol Today.
1994;10(7):273 – 275.
275.
References 
Jubelt B, Miller JR. Parasitic infections. In:
Arambuloo PV,
Arambul PV, Cabrera BD, Cabrera
Cabrer a MG. The Rowland LP, editor. Merritt’sNeurology.
use of mebendazole in the treatment of 10th ed. Philadelphia: Lippincott Williams
Taenia saginata taeniasis in an endemic and Wilkins; 2000.  
area in the Philippines. Acta Trop. Pawlowski ZS. Perspectives on the control of
1978;35(3):281 – 286.
286. Taenia solium. ParasitolToday. 1990;6(12):
Arambulo PV, Cabrera BD. Studies on the 311 – 313.
313. 

zoonotic
and cycle of Taenia
cysticercosis
saginatataeniasis 
in the Philippines. Int J  JHos.inAg cEasM
Quim e ,oC
f   osun bdceuB oauns oanC
taJn, eR  Ce br 
d Pc,er  ro r ra ssl
Zoonosis. 1976;3:77 – 108.108. cysticercosis treated with praziquantel.
praziquantel. Phil
Beaver PC, Jung RC, Cupp EW. Clinical J Microbiol Infect Dis. 1984;13(l):25 – 335.
5.  
 parasitology.
 parasitolo gy. 9th ed. Philadelphia:
Philadelp hia: Lea & Roberts LS, Janovy J. Foundations of
Febiger; 1984.   parasitology. 5th ed. Dubuque: Wm. C.
Belding DL. Textbook of parasitology. 3rd Brown Publishers; 1996.  
ed. New York: Appleton-Century Crofts; Strickland GT. Hunter’s tropical medicine
1965.  and emerging infectious diseases. 8th ed.
Bengzon AR, Perlas AP,Reyes VA.
V A. Cysticercosis Philadelphia: W. B. Saunders; 2000.  
cerebri in the Philippines. Acta Med Tsang VC, Brand JA, Boyer AE. An enzyme
enzyme
Philipp. 1965;27(l  – 
– 4):1.
4):1.  linked immunoelectrotransfer blot assay
Cabrera BD. Case report: Multiple infection and glycoprotein antigens for diagnosing
with adultTaenia solium. ActaMed Philipp. human cysticercosis ( T. solium). J Infect
1965;1(3):147 – 150.
150. Dis. 1989;159:50. 
Corona T,Lugo R,Medina
R,Medin a R, SoteloJ
SoteloJ. Single-day Urbina EC. Ocular cysticercosis. Phil J
 praziquantel
 praziquantel therapy for neurocysticercosis.
neurocysticercosis. Ophthamology. 1988;17(4):153 – 155.
155. 
 N Engl J Med. 1996;334:125.   White AC Jr. Neurocysticercosis:
Neurocysticercosis: a major cause
of neurological disease worldwide. Clin
Infect Dis. 1997;24:101 – 113.
113. 
 

CHAPTER 4: Cestode Infections   207 

Hymeno e
l pi 
snana
 

 ymenolepis nana , commonly known as Mature proglottids contain three ovoid

the dwarf tapeworm, is a cyclophyllidean   testes and one ovary in a more or less straight 
tapeworm and is the smallest tapeworm  pattern across
acro ss the segment.
seg ment. When segments
infecting humans. It is found worldwide, mainly  become gravid, the testes and the ovary
among children. The parasite
parasite is the only human disappear while the uterus hollows out and
tapeworm, which can complete its entire life    becomes filled
fi lled with
wit h eggs. Gravid
Gra vid segments
segment s 
cycle in a single host, indicating that it does not (Plate 4.7) are separated from the strobila and
require an obligatory intermediate host. Man disintegrate as they pass out of the intestines,
intestines,
can harbor both the adult and the larval
l arval stages releasing eggs in the stool. 
of the parasite. Eggs are spherical or subspherical, colorless
or clay-colored, measuring 30 to 47 µm in
Parasite Biology 
diameter (Plate 4.8). The oncosphere has a thin
The adults, with a delicate strobila outer membrane and a thick inner membrane
measuring from 25 to 45 mm in length and 1 with conspicuous bipolar thickenings, from
mm in width, reside in the ileum. The scolex each of which arise four to eight hair-like polar
is subglobular with four cup-shaped suckers  filaments embedded in the inner membrane. 

lateed  4w.i6t)h.  aTshiner geleisr oawr oetf rr 2a  c0tat b

(aPr r m  bole30r oYs-tsehllau pmed Tahsesseed  eogugtsi,nhtoow
 p theev er n, vdir ioenim nte.diately  once
mem
hooklets. The neck is long and slender. The The life cycle has a dual pathway: a direct 
anterior proglottids are short and the posterior and an indirect development (Figure 4.3). In
ones are broader than long. No more than 175 the direct cycle, the host ingests eggs, which
to 220 segments compose the entire length of hatch in the duodenum. The liberated embryos
the strobila. The proglottids measure 0.15 to   penetrate the mucosal villi and develop into the  
0.3 mm in length and 0.8 to 1.0 mm in width.
The genital pores are found along the same side
of the segments. 

Plate  4.6. Hy 
meno p s spp. sco le x
 l epi  Plate 4.7. Hymenolepisspp.gravid segment
(Courtesy of the Department of Parasitology
Parasitology,, (Courtesy of the Department of Parasito
Parasitology,
logy,
UP-CPH)  UP-CPH) 
 

208   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

infective cysticercoid
cysticercoid larvae. After 4 to
t o 5 days,
the larvae break out of the villi and attach to
the intestinal mucosa to develop into adults.
Infection through the indirect cycle is usually via
the accidentalhosts
intermediate ingestion
like theofrice
infected arthropod
and flour  beetles
 beetles
(Tenebrio sp.) and sometimes through fomites,  
water, or food contaminated with the larvae.
The cysticercoid larvae are released and will
eventually develop into the adult tapeworms  
in the intestines of the host. It takes 20 to 30
30
days from the time of ingestion for the eggs to
appear in the feces. Eggs are optimally viable
immediately after discharge from the bowel.
Plate  4.8.  Hy 
meno p snana e gg 
 l epi  gg   Autoinfection can occur through the fecal-oral
(From World Health Organization. Bench Aids for
the diagnosis of intestinal parasites. Geneva,
route or within the small
s mall bowel. Oncospheres
Switzerland: WHO Publications; 1994.) from the eggs are released and they invade the
host villi to start a new generation.
 

CHAPTER 4: Cestode Infections   209 

Pathogenesis and Clinical Manifestations   of abnormal cysticercoids in the viscera that

occurs in an immunosuppressed condition. This
Symptoms are generally produced because may suggest that the parasitic condition should
of the patient’s
the patient’s immunological
 immunological response to
 be treated first before any immunosuppressive
the parasite. Light worm burden is generally
asymptomatic.
asymptomat ic. Clinical
C linical manifestations include therapy is given. 
headache, dizziness,
dizziness, anorexia, pruritus of nose  Epidemiology 

anaidn,a pnualsl,or d,iaar nr hdew
 p a,eivgohmt iltoinssg., Sa b
omdoemininf eaclted  Hymenolepis nana is found in areas with
children are restless, irritable, and exhibit sleep warm climate like Southern USA, Latin
disturbances.. Rarely, convulsions occur. Heavy
disturbances America, the Mediterranean, EastAsia, and the
infections may result in enteritis due to necrosis Philippines. An estimated 20 million people are
and desquamation of the intestinal epithelial infected. Transmission generally occurs where
cells. With time, regulatory immunity may there is poor sanitation, overcrowding, and
limit or eventually clear the H. nana populat
 population
ion  poor personal
personal hygiene practices.
practices. Direct contact
contact
spontaneously. Infections in children resolve  plays an important
importan t role because the eggs cannot
spontaneously in adolescence. 
survive long outside the host. It is a familial and
institutional infection common in orphanages,
Diagnosis  day care centers, and mental institutions.
Prevalence varies from 5 to 20% among children
Specific diagnosis is made by demonstration
and young adults in communities where direct
of the characteristic eggs in the patient ’s stool.
 patient’s
transfer of embryonated eggs from hand to  
In light infections, concentration of the stool
specimens on alternate days is useful.
usefu l. Generally, ocecwur o.r m is also f ound among
thhis lhikuemlyantota p
mouT
 proglottids are not recovered because they
the mice and less frequently among the rats. The
undergo degeneration prior to passage with
species in mice and rats is considered to be a
stools. 
distinct subspecies called  H. nana
nana var . fraterna.
 fraterna
Treatment  Although very rare, some strains were found
to be infectious to humans as well. Therefore,
Th erefore,
The drug of choice is praziquantel given infected mice and rats may be potential sources
as a 25 mg/kg single
si ngle dose. Praziquantel causes of infection. 
vacuolization and disruption of the tegument In the Philippines, two independent
in the neck region. The drug dosage for surveys of Jueco in 1983 and Cross, et al. in
hymenolepiasis is higher than that for taeniasis 1984 showed a prevalence of less than 1%
1 % in
 because of the
the relatively resistant
resistant cysticercoids humans. Infection among rodents was found
in the intestinal tissue. Stool examination to be low as well. 
may be repeated after 2 weeks. Treatment is  
usually repeated after 2 weeks to cover for the
worms emerging from the remaining viable 
Prevention and Control 
The life cycle involves a single host and
cysticercoids.
cysticercoi ds. Treatment
Treatment is considered successful transmission is direct. This makes prevention
if stools are negative for H. nana eggs at one more difficult, especially in crowded dwellings.
month post treatment. Nitazoxanide (500 mg Emphasis should be placed on personal hygiene
orally for 3 days) may be used as an alternative and environmental sanitation. Infected cases
drug. 
should be thoroughly treated. Rodent control
Evidence in mice has shown that infection must be observed. Food must be properly stored
is influenced
influenced by by steroid treatment or by T-cell
and protected from possible infestation with
deprivationn allowing an increased multiplication 
deprivatio grain beetles. 
 

210   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Hymeno e
l ps
i di 
mi nuta
 

dimin uta is a cosmopolitan

 ymenolepis diminuta
 parasite primarily of rats, hence the  
common name, rat tapeworm. Accidental
human infections do occur resulting in
hymenolepiasis. Aside from morphological
differences with  H. nana,  H. diminuta differs 
in that it requires an intermediate host.
Parasite Biology 

The adult tapeworm is larger than H.nana.

The worm measures about 60 cm in length.
The scolex differs from that of the H. nana by
having a rudimentary unarmed rostellum. As in   Plate  4.9. Hy 
menoe
l  p
 psi d 
i mn t  e gg
i ua
 H. nana, mature proglottids are broader than (Courtesy of the Department of Parasitolog
Parasitology,
y,
they are long, and the arrangement and number UP-CPH) 
of sexual organs are similar: three ovoid testes  
ancr dososntehoevsaer gyminenatm
.  Tor heeo pr r loegsslosttr iadigs hatr  pe alattr egr enr Pathogenesis and Clinical Manifestations  

and may reach 0.75 mm in length and 3.5 mm The worm burden in rodents is relatively
in width. The genital pores are unilateral. Each low.In man, the highest number recorded is 19
gravid proglottid contains a sac-like uterus filled worms. Clinical manifestations are minimal and
with eggs.  non-specific.
non- specific. The life span of  H. diminuta in
 H. diminuta eggs are circular, about 60 to humans is short, which possibly explains why
80 µm in diameter and are bile-stained (Plate human infections are usually light. 
4.9). The oncosphere is enclosed in an inner
Diagnosis 
membrane, which has bipolar thickenings but
lacks the bipolar filaments. The hooklets usually Diagnosis is based on the identification
have a fan-like arrangement. of eggs from the stool. H. diminuta eggs are
The gravid proglottids separate from the distinguished from H. nana
nana eggs by their more
main body of the worm, disintegrate, and release circular shape, larger size, and lack of bipolar  
eggs into the feces. Eggs, when ingested by a
wide range of adult and larval insects like fleas, fi s. oAr 
anladmtehnetm oleosg,ythoef  wt heoslceowleoxr  maisy b
 tpthim
 p  ebx p
e uelsled
 beetles, cockroaches,
cockroaches, mealworms,
mealworms, and earwigs, as an aid in diagnosis.  
develop into the infective cysticercoid larvae.
When these infected insects are ingested by the Treatment 
rat or accidentally ingested by man, the larva is Treatment is similar to Hymeno lepis nana.
 Hymenolepis
released and develops into the adult worm in Praziquantel is given as a 25 mg/kg single dose. 
about three weeks (Figure 4.4). 
 

CHAPTER 4: Cestode Infections   211 

Epidemiology  Prevention and Control 

Human infection occurs worldwide but Prevention and control measures include
is more common among children than adults rodent control, elimination of the insect
in poor communities with rat infestation. It intermediate hosts, protection of food, especially
 probably occurs by accidental ingestion of grain the precooked cereals from such insects, sanitary
 beetles infesting dried grains,
grains, dried fruits,flour,  disposal of human waste, and treatment of  

athnedPcheir rle i  ppa pls.inIens,  p
apr neavtaiole su.rr v dd eiim
lenwceidoef   H 
H  y ionf ur t aatw
 m s ians human cases. 
found to be about 8%.
 

212   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

D
 p
i yd
i 
l i 
umcan inum
 

ipylidium caninum is a very common

intestinal parasite of dogs and cats  
worldwide, especially in dog populations where
ectoparasitism is high. Dipylidiasis in humans is
accidental and is observed to be more common
in children than in adults. 
Parasite Biology 

The pale reddish adult worm measures

10 to 70 cm in length. The scolex is small
and globular with four deeply cupped suckers
and a protrusible rostellum, which is armed
with one to seven rows of rose thorn-shaped
hooklets. The proglottids are narrow with two
sets of male and female reproductive organs and
 bilateral genital pores, earning for this parasite 
tThhee cgor m ido pnr ongalm
avm avle- pthoer esidzet a pnedwsohr a p
otetiddsohu b me.
of a pumpkin seed and are filled with capsules
or packets of about 8 to 15 eggs enclosed in
an embryonic membrane (Plate 4.10). When
the gravid segments are detached, they either
migrate out of the anus or are passed out with
the feces. The ova are released by contraction Plate 4.10. Dipylidiumcaninumgravid segment
of the proglottid or by its disintegration outside (Courtesy of the Department of Parasitology,
Parasitology, 
the host. Eggs are spherical, thin-shelled with a UP-CPH)
hexacanth embryo (Plate 4.11). 
Some of the egg capsules may remain in
the fur of the host or in the host’s resting place.
Here, larval fleas
fleas ingest
 ingest the ova as they feed
on epidermal debris. Among the intermediate
hosts are the larval stages of Ctenocephalidescanis
Ctenocephalidescanis
(dog flea), Ctenocephalides felis (cat flea), and/
or Pulex irritans (human flea). Trichodectescanis
irritans
(dog louse) has also been involved. In the body
cavity of the arthropod, the hexacanth embryo
develops into the cysticercoid larvae, which is
able to survive
survi ve theflea’s development. Whenthe
insect is ingested by mammalian hosts (dogs, Plate 4.11. Dipylidiumcaninumegg cap
capsul
sule
e
cats, humans), the cysticercoid is liberated and (Courtesy of the Department of ParasitoParasitology,
logy,
UP-CPH) 
 becomes an adult in 3 to 4 weeks (Figure 4.5). 
 

CHAPTER 4: Cestode Infections   213 

Pathogenesis and Clinical Manifestations   of the egg capsules is not recommended, since
the gravid proglottids do not disintegrate in the
Infection is rarely heavy and symptoms intestines but in the environment. Egg capsules
are minimal. Slight intestinal discomfort,
are rarely recovered from the stool.  
epigastric pain, diarrhea, anal pruritus, and
allergic reactions have been reported. While Treatment 
most patients are asymptomatic, moderate
eosinophilia has been reported. 
Treatment consists of praziquantel
prazi quantel 5 to 10
Diagnosis  mg/kg given as a single dose.  
Epidemiology 
Diagnosis is established upon recovery
of the characteristic gravid proglottids passed Human infection is rare but has been
reported in European countries, USA, Argentina,
Argentina,
out singly or in chain. Gravid proglottids may
crawl out of the anus, and may be passed out
Rhodesia, China, and the Philippines. Infants
and very young children are usually infected
involuntarily. Proglottids should be pressed
 because of their close contact with their pet
or flattened between two glass slides for  
cats and dogs. Likely, transmission could have  
examination. Stool examination for the presence 
 

214   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

occurred through hand to mouth contamination city of Manila showed a prevalence of 5.19 to
or accidentally swallowing the arthropod hosts 36.0%, while dissection of dog and cat fleas for
when hugging and kissing the animal. Parents cysticercoids showed only a prevalence of 2.4%. 
usually observe the presence of actively motile
Prevention and Control 
 proglottids in children feces or underwear.
underwear.  
Adults are not commonly infected possibly Periodic deworming of pet cats and dogs is
 because of age tolerance against the parasite.   recommended. Insecticide dusting of dogs and  
In the Philippines, the first human infection cats are effective against fleas. The potential
was reported
report ed as early as 1912 by
b y M.P.
M.P.Mendoza- danger of playing with pets must be included
Guanzon in a child. Surveys of dogs in the   in the health education of children.  
 

CHAPTER 4: Cestode Infections   215 

Rai 
l 
etn
i 
i agar isoni

aillietina garrisoni belongs to the Family membranes: an outer elongated membrane

Davaineidae. Railli
 Raillietina
etina madagas
madagascarie nsis 
cariensis and an inner spherical membrane. The gravid  
was first reported by Garrison to be present in segments detach from the rest of the strobila
an adult Filipino in 1911. R. garrisoni
garrisoni was later  by apolysis and may be passed out in the feces.
documented in three children. It is generally
gen erally The segments are motile, white, and appear like
 believed that the species are identical.
identical. Tubang
Tubangui
ui  grains of rice when passed out with the feces. 
further showed that this was a common Gravid segments may be ingested  
tapeworm of rats. Almost all human infections  by the insect intermediate host, the flour
in the Philippines have involved children.    beetle Triboliumconfusum (Plate 4.13). The
Parasite Biology 
development from egg to thet he cysticercoid larval
stagetakesabouttwo weeks.Infectedinsectsare
The tapeworm (Plate 4.12) is about 60 accidentally ingested and the cysticercoid larva
cm in length with a minute, subglobular scolex attaches to the intestinal villi to develop into an
with four acetabula. The rostellum is armed adult in about 8 weeks. Direct infection does
with two alternating circular rows of 90 to not occur if eggs are ingested by the mammalian
140 hammer-shaped hooks. Several rows of   host; therefore, there is no autoinfection in R. 
 R. 

 p theedr osvtaer lylusm
s pr iongelsoattlisdo  shuar sr oau bnidlo b u.rr Tohuenm ur ye
deadt b
 garrisoni infection.
36 to 50 ovoid testes. The genital pore opens
on the side near the anterior lateral border of
the segment. The fully gravid proglottids are
about 2 mm in length containing 200 to 400
egg capsules with one to four spindle-shaped
eggs. The oncosphere is enclosed in two thin 

Plate 4.13. Flour beetle (Tri

(Triboliumsp
mspp.)),,th the
e
intermediate host of Rai  l 
entiagar ison i
(Courtesy of Dr. Lilian de las Llagas)

Pathogenesis and Clinical Manifestations 

Patients are usually asymptomatic. Children

are brought for medical consultation when
 proglottids are passed out with their feces.  
Diagnosis 
Plate 4.12. Railetinagarrisoni adult (Courtesy
of the D epartment of Parasitology,
Parasitology, UP-CPH)  Diagnosis is made by finding the
characteristic
characteristic proglottids or ova in stools. 
 

216   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Treatment  Cross JH, Basaca-sevilla V. Biomedical surveys

in the Philippines. Manila (Philippines):
Sometimes, long strobila or the complete US Naval Medical Research Unit-2; 1984.  
tapeworm may be expelled by the child
Hinz E. Human helminthiases in thePhilippines.
spontaneously
spontaneo
may usly without
be given to expeltreatment. Praziquantel
the worm.   Berlin: Springer-Verlag; 1984. 
Jueco NL. Raillietina
 Raillietina(A rat tapeworm): Infection
I nfection
Epidemiology  in young children in the Philippines. Acta
 Raillietina
 Raillietina garrisoni is a common intestinal
garrisoni
Med Philipp. 1975;11(2):49 – 5 50.
0.
Jueco NL. Rodent diseases transmissible to man.  
cestode of rodents in the Philippines. More
Acta Med Philipp. 1983;19:164.  
than 20 human infections have been reported
Macpherson C, Meslin F, Wandeler A. Dogs
in Philippine scientific journals. Almost all zoonoses and public health. New York:
infections occurred in children who were below CABI Publishing; 2000. 
three years of age. In Thailand, thefirst
the first  human McPhee SJ, Papadakis MA, Tierney LM,
case was reported as early as 1891, and another editors. Current medical diagnosis &
11 cases, all children, were reported from 1960 treatment. 46th ed. McGraw-Hill; 2007.  
to 1970. Raillietina infections have also been Mirdha BR, Samantray JC. Hymenolepis nana:
reported in Tokyo, Taiwan, Australia, Ecuador, A common cause of paediatric diarrhoea
and North Iran. In all cases, the infections were in urban slum dwellers in India. J Trop
Tr op
confined to children usually 5 years and below.  
Pediatrics. 2002;48:331 – 44..
Prevention and Control  Rai SK, Uga S, Kataoka N, Matsumura T.

Elimination of rodents from households, laas no)f : m

(Jta p
A eiasyr r asC
K eydoikcuals p . o be
it ol.o, gLyt.d1.;st1e9d9.6K 
 proper storage
storag e of grain products, and sanitary
san itary Schenone H. Praziquantel in the treatment of  
waste disposal can help preventive infection.   Hymenolepisn
 Hymeno ana infection in children. Am  
lepisnana
References  J Trop Med Hyg. 1980;20:320.
Wijesundera M. The use of praziquantel in
Arambul o PV, Sarmiento RV. The occurrence
Arambulo human infection with dipylidiasis. Trans
Trans R
of some important zoonotic helminths of Soc Trop Med Hyg. 1989;83:383.
the gastrointestinal tract of dogs in Manila. World Health Organization. Bench Aids for the
World
Phil J Vet Med Assoc. 1970;2:3 – 1
11.
1.  diagnosis of intestinal parasites. Geneva:
Geneva:
Biswash H, Arora RR, Sehgal S.
S . Epidemiology World Health Organization; 1994.  
of Hymenolepis nana infection in a selected
 Hymenolepis Yutuc LM. The cat flea
flea unknown
 unknown to sustain
rural community. J Commun Dis.  the larva of Dipylidium caninum from the
1978;10:170. Philippines. Phil J Sci. 1968;97(3):285. 
 

CHAPTER 4: Cestode Infections   217 

D
 p
i hyo
l botr iuml 
atum
 

iphyllobothriumlatum belongs to
t o the Order
Ord er found at the midventral common genital pore.
Pseudophyllidea. It is just one of the 13
1 3  The dark, rosette-like, coiled uterus located  
species of Diphyll
 Diphyllobothriumthat infects human.
obothrium in the middle of the gravid proglottid extends
It is commonly called the fish tapeworm or the from the ootype and opens through a uterine
 broad tapeworm. Diphyllobothri
Diphyll obothriasis
asis refers
r efers to  pore in the midventral
midvent ral line behind the common
the intestinal infection with the adult worm.  genital pore. A symmetrical bilobed ovary is  
 present at the posterior third of the proglottid
Parasite Biology 
immediately above the Mehlis’ gland. From
The adult tapeworm measures from 3 to 10 the common genital pore, the vagina extends
m in length and may have 4,000 proglottids. up to join the oviduct and the vitelline duct.
The scolex is spatulate and measures 2 to 3 Unlike in Taeniidae, the proglottids of  D.
mm in length by 1 mm in diameter (Plate latum disintegrate only when the segment has
4.14). It has two bothria or sucking grooves, completed its reproductive function. 
which are located dorsally and ventrally. The With distention of the uterus, the uterine
neck is long and attenuated, and is followed  pore is relaxed an
and
du unembryonated
nembryonated ova are
 by immature proglottids. The terminal
terminal four-  discharged from the proglottid. Approximately
Approximately 
fif ths of  the wor m is com posed of  matur e and 1(P,0la0t0e,04.1
005)ovaar emuasyu b
alleyr yeelellaosw
edisdha bilr yo.wTnh,ewoivtha
gr avid pr oglottids. The matur e  pr oglottid has a
longer width than its length. It measures 2 to 4 a moderately thick shell and an inconspicuous
mm in length by 10 to 12 mm in width, and operculum. Opposite the operculum is a small
contains one set of reproductive organs. The knob-like thickening. The mean size of the eggs
testes are located in the dorsolateral part of the is 66 by 44 µm, with a range of 58 to 76 µm in
 proglott id. The vas efferens converge
 proglottid. conv erge to form length and 40 to 51 µm in width.  
a vas deferens and this enlarges into a seminal The ova complete their development in
vesicle and terminates in a muscular cirrus  water and release the free-swimming coracidium 

Plate 4.14. D p

i hylobothriumlatumscolex Plate 4.15. Dp
i hyo
l  bothru l tumegg
i ma
(Courtesy of the Department of Parasitology, (Courtesy of the Department of Parasittology,ology,
UP-CPH) UP-CPH) 
 

218   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

(Figure 4.6), a ciliated embryo, which is ingested intestinal wall and reaches maturity in about
 by freshwater copepods ofthe generaCyclops and 3 weeks. 
omus. A procercoid larva develops in the
 Diaptomus
 Diapt
Pathogenesis and Clinical Manifestations  
copepod. The procercoid measures 550 µm and
still retains the three hooklets in the cercomer, Infections are usually limited to one worm,
a caudal attachment organ. The copepod is although there have been reports of mechanical
in turn ingested by fish.
fish. The
 The procercoid larva obstruction due to a large number of worms.  
migrates through fish tissues and develops into   Infected individuals may show no signs of  
aT phlee pr olecr eor coer idcoliadr vlar ivna tohr es pmaur sgcalnesum
andmveiasscuer eas. ease. Some, however, may ex per ience ner vous
distur  bances, digestive disor der s, a bdominal 
20 mm or more and appears glistening, opaque discomfort, weight loss, weakness, and anemia.
white, and unsegmented. Fish with theinfective theinf ective Symptoms may be due to absorbed toxins or
 plerocercoidd larva is ingested raw by a definitive
 plerocercoi  by-products
 by-prod ucts of degenerating
degenerati ng proglottids,
proglo ttids, or due
host like man, dog, cat, and other mammals. to mucosal irritation. 
Carnivorous fish may serve as paratenic or  D. latum infection results in
transport hosts as well. Among fish intermediate hyperchromic, megaloblastic anemia with
hosts are perch, trout, salmon, and pike. In the thrombocytopenia and leukopenia. Anemia
definitive host, the plerocercoid attaches to the   seen in diphyllobothriasis
diphyllobothriasis is typically similar to 
 

CHAPTER 4: Cestode Infections   219 

that seen in Vitamin B12  deficiency and could b
 b e for the propagation of the infection in the
mistaken for
f or pernicious anemia. Worms
Worms located endemic areas.
high up in the jejunum compete effectively with  D. latum is prevalent in the temperate zones
the host f or  the Vitamin B12 in the diet. If  wor ms where the population has a habit of eating raw
are pushed further down the intestines, with
w ith or improperly cooked fish.
fish. It
 It is present in the
treatment, anemia is relieved. The vitamin B12 Baltic countries, Switzerland, Romania, and
content of D. latum is approximately 50 times   the Danube Basin. In Asia, it can be found in 
that of T. saginata.  Russia, Turkistan, Israel, Northern Manchuria,
Manchu ria,
Diagnosis  and Japan. In the Americas, it can be found in
Chile, Argentina, and in some North American 
Residence in or travel to an endemic area,
ar ea, states and Canada. Seven human infections have
a raw-fish diet, and a pernicious type of anemia  been documented in the Philippines. 
may be suggestive of diphyllobothriasis.
diphyllobothriasis. Definite
Prevention and Control 
diagnosis is made on finding the characteristic
characteristic
operculated eggs or on occasion, proglottids in All freshwater fishes should be thoroughly
stools. Sometimes, proglottids may be vomited. cooked. Freezing for 24 to 48 hours at a
Since eggs are usually numerous, direct fecal temperature of  – 18°C
18°C kills all plerocercoids.
plerocercoids.
smears usually suffice. The Kato technique is In endemic areas, prevention should center
also useful in demonstrating eggs.  on controlling the source of infection, proper
To differentiate anemia due to disposal of sewage and marketing of fish.
fish. 
diphyllobothriasis from pernicious anemia,  
References 
eoxf af m er rnr  eisceinouce
r eienahtyiodnr oocf htlhoer r igcasatcr iidc  jjius icuesef f our lt. hPe p ces Beaver PC, Jung RC, Cupp EW. Clinical
anemia is associated with achlorhydria.    parasitology.
 parasitolo gy. 9th ed.
ed . Philadelphia:
Philadel phia: Lea &
Treatment  Febiger; 1984. 
Belding DL. Textbook of parasitology. 3rd
The drug of choice is praziquantel as 5 to ed. New York: Appleton-Century Crofts;
10 mg/kg single dose. The criterion for cure is 1965. 
recovery of the scolex in feces
f eces after treatment. Garcia EY, Africa CM.
C M. Diphyll
 Diphylloboth
obothrium
rium latu
latum
m
If the scolex is not recovered, a repeat stool (Linnaeus, 1758) Luhe, 1910 in a native
examination
examinati on is done
d one after 3 months
month s to be ce
certrtan
anii Filipino. Phil J Sci. 1935;57:451 – 7
7..
that the patient is no longer infected.   Hinz E. Human helminthiases in thePhilippines.
Epidemiology  Berlin: Springer-Verlag; 1984. 
Mahmoud AA. Tropical and geographical
Human infection is dependent on the medicine companion handbook. 2nd ed.
 presence of human or animal definitive hosts, Singapore: McGraw-Hill Book Co.; 1993.  
the presence of suitable intermediate hosts,  Neva FA, Brown HW
HW.Basic clinical
clinical par
parasit
asitolo
ology.
gy.
dietary habits, and amount of pollution of fresh 6th ed. Connecticut: Appleton & Lange;
waters. The preference for eating raw fish and
the lack of sanitary toilet facilities contribute 1994.
Roberts LS, Janovy J. Foundations of
to the transmission of the parasite. Although  parasitology. 5th ed. Dubuque: Wm. C.
other mammalian hosts like dogs, cats, and Brown Publishers; 1996.  
 bears exist as reservoir
reservoir hosts, man is responsible
responsible 
 

220   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Extraintestinal Cestodes
Vicente Y. Belizario, Jr., Francis Isidore G. Totañes

Ech inococcusspp.  The larval stage, called hydatid cyst, is

formed through central vesiculation. Cysts  
uman echinococcosis is regarded as an may grow at rates ranging from 1 to 5 cm in
H emerging/re-emerging zoonotic disease. 
The disease is caused by the larval stage of
diameter per year. Numerous protoscolices
may be found within the cyst. Development is
coccus spp., which is acquired when the
 Echinococcus
 Echino completed when the cysts in tissues are ingested 
eggs of this parasite are ingested. Echinoc
 Echinococcus
occus  by carnivores or omnivores. Once inside the
spp. belong to the Family Taeniidae, Order definitive host, the protoscolices evaginate and
Cyclophyllidea. There are six recognized attach to the intestinal wall where they develop
 Echinococcus species, four of which are of into adults. They reside in the small bowel of
 public health importance.
import ance. E . granu losus and E .
 granulosus the host where they start to release eggs that are
multilocularis cause cystic echinococcosis and then passed out in the stool (Figure 4.7).  
alveolar echinococcosis, respectively, while  E . The hydatid cysts usually measure 1 to 7
vogeli and E . oligarthrus both cause polycystic
polycys tic cm in diameter.The
diameter.T he cyst has an outer
out er laminated
laminated
echinococcosis. E.  E. multil
multilocularis, E . vogeli, and 
ocularis, hyaline layer and an inner nucleated germinal
 E. oligarthrus are less common because their life   layer. Protoscolices may be found in brood  
cycles are sylvatic.   yesr u, leasn,dwdhaiuchghctoer ntcayisntsow
claa p nlhyicthhear geer m
e pilnicaal s
Parasite Biology 
of the mother cysts. The brood capsule may
The adult worm inhabits the small rupture and release protoscolices. Protoscolices
Protoscolices
intestines of canines. It measures 3 to 6 mm in and brood capsules that lie free in the cyst are
length and possesses a pyriform scolex, a short referred to as hydatid sand (Plate 4.16). Up
neck, and three proglottids: one immature, one to 2 million protoscolices may be found in an
mature, and one gravid. The scolex is typically average cyst. 
taeniid in that it has four acetabula. It is armed Pathogenesis and Clinical Manifestations  
with 30 to 36 hooks. The gravid proglottid is
usually the widest and the longest proglottid. Pathology
Pathol ogy of human cystic echinococcosis
echino coccosis is
The uterus is midline, with lateralevaginations, caused by
b y the developi
d eveloping
ng larval
larv al cyst in the tisuses
and is filled
filled with
 with eggs which resemble those of the intermediate host. The most common
of other taeniid worms. Eggs may be released and most important site of involvement is the
inside or outside
outsid e the host.  liver, which is seen in 70% of the cases, 85%
The eggs are swallowed by suitable of which is located in the right lobe. The lungs
intermediate hosts, such as goats, horses, camels, are involved in 20 to 30% of cases, while other
and sheep.
the eggs. Man
The may
eggs alsoinaccidentally
hatch the duodenumingest
and organ involvement,
orbit, make up 10% such as theCysts
of cases. brainare
andless
the
release oncospheres thatpenetrate the intestinal commonly seen in the spleen, kidneys, heart,
wall of the intermediate host. The oncospheres  bone, and central nervous system. The cysts
then migrate into the mesenteric venules which of E. granulosus are called unilocular hydatid
lead them to various organs and tissues where cysts, while those of  E. multilocularis are
they eventually lodge and develop into cysts.   considered alveolar cysts. As the unilocular cyst 
 

CHAPTER 4: Cestode Infections   221 

Figur e  4.7.  Lif e  c yc le  o f E c

c  hi no c o cc usspp.
(Accessed from 
from  www.dpd.cdc.gov/dpdx)
www.dpd.cdc.gov/dpdx) 

develops, inflammatory reactions may occur in

surrounding tissues. Recent studies in mice have
shown that infection with E. granulosus
granulosusleads to
down-regulation of inflammatory cytokines,
resulting in local immunosuppression. This
may be the mechanism by which the parasite is
able to escape host cell-mediated response.Mass
effect brought about by the enlarging cyst results  
iun odr egr agno iam
tr  aihrr  m
 po p y aendt atsistshueneicgr h b
 obsoisr .ing tissues
Although echinococcal infection may be 
acquired
the liver during
and thechildhood, infections
lungs are often involving
diagnosed in
adults due to the cysts’
cysts’ slow
 slow growing nature.
Plate 4.16. Hydatid sand Simple or uncomplicated cysts may not produce
(Courtesy of the Department of Parasittology,
ology,  any symptoms, and patients may harbor the
UP-CPH) cysts for years. In some cases, the presence of
the cyst is only an incidental finding
finding  in routine  
 

222   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

radiographic examination. Once symptoms of residence in an endemic area, and close

start to occur, they typically reflect
reflect  the site of association with dogs are important in the
involvement. Hepatic cysts are mostly found diagnosis of echinococcosis. The World
in the inferior right lobe, and may present as Health Organization (WHO) has developed
hepatic enlargement, right epigastric pain or a standardized classification system for hepatic
 jaundice.Abdominalcysts may cause discomfort cysts detected by ultrasonography, as shown in
when the cysts are large enough. Cysts may  Table 4.1. 
rupture from coughing, muscle strain, trauma, Positive serologic tests, such as the use
aspiration, and operative procedures. When this of indirect hemagglutination (IHA), indirect
happens, the protoscolices, brood capsules, and  fluorescent antibody (IFA) test, and enzyme 
enzyme  
daughter cysts may metastasize and reach other immunoassays (EIA) are adjunct to radiologic  
tissues to develop into secondary cysts after 2 to
Table 4.1. WHO classification for hepatic
8 years. Cysts may also become intrathoracic if echinococcal cysts 
they are located in the superior lobe of the liver
and rupture into the thoracic region. Classification Description
The rupture of a hepatic cyst into the
 biliary duct produces a characteristic triad
of findings: intermittent jaundice, fever, and
eosinophilia. Peribronchial
Peribronchial cysts may discharge
into a bronchus and result in sudden coughing
accompanied by allergic symptoms. Sputum
Sputum 
anady bciotsnotaf inmf er m
m thr ya b
o b nelo. oIndv, omlvuecm
use,nhtyodf athide br 
 fluaiidn,
may cause increased intracranial pressure and
Jacksonian epilepsy. Renal involvement may
cause intermittent pain, hematuria, kidney
dysfunction, and hydatid material in the urine.
Secondary infection of the cyst may also occur.
Bacteria may enter the cyst and lead to pyogenic
abscess formation. A patient with this condition
usually presents with chills and high fever. 
Secondary cysts and infected cysts result in
higher mortality rates. In cases where primary diagnosis. These tests have sensitivities ranging
cysts rupture, serious anaphylaxis may result from 60 to 90% and may
m ay be used as screening
from a large amount of hydatid material tests. Although serology may be useful to
entering the bloodstream. Multiple cysts on   confirm presumptive diagnoses, one must  be  
different major organs, seen in 20 to 40% of wary of false positive findings which may occur
infected individuals, may consequently result if the patient is infected with other helminths,
in
themultiorgan failure.
cyst is the most Intrabiliary
common rupture of 
complication, or if he has
negative a chronic
finding,  on theimmune
im mune
other disease.
hand, will alsoA not
followed by suppuration.   completely rule out the disease since some cyst
Diagnosis 
carriers have undetectable antibodies. Serology
may have a relatively high sensitivity (80-100%)
Radiographic findings and/or and specificity (88-96%) if cysts are located in
ultrasonography, combined with a history   the liver, but when cysts are located in other  
 

CHAPTER 4: Cestode Infections   223 

organs such as the lungs and the brain, the worldwide. Cystic echinococcosis is most
serodiagnostic reactivity is lowered, decreasing
serodiagnostic  prevalent in countries in the temperate
the reliability of this adjunctive diagnostic test. zones, such as southern South America, the
Detection of IgG antibodies to hydatid cyst Mediterranean, southern and central parts of
fluid-derived native or recombinant antigen B Russia, Central Asia, China, Australia, and
subunit, through ELISA or immunoblot, is the  parts of Africa. Reemergence of cases have
current gold standard serology for human cystic   been reported
reporte d in Bulgaria, where the incidence  
echinococcosis.  of echinococcosis in children increased from 
0.7 to 5.4/100,000 between the 1970s and the  
Treatment 
mid-1990s. Similarly, prevalence of infected
Surgical resection is still considered canines in Wales
Wales doubled between 1993 (3.4%)
(3. 4%)  
the preferred treatment for echinococcosis  and 2002 (8.1%).
 presenting with a large (>10 cm in diameter) Filipinos who have traveled to or worked
liver cyst, secondary infection, or cysts in in endemic areas may get infected. A 35-year
extrahepatic sites. Small (<7 mm in diameter), old Filipino overseas contract worker in the
isolated cysts, uncomplicated cysts, and Middle East presented with a right hilar mass
 patients with negative serology respond best to on routine chest x-ray. Thoracotomy
Thoracotomy showed a
chemotherapy with benzimidazole compounds. 10 cm by 6 cm cystic mass containing hydatid
Treatment with albendazole (10-15 mg/kg/ sand. Another Filipino overseas contract worker
day) or mebendazole (40-50 mg/kg/day)   from Iraq presented with a growing mass in
for a minimum of three months has been   the hip area. Biopsy results showed presence of  
d emir oantisotnr a,teind jetcot b
as p ivier .atPioer ncu(PtaAnIeR 
ioen,ef r f ee-cats p ou) s wyitdhatnido sa p
h nda.r eM
a p ntohr eisr teocr eynotf lyt,r avFeil i p
toinano ef enm le,ic
deam
technique may be indicated for patients with area, consulted her physician for neurologic
single or multiple cysts in the liver, abdominal symptoms. Histopathologic findings of tissue
cavity, spleen, kidney, or bones, who cannot obtained during neurosurgery also showed the
undergo surgery. This technique involves: (a)  presence of hydatid sand. 
ultrasound-guided percutaneous puncture, (b) Prevention and Control 
aspiration of substantial amounts of cystic fluid,
fluid,  
(c) injection of a protoscolicidal agent (e.g., Prevention is achieved by reducing the
95% ethanol or hypertonic saline) for at least 15 infected populations and by minimizing
minutes, and (d) re-aspiration. Treatment with opportunities for transmission. Regular testing
PAIR plus albendazole or mebendazole has been and quarantine, and treatment of dogs with
shown to have greater efficacy  and lower rates  praziquantel in endemic areas are important
of morbidity, mortality, and disease recurrence.
recurrence.  control strategies that have resulted in the
reductionn of echinococcosis cases. Tominimize
reductio
Epidemiology  transmission, dogs should not be allowed in
Cystic echinococcosis
echinococcosis is the most common slaughterhouses,
slaughterhouses, and refuse from these facilities
 presentation of echinococcal
humans, accounting for >95% ofinfection in
global cases, should be sterilized
education or properly
should include disposed. on
knowledge Health
the
with a burden of disease of about one million mode of transmission, and should emphasize
disability-adjusted life years (DALYs). There the danger of intimate contact with dogs. 
are approximately 2 to 3 million cases of  New strategies for the control
contr ol and prevention
preventio n
human cystic echinococcosis, and 0.3 to 0.5 of echinococcosis include vaccination of
million cases of human alveolar echinococcosis  livestock, which has been proven to provide  
 

224   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

>95% protection against E. granul osuss, as well

granulosu Ito A, Sako Y, Ishikawa Y, Nakao M, Nakaya  
as the development of more sensitive diagnostic K. Differential serodiagnosis of cystic
techniques for definitive
definitive and
 and human hosts.  and alveolar echinococcosis using ntrtive
and recombinant antigens in Japan.
 
References Southeast Asian
A sian J Trop
Trop Med Public Health.
Heal th.
Ahluwalia BK, Khurana AK, Gupta NC,   2001;32(Suppl2):111 – 5
5.. 
Mehtani VG. Hydatid cyst of the orbit.   Lightowlers MW, Flisser A, Gauci CG, Heath  
Philipp J Ophthalmol. 1989;18(4):145 – 6.
6. DD, Jensen O, Rolf R. Vaccinat
Vaccination
ion against
Akkiz H, Akinoglu A. Colakoglu S, Demirytirek cysticercosis and hydatid disease. Parasitol
H, Yagnrur O. Endoscopic management  Today. 2000;16(5):191 – 5 5..
of biliary hydatid disease. Can J Surgery. Mondragon-dela Pena C, Ramos-Solis S,
1996;39:287 – 92.
92.  Barbosa-Cisneross O, Rodriguez-Padilla
Barbosa-Cisnero Rodriguez-Padilla 
Budke CM. Global socioeconomic impact of C, Tavizon- Garcia P, Herrera-Esparza
Herrera-Esparza R.
cystic echinococcosis. Emerg Infect Dis.  Echinococcus granulosus down regulates
2006; 12:296 – 303.
303.  the hepatic expression of inflammatory
Canete R, Escobedo AA, Almirall P, Gonzalez cytokines IL- 6 and TNF alpha in BALB/c
ME, Brito K, Cimerman S. Mebendazole in mice. Parasite. 2002;9(4):351 – 1
16.
6.
 parasitic infections
infectio ns other than those caused Moro PL, Schantz PM. Echinococcosis:
 by soil-transmitte
soil-t ransmittedd helminths.
helmint hs. TransR Soc historical landmarks and progress in
Trop Med Hyg. 2009;103:437 – 42. 42. research and control. Ann Trop Med
Center for Disease Control and Prevention —   Parasitol. 2006;100:703 – 1
14.4.

[Inivtiesr inoento].f  P2a0r 1a1sit[iciD
D teidsea2s0e1s.2EcMhianr o3c]o.ccosis Mor r 
oevPiLew, .SIcnhtaJntIznf PecMt D
.  Eisc.h2in00o9co;1c3co:1s2is5: – 
  a33. 
Available from http://www.dpd.cdc.gov/
from http://www.dpd.cdc.gov/ Romig T, Dinkel A, Mackenstedt U. The
dpdx/html/Echinococcosis.htm    present situation of echinococcosis in
Craig PS, McManus DP, Lightowlers MW, Europe. Parasitol Int. 2006;55:S187 – 991.
1. 
Chabalgoity JA, Garcia HH, Gavidia Schantz PM, Gottstein B, Ammann R, Lanier
Cm, et al. Prevention and control of A. Hydatid and the Arctic. Parasitol Today.
cystic echinococcosis. Lancet Infect Dis . 1991;7:35 – 6.
6.
2007;7:385 – 94.
94. Wang Y,
Y, Bradshaw I, Rogan MT, Craig PS.
Dalisay JS. Pulmonary echinococcosis (a case Rapid dot-ELISA for the detection of
report). Chest Dis. 1985;14(4):148
1985;14(4):148 – 51.
51.   specific antigens in the cyst fluid from
Ito A, Wandra T, Sato MO, Mamuti W, Xiao
X iao human cases of cystic echinococcosis.
echinococcosis. Ann
 N, Sako Y, et al. Towards the international Trop Med Parasitol. 2002;96(7):691 – 44.. 
collaboration for detection,
d etection, surveillance World Health Organization. International
and control of taeniasis,
t aeniasis, cysticercosis
cysticercosis and classification of ultrasound images in cystic  
echinococcosis in Asia and the Pacific.   echinococcosis
echinococcosis for application in clinical
SoutheastAsianJTropMedPublicHealth.   and field epidemiological settings. Acta

2006;37(suppl 3):82 – 90.
90. Trop. 2003;85:253 – 6
61.
1. 
 

CHAPTER 4: Cestode Infections   225 

Spirometraspp. 
Winifreda U. de Leon  

 parganosis refers to the larval infection Parasite Biology 

with the plerocercoid larvae, also known 
as spargana, of pseudophyllidean tapeworms T e gr avi r ur so,gilnotctiodnstr oaf stS  p
have ahs pir al udte p
ir omet r a .
to the r oses p
tte
falling under the Genus Spirometra . There
uterus observed in  Diphyllobothrium sp.
are many species of Spirometra , but those
Spirometra eggs are operculated and immature,
i mmature,
commonly involved in human sparganosis are similar to those of  Diphyllobot
 Diphyllobothriu
hrium,
m, although
Spirometra mansoni, Spirometra erinacei, and
smaller.
Spirometra ranarum. Adults of these worms  
Spirometraeggs are passed out with the feces
are intestinal parasites of cats, dogs, and other
carnivores. 
of the definitive hosts and become embryonated
in water (Figure 4.8). The coracidium, once  
 

226   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

released, infects Cyclops and develops into the cm in length. When the larvae are flattened,
flattened,  a
 procercoid larva. Once the infected Cyclops spatulate scolex can be appreciated, together
are ingested by the secondary intermediate with pseudosegmentation, and a slit like
hosts such as frogs, snakes, and chickens, the invagination at the anterior end. Species
 procercoidd larva develops
 procercoi develops into the plerocercoid
plerocercoid identification, however, can only be done
larva which is also known as sparganum (pl. through experimental animal infection.  
spargana). If the infected tissues of the second  
intermediate host are ingested by the definitive Treatment 
host (cats and dogs), the plerocercoid larva The main form of treatment is surgical
develops into an adult worm. These adults are  removal of the larvae from the infected tissues.
usually mistaken for adult  Diphyllobothrium Praziquantel has been recommended, but its
latum , although Spirometra sp. adults are efficacy in
efficacy  in humans has not been proven. 
shorter.
Epidemiology 
Pathogenesis and Clinical Manifestations  
Cases of sparganosis have been reported
Humans may be infected through: (a) worldwide: in Africa, India, Holland, Australia,
drinking water containing Cyclops or copepods and South America. In Asia, the majority  
infected with procercoid larvae; (b) eating of cases came from Japan, Korea, Thailand,
Thailand,
infected second intermediate hosts like frogs, Malaysia, and Indonesia.  
toads, or snakes containing the plerocercoid The first  case reported in the Philippines
first case
larvae; (c) applying plerocercoid
plerocercoid infected flesh  was in 1935, when a sparganum was recovered 
of ef ,r ovgasgainnad, sannadkesskains  ppr oeusultlitcinesgoinn ssour  besseoqnutehnet
ey f  om t e a bdoPmuilnilaalnw
sr cinallhy f rr o  m ,  aBlul loacf  aan.seTmhienaser icaonnd
 penetration into cutaneous tissues; and (d) case, reported in 1950, was that of a fisherman
consumption of infected flesh of paratenic hosts from Libon,
Libon , Albay,
Albay,presenting
presentin g with a 4cm lower
lo wer
like wild pigs. The resulting condition is called chest lump. The third case, reported in 1953,
sparganosis.  was that of a 50-year old nun,
nu n, also from Pulilan,
The larvae may be found in any part of Bulacan, complaining of an erythematous,
the body. Most commonly, they are found in slightly painful, pruritic mass in the inner aspect
and about the eyes, in the subcutaneous and of the thigh. Although two of the cases were
muscular tissues of the thorax, abdomen, thighs, from the same place, it was possible that the
inguinal region, and in the viscera. Patients may nun got infected during her stay as a missionary
complain of painful edema due to migrating in Mindanao. A fourth case, reported in 1962,
larvae, hence, the condition is also known as was that of a 46-year old female with a slightly
migrating tumor. Local indurations, periodic  painful, subcutaneous
subcutaneou s nodule at the base of the
giant urticaria, edema, and erythema with neck. In the late 1970’s,
1970’s, and
 and the early 1980’s,
chills, fever, and high eosinophilia may be seen two more cases of human sparganosis were
in patients.  confirmed  at the Department of Parasitology,
confirmed
Diagnosis  College of Public
Philippines Health,
Manila.   University of the
Sparganosis is diagnosed through the In all six cases, the spargana were motile
recovery of the plerocercoid larvae from upon excision of the mass. With the last two
infected tissues. The larvae that are opaque cases, the spargana showed the typical solid
and glistening white usually measure about 3.5    body with worm-like appearance. There 
 

CHAPTER 4: Cestode Infections   227 

was pseudosegmentation with a slit-like References 

invagination at the head end. None of the
Ahluwalia BK, Khurana AK, Gupta NC,  
 patients gave a history
histor y of consuming
consumi ng raw frogs,
Mehtani VG. Hydatid cyst of the orbit.  
 birds, or snakes, nor did they admit having
applied the flesh of such animals as a poultice. AkkizPhilipp J Ophthalmol.
H, Akinoglu 1989;18(4):145
A, Qolakoglu  – 6.
S, Demirytirek
Presumably, transmission may have occurred
through drinking water with Cyclopscontaining  H, Yagnrur O. Endoscopic management 
 procercoids.  da9t2id.  disease.  Can  J  Suger y. 
o1f 99 b6il;i3a9r y:2h87y – 
To date, there have been other cases  
Beaver PC, Jung RC, Cupp EW. Clinical
of human sparganosis encountered in the
 parasitology.
 parasitolo gy. 9th ed.
ed . Philadelphia:
Philadel phia: Lea &
Philippines. One interesting case was the
Febiger; 1984. 
involvement of the central nervous system
Belding DL. Textbook of parasitology. 3rd
of an adult female Filipino complaining of
ed. New York: Appleton-Century Crofts;
headache, seizures, confusion, and hemiparesis. 1965. 
On computed tomography scan, an area of
Garcia EY. Toxoplasmosis and sparganosis in
low density, distinct from other brain lesions, native Filipinos (clinical reports). J Philipp
was detected. Multi-Dot ELISA technique on Med Assoc. 1950;26:227. 
the serum and the cerebrospinal fluid
fluid of
 of the
 patient was positive
positiv e for Spirometra antigen, but Garcia OP, Reyes Al. Sparganosis in Filipinos.
With a review of reported cases in the
not for cysticercus or Paragonimus antigens.
Philippines. J Philipp Med Assoc.  
The positive reaction was confirmed using the 
1962;38(8):608 – 11.
11.
maicyr ohPavlaet b
M e eEeLnISaAcq pur ir oecdedtuhreo.uT
gh edr ininf kecintigonof Hinz E. Hunman helminthiases in the
Philippines. Berlin: Springer-Veriag; 1984.  
water contaminated with infected Cyclops. 
Jeong SC, Bae JC, Hwang SH, Kim HC, Lee L ee
Infection can be prevented by drinking
BC. Cerebral sparganosis with intracerebral
intracerebral
 boiled or filtered wat water, er, by cooking
coo king poss possible ible
hemorrhage: a case report. Neurology. 
intermediate and paratenic hosts thoroughly, 1998;50(2):502 – 3
3..
and by avoiding the practice of applying the
Mastura AB, Ambu S, Hasnah O, Rosli R.
 of frogs to inflamed
flesh of
flesh  areas. 
inflamed areas.
Spargana infection of frogs in Malaysia.
Southeast Asian J Tro
Tropp Med Public Health.
Healt h.
1996;27(1):51 – 2
2..
 

228   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

CHAPTER 5  

Trematode Infections 

Blood Flukes
Edsel  Maur ic e T. Salvaña, Vic ente  Y. Belizar io, Jr . 

flukes 
chistosoma is a genus of parasitic blood flukes   pathogenicity,
 pathogen icity, and immunogenicit
immuno genicity.
y. Injection
Injectio n
that infect birds and mammals, including   of irradiated cercariae of the Chinese strain
humans. Five species of medically important  confers resistance against the homologous strain
Schistosoma have been identified: S. japonicum,   but not against the Philippine
Philippi ne strain. The mouse
S. mansoni, S. haematobium, S. mekongi, and S.  pathogenicity
 pathogen icity of the Chinese strain is less than
intercalatum. S. japonicum is the predominant that of the Philippine strain. 
species in the Philippines and will be discussed Differences also seem to exist among the
in detail in this chapter. various island strains (Mindoro, Leyte,Sorsogon,
Schistosoma japonicum or the Oriental and Mindanao) in the Philippines. However,
 blood fluke causes schistosomiasis japonica.  no studies have definitively showed variations  
It is endemic in China, the Philippines, and and similarities in host range, pathogenicity,
Indonesia. It was first
first described
 described in Japan but   susceptibility to chemotherapeutic
chemotherapeutic agents, and 
has been eliminated, with the last human case other characteristics among these strains. Most
reported in 1977. For centuries, schistosomiasis studies on different aspects of the biology of S.
has caused significant m orbidity and mortality. 
morbidity cum have been done on the Leyte strain,
 japonicum
 japoni
S. japonicum eggs have been identified in a with the findings extrapolated for other island
female corpse from the Western Han Dynasty, strains. 
2,000 years ago. While the disease was described
Parasite Biology 
as early as 1847 by Fuji, the adult S. japonicum
was first described by Katsurada only in 1904.  The S. japonicum life cycle involves
The first
first Chinese
 Chinese case was diagnosed by an intermediate snail host and a definitive
Logan in 1905, and Wooley reported the first mammalian host, with free-living stages in
case in the Philippines in 1906. Strains of S.  between (Figure 5.1). Embryonated eggs from
icumfrom the different geographic regions  
 japonicum
 japon the stool of a definitive host come into contact 
aor f ethgens p cte b
etei caiellsy dOisntcionm qtueirm
l auntiaalal sr ein e esndaiailtse initoh f reseh-swiam
w r  aindg hmaitr cahciwditah. inM2ir taoci4diha our s
tem
hosts. Phenotypic variations include minor seek out and infect the snail intermediate
morphological characteristics, infectivity   host, Oncomelania hupensis quadrasi , and
to Oncomelania snails from different areas, develop into sporocysts. Sporocysts are able to
 periodicity
 periodici ty of cercarial emergence, ability to reproduce asexually and can later give rise to
develop in different definitive hosts, growth free-swimming cercariae after 60 to 70 days.
rates, egg production, pre-patency periods,   The cercariae penetrate the skin of the definitive
definitive  

228 
 

CHAPTER 5: Trematode Infections   229 

host when the host comes into contact with to 2,000 immature eggs/day in the branches
br anches
infested fresh water. Cercariae then lose their of the portal vein. These require 10 to 12 days
tails and transform into schistosomula and enter to mature and embryonate. Eggs deposited  
superficial lymphatic vessels or subcutaneous
veins and reach the lungs. Most authors believe
that from the pulmonary circulation, the 
stchhei p stoam
stor  vaastcur lea.r lH
l  vueleins mwihger ar etetihnetyr am y towr evaecr h,
there is some evidence that schistosomules can
escape from the lungs into the pleural cavity and
 pass through the diaphragm into the liver to
reach the portal vein. In the portal circulation,
schistosomules differentiate into male and
female forms and pair up, with the larger female Plate 5.1. Schi stosomaa i ummae
j ponc l (lef
(left)
t) an
and
d
occupying the gynecophoric canal on the adult female (right) (Courtesy of the Department of
male (Plate 5.1). Each female fluke deposits 500  Parasitology, UP-CPH) 
 

230   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

in mucosal or sub-mucosal terminal veins or

capillaries escape through ulcerations into the
intestinal lumen and are subsequently exported
with the feces. Egg deposition usually begins
from the 24th to the 27th day after cercarial
 penetration. 
While the intermediate snail host is specific
for each schistosome
schistosome species, S. japonicum 
has a wide range of definitive hosts including 
domestic mammals such as dogs, pigs,
p igs, cats,
carabaos, and cows, along with sylvan reservoirs
such as rodents and monkeys. Susceptibility to Plate 5.2. Schs j ponc iumegg
 i tosomaa
infection can vary among different definitive (Courtesy of the Department of Parasitology
Parasitology,,
hosts. Some hosts are considered permissive, UP-CPH) 
i.e., S. japonicum matures and oviposits over
an extended period (e.g., humans, monkeys, 5.2). Eggs are in the multicellular stage when
rabbits, and mice); while others are non- released from the adult female and require 10 to
 permissivee wherein schistos
 permissiv s chistosomes
omes are stunted
stu nted 12 days to embryonate and mature. Immature
or they may mature but die out prematurely.   eggs passed out with feces no longer
long er mature in
Infection rates can also vary between the soil and are not viable. Mature eggs in feces
individuals of the same species. This is likely   can survive and still hatch for up to a week if  

r deus pe otnosev,ar ainatdiohnass  b
ineeim
n m neonasctr iavtaetdioin  and
deum d io.nIninvienwdoef m  tihce anr aetaus r eof of ththe e
 bsulotw
r aeisnif caclaltidoinstr isi b
different genotypes (e.g., inbred strains of mice). Philippines, the prolonged survival time of the
Some evidence suggests that in a particular ovum increases the probability that the eggs
endemic island of the Philippines, only one will be washed down to a water course where
strain is common to the different definitive snails are present. 
hosts. A large series of experimental crosses of Eggs hatch only in clean fresh water with
cercariaee srcinating from a single miracidium
cercaria sufficient oxygen. They will not hatch in
obtained from different naturally infected salinity greater than 0.7% or at mammalian
mammalian hosts from Leyte was made between
between  body temperatures.
te mperatures. A temperature
temperat ure of between
betw een
1954 and 1957. All of the crosses of flukes
flukes  of 25 to 31°C in slightly alkaline water is ideal.
different vertebrate srcin were successful. It is Hatching occurs almost instantaneously upon
easy to presume that these crossings occur in immersion in water. Most viable eggs will hatch
the transmission sites in nature and that only   within 2 to 4 hours. Many miracidia can survive
one strain of S. japonicumexists in this endemic overnight. Essential morphological features  
island. of the miracidium include an apical papilla,
S. japonicum egg is ovoid, round or pear-  epidermal plates covered with cilia, a primitive
pri mitive
shaped, and
diameter is pale
ranges yellow
from 46 toin110
color.
µm,The longer
while the gut, a pair
glands of cephalic
opening unicellular
by a duct at the basepenetration
of the apical
shorter diameter ranges from 37 to 90 µm. It  papilla, two pairs of flame
flame cells,
 cells, and germinal
has a thin shell onto which residual tissue or red cells. The miracidia are phototactic and swim
cells may be adherent. A curved hook or spine actively in surface water. They remain infective
may be observed near one of the polar ends, for snails for 8 to 12 hours, but infectivity
 but only if the egg is properly oriented (Plate  diminishes with time.  
 

CHAPTER 5: Trematode Infections   231 

The mechanism by which snail intermediate shed cercariae. Mortality among infected snails
hosts are located and infected by miracidia, as is increased in comparison with uninfected
well as what may divert them from infecting snails. Infected Oncomelania have decreased
snails has not been well-elucidated. Although egg-laying capacity.  
it is postulated that secretions or excretions Mature cercariae emerge from daughter
of O. h. quadrasi attract the miracidia, but sporocysts and escape from the snail into fresh
these chemotactic molecules have not yet been  water. The cercaria
cercaria has a body and a forked tail. 
identified. In early experiments performed The main body measures from 100 to 500 µm µm
in Leyte, initial contact between a single in length and 40 to 60 µm transversely. The
miracidium placed equidistant from O. h. tail trunk is 140 to 150 µm by 20 to 35 µm;  
quadrasi and other snails was purely random. and the fork is 50 to 70 µm long. The cercaria
After contact with soft parts of the snail,   has an oral sucker, which occupies the anterior
miracidial penetration is effected by movement
movement end of the body, and a small ventral sucker.
andthelyticaction ofcephalicglandsecretions. Cercarial penetration is mediated by lytic
Factors that influence the infection of snails by enzymes secreted by cephalic glands and aided
miracidia include the age of the snails and the  by muscular activ
activity.
ity.
miracidia, the number of miracidia per snail, There are several ways by which cercariae
the length of contact time, water flow,
flow, and
 and emerge from snails infected by miracidia. Singly
Singly
turbulence. infected snails may shed cercariae as early as the
The ciliated surface of a miracidium 42nd day after miracidial penetration, although
disappears once penetration is completed.  the average time is 62 days. Multiply infected  

intiothainfir setvger nale r daatiyosn,  tohr e  moitr haecr ids piuomr ocdyesvtenloe par s

W veh  at  llonger  ,s b
acilasr itaekeansdomheaw
scner  er oior ed.
heudt dsihnegd  pm
the point of entry. At 96 hours after penetration, The total number of cercariae shed during the
th e
it transforms into an elongated sac filled
filled with
 with whole length of infection is about 230 for singly
germinal cells. On the 8th day, germ cells bud off infected snails and 280 for snails with multiple
the epithelial lining and develop into daughter infections. On the average, a snail sheds only
sporocysts. These migrate through loose about two cercariae per day. Snails may climb
connectiv e tissue to the liver. In the connective
connective vegetation above the water line or get stranded
tissues of the liver,
liver, further development of germ on the dryer portion of the snail habitat for
 balls into daughter
daught er sporocysts
sporocyst s takes place. Free several days. Because O. h. quadrasi can easily
swimming cercariae are ultimately produced.  withstand drying for 7 to 10 days becauseb ecause of
Thus, from a single miracidium, through its operculum, it may shed scores of cercariae
the process of asexual multiplication within upon re-entry into water. This phenomenon
the mother and daughter sporocysts, scores is exploited in the laboratory to recover more
of cercariae of a single sex are produced. The  cercariae.. Snails are taken out of the aquaterraria 
cercariae
limiting factor for the number of cercariae that for 2 to 4 days before these are crushed or made
develop from one miracidium is the size of the to shed the parasites. 
snail host.ofIncercariae
thousands areand
S. mansoni since their , 
S. haematobium
produced Studies
are most done inin
abundant Leyte indicate
the field that the
 during
field during cercariae
early
snail hosts are much larger.   evening hours. These observations parallel those
Only a relatively small proportion of the of Bauman et al. who also found that the natural
miracidia that enter snails eventually produce release of cercariae is nocturnal, occurring from
cercariae. Only 6 to 10% of exposed O. h. early evening to midnight. Two factors have
quadrasi found in a study done in Mindoro  been proposed to explain this occurrence: the 
 

232   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

negative effects of exposure to sunlight, and intrahepatic portions of the portal vein. This is
the fact that O. h. quadrasi is more active and likely the more common path of migration to
mobile at night, allowing it to reach water the portal circulation, while the vascular route
sources more often in the evening. Cercariae via the arterial circulation may be a secondary
can survive for up to 24 hours after release, and  pathway.  
so infested water can be infectious at any time Unlike other trematodes, schistosomes are
during the day.  dioecious. Adults have a large sucker capping the  
Cercariae swim on the surface of the water, anterior end, a ventral sucker, and a gonophore,
which facilitates contact and attachment to located slightly posterior to the ventral sucker.
the skin of the host. Host identification
identification  by S.
S.   The suckers aid in movement and enable the  
icum seems to be non- specific, although
 japonicum
 japon flukes to maintain their position inside  veins.
in thermal gradients they show a preference to The male is the shorter but sturdier sex and
a temperature of 35°C ± 3°C. Penetration is measures 12 to 20 mm in length by 0.4 to 0.5
stimulated by skin lipids. Some chemicals like mm in diameter. It has a gynecophoral canal
dimethylate and niclosamide repel cercariae where the longer and more slender female is
when applied to the skin. However, routine held (Plate 5.3). Females measure 15 to 26 mm
use is impractical due to the need for frequent  by about 0.3 mm. They can live for up to 30
reapplication.  years but the mean life span is much shorter
After skin penetration, the cercaria loses (3-8 years). In the male, the testes are arranged
its tail and transforms into a schistosomule. in one row above the ventral sucker, while in
Schistosomuless have adapted to survive in serum 
Schistosomule the female, a single pyramidal ovary is located  
oter g pum   ayt a3fi
hyesniot liosgr iec pslalciende b 7°vCe .toTsheevecne-r lcaayr eir aeld in thSecm . es have an incomplete digestive
hiisdtolisnoem
membrane. In the laboratory, a cercaria can be system and an excretory system made up  
transformed into a schistosomule by repeated of flame cells. These internal structures are
 passage through small bore syringe needles surrounded by circular and longitudinal
resulting in shearing off of the tail, by passage muscles. The worms ingest red blood cells
through isolated skin, and by application to a and possess a protease (hemoglobinase) that
surface with skin lipids or crude egg lecithin.  breaks down
do wn globulin
glob ulin and hemoglobin.
hemoglo bin. They  
One study showed that schistosomules can be
found in the pleural cavity on the 2nd day of
infection, in the parenchyma of the diaphragm
on the 4th day, in the liver parenchyma on the
6th day, and in the intrahepatic branches of the
 portal vein afterwards. There was a very close
correlation between the number of superficial
superficial  
lung petechiae on the 4th to 6th day after
cercariall penetration, and the number of flukes
cercaria
recovered These
 perfusion. Tathese
day observations
30 from the
observationsportal system
seem to by  
indicate
that schistosomules break out of the pulmonary
microvasculature and traverse the lungs to
escape into the pleural cavity. They later go Plate 5.3. Schistosomajaponicumadults
ts in
through the diaphragm, enter the peritoneal copula (Courtesy of the Department of
space and penetrate the liver to reach the   Parasitology, UP-CPH) 
 

CHAPTER 5: Trematode Infections   233 

utilize glucose at a rapid rate and likely absorb the host and mature to lay eggs determine the
nutrients through the body wall. More research severity of infection, with repeated infection
is needed to elucidate the mechanisms for from continuing exposure causing the most
nutrient uptake and metabolism including severe burden of disease. Correlations between
enzyme systems.  excretal egg-output, number of resident flukes,
and egg counts in the liver have been shown in
in
Pathogenesis and Clinical Manifestations  
experimentally infected monkeys. 
Cercarial penetration of skin is usually Egg deposition can occur in any organ, but
accompanied by dermatitis with pruritus and those most commonly involved are the liver,
localized reaction known as “swimmer’s itch.” intestines, lungs, and much less frequently,  
This is similar
s imilar to that se
seen
en from non-jap
non-japonic
onicum
um the central nervous system. In whatever organ
and non-schistosome cercariae that do not lead the eggs are entrapped, the primary lesion is a
to chronic disease in humans. The manifestation granulomatous hypersensitivity reaction around
is self-limited and repeated cercarial exposure a single egg or egg cluster. Since S. japonicum
causes these acute reactions to wane over time. typically deposits eggs in clusters, very large and
 Non-endemic
 Non-end emic travelers to endemic areas are the destructive granulomas are formed. After initial
most likely to experience this phenomenon.   egg deposition, there is an accelerated
accelerated formation
Typically after 2 to 12 weeks following of larger and more destructive granulomas.  
cercarial ppenetration,
cercarial enetration, schistosomule migration However, as the infection becomes chronic,
can give rise to a syndrome characterized
characterized by easy granulomas become smaller or modulated.
fatigability, respiratory symptoms, arthralgias,  Appreciation of the immunologic basis of this  
m ilieae,nf etveer r m, eadnd
a bydaolgmiains,alm paalainis,e,w  ehoicsihnoh pash b aghaeinostmtehneodnisr eaises. tIhmemquensitziaotni onf  vtoa p
 p ccr inoamtiotne
“snail fever,” Katayama fever, or Katayama a modulated granuloma response could lead
syndrome. The latter term is currently preferred to a reduced likelihood of developing severe
since not all patients may present with fever. hepatosplenic disease.  
Hepatosplenomegaly is not uncommon and In view of the collateral circulation
can be quite debilitating during this period of established, eggs are shunted into the systemic
infection, and in rare cases may lead to severe circulation and filtered in the pulmonary
hepatic dysfunction and death. Migration microvasculature,
microvasculature, eventually causing pulmonary
through the pulmonary circulation can cause hypertension. 
wheezing and coughing. Aberrant migration The clinical course of infection is arbitrarily
of maturing schistosomules may occlude the divided into three stages, namely: (a) incubation
circulation of the brain and the spinal cord (corresponding to the period from cercarial
 precipitating
 precipitat ing seizures,
seizu res, paresthesias,
paresthes ias, transient
transi ent  penetration and schistosomular migration to
ischemic attacks, and strokes. While most the time theflukes
the flukes  mature); (b) period of early  
 patients will get better without medication, egg deposition and extrusion; and (c) period of
treatment with anthelminthics usually leads to tissue proliferation. Since there is a significant
faster
Theresolution of symptoms.
main pathology  
and chronic disease overlap of the
disease due second and
to repeated third stages
infection, of the 
it is usually
manifestations of schistosomiasis japonica are more useful to refer to organ involvement as the
due to the host granulomatous reaction to eggs  basis for clinical classification or description. 
deposited in the liver and other organs. Since   American soldiers who landed in Leyte
S. japonicum does not multiply in the definitive in 1944 and acquired schistosomiasis became
host, the initial quantum of cercariae that infect  subjects for the study of early manifestations. 
 

234   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Among 42 soldiers studied, itching soon after

exposure was noted in four cases. In another
series of 41 patients, only one experienced
itching. The majority of subjects had chills,
fever or non-productive cough during the
 period corresponding
corresponding to larval or schistosomular
schistosomular
migration. Another longitudinal study involving 
337 cases established that the pre-patent period
ranged from 42 to 52 days.
Colonic involvement in schistosomiasis
 japonica starts during the early period of egg
deposition. Ulcerations caused by eggs result
Plate 5.4. A boy from Leyte with portal
in dysentery or diarrhea, depending on the hypertension and ascites secondary to
worm burden. In the chronic stage, colonic schistosomiasis (Courtesy of Dr. Edito Garcia) 
schistosomiasis is usually asymptomatic,
although there may be occasional bouts of  porto-systemic
 porto-systemic collateral circulation.
circulation. Jongco and
and
diarrhea. Chronic colonic schistosomiasis has Flaminiano reported in 1961 that pulmonary
 been observed as an incidental finding
finding with
 with schistosomiasis is the most common cause of cor
some malignancies, but a causal relationship  pulmonale
 pulmon ale in Filipino
Filipin o children.
children . Cor pulmonale
has not been established.  may become symptomatic before portal
Hepatosplenic disease is the most serious  hypertension is clinically apparent and may 
ar saecqtueer inzceed  bof y che p
cohn r oantiocs p is.or Italis
oseogmaliya,s p
 psclehnisotm
lead to a delay in
i n diagnosis of schistosomiasis. 
Cerebral schistosomiasis (Plate 5.5) is 
hypertension, ascites, and development of estimated to occur in 1.7 to 4.3% of infections.
collateral circulation, which can lead to Among the Americans that landed in Leyte
esophageal and gastric varices. An analysis by in 1945, 2% had cerebral manifestations.
Pesigan et al. of 2,540 cases of schistosomiasis Cerebral manifestations may present as motor
 japonica detected by stool examination
examinat ion during or sensory disturbances depending on the site
surveys of Department of Health teams in 1950 of egg deposition and granuloma formation. 
and 1951 showed that 31% had developed mild
hepatosplenic disease, 9.1% had definite signs  of
of
ascites, and 1.4% had severe portal hypertension
with prominent ascites (Plate 5.4). Cinco et al.
reported that 14% of cases of schistosomiasis
had a history of hematemesis and/or melena.  
Pulmonary involvement may initially 
occur during the period of larval migration,
which can result in coughing, wheezing,

and other respiratory

schistosomiasis, symptoms.
the lungs followInthe
chronic
liver  
and intestines in having the most number of
schistosomal lesions. Cor pulmonale can result
from obstruction of the pulmonary
pul monary vasculature Plate 5.5. Schi stosomaegg in the
th e brai n
due to granuloma formation and fibrosis. Eggs (Courtesy of the Department of Parasitology,
likely reach the pulmonary circulation via the   UP-CPH)
 

CHAPTER 5: Trematode Infections   235 

Early neurologic involvement is brought about kept indefinitely. Processing can therefore be
 by the parasite’s transition from the portal resumed in the laboratory or at some later
vein via mesenteric and pelvic veins to the convenientt time. Protozoans are also preserved
convenien
spinal veins. Acute cases usually present with and stained in the preparation allowing
fulminating meningoencephalitis with fever, diagnosis of polyparasitism.  
headache, confusion, lethargy, and coma, while
while The Kato-Katz technique is the preferred
chronic cases give a clinical picture of a tumor 
t umor   egg-counting technique and is considered the  
with localizing signs and increased intracranial most suitable for quantification
quantification of
 of eggs. It is
 pressure.  the most commonly used stool examination
technique for evaluating epidemiology, effect 
Diagnosis 
of control measures, and drug trials. The
Because S. japonicumis primarily a parasite Kato-Katz preparation can be kept for at least
of the portal vein and its branches, eggs are 2 weeks for later examination depending on the
not immediately demonstrable in the feces workload. There is practically no loss of eggs
unless they are deposited in the terminal during storage and processing which makes
vein or capillaries of the intestinal mucosa or the technique satisfactory for determining
submucosa, and subsequently escape to the fecal egg density. Specimens with less than 20
intestinal lumen. In infections where there  eggs per gram of feces require examination of
is scarring or fibrosis
fibrosis of
 of sites of ulcerations, at least three Kato-Katz preparations to have
 passage of eggs into the intestinal lumen can 92% sensitivity. 
 be impeded. In these cases, stool examinations   Rectal snips and imprints require specialized  
cSacnhigsitvoesonmegeaetgivges r ceasnualtlsoe bveenr eincoavcetr ievde b eecctitoaln.
 inyf r  emqousi pm
t seensittiavnedt p  bItutis aar lesoamthoengmtohset
ecehr nsoiqnunesl.,  b
or liver biopsy. However, these procedures invasive since biopsy specimens are required.
require specialized equipment and are not Another drawback is the inability to distinguish
 practical for mass screening or field
field surveys.
 surveys.  between untreated andan d treated infection
i nfection since
s ince
Moreover, tissue diagnosis cannot reliably eggs can persist in rectal tissue long after active
distinguish active from treated infection.   infection has been eradicated. Some techniques
Microscopic examination techniques are such as vital staining and egg morphology
the most specific since these directly visualize and embryo motility have been proposed to
the parasite egg. Microscopic techniques distinguish viable from nonviable eggs, but none
include stool examination and rectal imprint.  of these are consistently reliable.  
S. japonicum eggs tend to clump together, so a The intimate tissue contact between
small stool sample may turn out falsely negative.  parasite and
an d host during
du ring cercarial
cercari al penetration,
penetr ation,
This may also occur in cases of light infection.  schistosomularr migration, intravascular growth
schistosomula
To establishing adiagnosis, the merthiolate- and development of adults, and deposition of  
iodine-formalin concentration technique eggs in the tissues
tissue s stimulate
stimulateand provo
provokeke specific
(MIFC) has sufficient sensitivity for moderate immune responses which can be demonstrated
and heavy
for very infections,
light infectionsbut it is
(<10 notper
eggs adequate
gram of as evidence
Locally of infection.
evaluated  
immunodiagnostic
feces). This technique has certain advantages tests include the following: (a) intradermal
over other stool concentration techniques test for immediate cutaneous hypersensitivity
making it suitable for field surveys. Fecal using adult worm extracts; (b) indirect
samples mixed with merthiolate-formalin hemagglutination using adult worm and egg  
(MF) solution in screw-capped vials can be   antigens; (c) circumoval precipitin test (COPT);  
 

236   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

and (d) the enzyme-linked immunosorbent 55 to 91% (n=14). Urine and serum tests on
assay or ELISA using soluble antigens of other schistosome species in Africa and Brazil
adults and eggs. A multicenter evaluation of S. have so far shown disappointing sensitivity and
icum diagnostics conducted by the World
 japonicum
 japon specificity for antigen based tests. A variety of
Health Organization, in which the Philippines the currently available antibody and antigen
 participated,
 participat ed, showed
showe d that crude
crud e egg antigens
antig ens tests should be compared using sera collected
were most specific.
specific. In
 In view of this, only the   from low endemic areas. This will determine 
COPT, ELISA, and indirect hemagglutination which assays are practicable for field use in
using egg antigens are recommended for use.   endemic areas. The method of choice will
There are inherent problems with depend on cost, simplicity, and sensitivity.  
 parasitological diagnosis especially in low The COPT demonstrates the formation
endemic areas. Thus, there may be
b e a role for of bleb-like or septate precipitates attached to
antibody or antigen detection that may have one or more points on the egg surface after
advantagess over parasitological
advantage parasitological diagnosis. In the incubation of schistosome eggs in a patient’s
Philippines, a proportion of COPT positive but serum. It is currently regarded as the method of
single Kato-Katz negatives were shown to have choice for definitive diagnosis of this infection
eggs on repeated
r epeated sampling.   in the Philippines. The sensitivity of COPT is
The intradermal test is highly sensitive due to the fact that it is a microprecipitation
micr oprecipitation
 but nonspecific for infection. It cannot reliably reaction visualized under the microscope with
distinguish active from old infection. It is no sensitivity comparable to passive or indirect
longer used
us ed routinely
routi nely as
a s otherimmunodia
otherimmunodiagnostic
gnostic  hemagglutination.

tests Ihnadvier er ce p
t hlaecmedagigt.lutination has b
 been shown   CecOoPmTe  m
year sTthoe b mhoer etitm
neagyatiavkee.  T haens  p enot
ptw
to be highly sensitive. However, it does require in examining is very much reduced with
specialized reagents and training but can be standardized egg preparation obtained from  
 performed with minimal equipment
equipmen t in the field. 50 to 60-day old S. japonicum infections of
ELISA formats are among the most sensitive rabbits. During this period of infection, there
tests but the need for laboratory equipment is a maximum proportion of mature eggs from
and trained personnel limits its use to banked the liver, which can be used as antigens for the
specimens and cannot be a point of care test. test. At least 25% of the
t he eggs can be visualized
 New lateral flow  assays, which use card tests
flow assays, with precipitates after incubation with a positive
with visually apparent results, harness ELISA serum, so examination of the slide requires a
technology for point of care and field use minimum amount of time.  
and have been validated extensively in China. Epidemiological studies in Barrio San
Lateral flow  assays are likely the best suited for Antonio in the town of
o f Basey, Samar,
Samar, where
where the
elimination programs. However, the biggest   whole population was examined using MIFC 
drawback for antibody detection tests remains and COPT, indicated that many infections,
the persistence of antibodies long after active  particularly
 particular ly of the population
popul ation above 10 years old
infection hasdetection
Antigen b een ttreated.
been reated.
reflects  active infection. were notpercent
Seventy detectedofbythea single stooltested
population examination.
positive  
In more recent studies, adult worm antigens  by COPT,
COPT, while only 40% tested positive
positi ve with
were found to be better than egg antigens for a single stool examination.
examination.  
detecting low level infections (<100 eggs/g). Because COPT is technically demanding
Egg antigens detected only 65 to 85%
8 5% of cases and requires specialized equipment, it is not
(n=7), while adult worm antigens detected   routinely used for field
field testing.
 testing. Moreover, it  
 

CHAPTER 5: Trematode Infections   237 

cannot distinguish active from past infection. intervals of several hours. Even if the patient
Currently, COPT is used as an adjunct tool for is not fully cured, the passage of eggs becomes
diagnosis in patients who are stool negative but significantly reduced. Improvement after
remain highly suspicious for schistosomiasis. ItIt treatment is clinically apparent. There is a
is not recommended for use as a screening tool reduction in the degree of portal hypertension,
in the Philippines.  hepatosplenomegaly, and cerebrospinal
manifestations. In local studies, egg reduction 
Treatment  rates have ranged from 80 to 96% in patients
Praziquantel, a heterocyclic who received treatment with praziquantel 60
 prazinoisoquinoline
 prazinoisoquinoline compound,
compound, represents
represents mg/kg in two divided doses.
a major breakthrough in the treatment of   The frequency of side effects varies in the
schistosomiasis. It is safe and highly
high ly effective different treated groups but these are generally
in single or divided doses against all the major mild and transitory. In a retrospective study
species of schistosomes. The active substance of 25,693 S. japonicum patients treated with
is a hygroscopic, colorless, almost odorless,  praziquantel in China, only 0.4% of patients
crystalline powder with a bitter taste, which were reported to have serious adverse effects.
is stable under normal conditions but melts In local studies involving more than 6,000
and decomposes at 136 to 140°C. It is very  patients, praziquantel given at 60 mg/kg in
soluble in chloroform and dimethyl-sulfoxide, two divided doses resulted in mild to
t o moderate
sparingly soluble in ethanol and very slightly
slightly side effects in 68% while severe reactions were
soluble in water. Praziquantel is active against  recorded in 1.2%. The most frequent adverse
adverse 
vintr othaant dscihnisvtiovsoo. m
avditur olt esxc pheisr tiomsoenmtes sh baovethshinow Ines eof r f edcitscoar me f e p
or itg, anstar uicseoar ,  dainf of ur esexia b,  doizmzineasl p
s,  ain
instantly become immobile and undergo headache, and fever. Most of these were noted
contraction on contact with the drug. to be mild and transient. 
Acute toxicity studies conducted in Artemisinins including artemether have
rats, mice, and rabbits have shown that in recently been shown to be effective in decreasing 
comparisonwithotheranti-schistosomaldrugs, S. japonicum infections when used as pre-
 praziquantel has a very
 praziquantel very low acute toxicity
toxicity profile. exposure prophylaxis during the planting season
Rats tolerated daily doses of up to 1 mg/kg for 4 in China. Artemether is effective against  
weeks, and dogs tolerated daily dosages of up to the juvenile stages of the worm and so this
180 mg/kg for 13 weeks without organ damage. drug is ideal for the non-endemic traveler.
 No effects were seen on the whole reproductive
reproduct ive However, routine use for endemic natives
nat ives may
 process in rats. Teratogenic effects were not  be problematic in areas where malaria is co-
observed in mice, rats or rabbits.   endemic since this may give rise to resistance.
resistance.
A single dose of 40 to 50 mg/kg, or 25 mg/ Combination therapy with praziquantel has  
kg in two doses or three doses of 20 mg/kg given shown high cure rates in laboratory animals
every 4 hours or even a dose as low as 10 mg/kg and may be an option in areas with high worm
given threeA
cure rates. times a day
dosage offor
302mg/kg
days provide high
given after
af ter  burden or
or emerging drug resistance
resistance.. 
Epidemiology 
 breakfast and repeated after lunch has been used
in trials involving more than 6,000 patients with Transmission dynamics vary considerably
light to moderate S. japonicum infections with in the different endemic areas due to the
a cure rate
r ate of almost 90%.   many factors that influence the common
Generally, a single large dose has the environment, the behavioral patterns of the
same efficacy as several smaller doses at   definitive host, and the bionomics of the
 

238   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

snail host. Extrapolation of data, whether

in snail populations, animal populations, or  
socioeconomic activities, may not completely
capture the true situation. Understanding the
epidemiology of schistosomiasis requires the
study of the effects of rainfall, socioeconomic
activity, cultural and behavioral patterns, and 
demographic characteristics of the human
 population and animal reservoir hosts in the
transmission of S. japonicum. Occurrence of  
disease in the community should be described in
relation to prevalence and intensity of infection.  
In the Philippines, schistosomiasis remains
remains
endemic in 12 regions covering 28 provinces,
190 municipalities, 15 cities, and 2,222
 barangays. Two additional
addit ional municipali
mu nicipalities
ties of
Gonzaga, Cagayan (Region 2) and Calatrava,
 Negros Occidental
Oc cidental (Region
( Region 6) were recently
recentl y
identified as schistosomiasis endemic areas
in 2004 and 2006, respectively, through  
the identification of indigenous cases, and  
edor Oe .r ehc.enqut asd 
i5n.2f e)c. tM ur veys ncaoinl dvuecteodr   t(hFr iogugr eh
r a i
 s

active surveillance by field schistosomiasis

teams revealed a national average prevalence
Figure 5.2. Map of Sch s
itosoma a ium-
j pon c
of 2.5% (Table 5.1). The at-risk population endemic provinces in the Philippines 
is approximately 6.8 million. The highest
 prevalence of infection is in children 5 to 15
Table 5.1. Prevalence of schistosomiasis stratified
years of age.  by province (2005-2007) 
A cross-sectional survey
sur vey done in Western
Samar that covered 1,425 households in 50 Provinces Prevalence(%)
 barangaysrevealed a schistosomiasis prevalence  Agusan del Sur
Sur
rate of 18%, with 3.2% having moderate to
heavy infection. Epidemiological surveys have
demonstrated 10% disease prevalence for
Cagayan in 2004 and 69% disease prevalence
prevalence 
for Calatrava, Negros Occidental in 2006.
A study involving 1,848 school-age children
described
Agusan dela Sur
resurgence
with anofoverall
schistosomiasis
pr evalenceinat 
prevalence
31.8% and proportion of moderate to heavy
intensity infections at 19.3%.
Pre-control assessment of the problem of
schistosomiasis is essential for evaluation of the
effectivenesss of control measures. The more
effectivenes
useful epidemiologic
epidemiologic indices are: (a) prevalence,
prevalence, 
 

CHAPTER 5: Trematode Infections   239 

Provinces Prevalence(%)
Information Systems (GIS) might allow the
number of individuals to be monitored for
ongoing transmission. New foci of transmission
may also be shown reflecting changes in
geographical location of transmission foci. 
S. japonicum is naturally transmitted
 between humans and other mammalian hosts,  
with either humans or animals alone being
able to maintain the infection cycle. Prior to
Source: Leonardo L, Rivera P,Saniel O, Villacorte E, Crisostomo
B, Hernandez L, et al. Prevalence survey of schistosomiasis
application of intervention measures like mass 
in Mindanao and Visayas, T he Philippines. Parasitol Int. chemotherapy or a program of sanitation, it is
important to have a measure of how much of
the contamination of the environment with
(b)  incidence, and (c) intensity or worm schistosome eggs is attributable to human
 burden estimated
est imated according
acco rding to
t o the number
nu mber of and animal reservoirs. This will be of value in
eggs per unit of weight of feces. It is essential  predictin g the success of sanitary
 predicting sanitar y disposal
dispos al of
that these indices are determined before the human feces and chemotherapy in reducing
implementation of the control program to have transmission and complementary measures of
 baseline data ffor
or evalu
evaluation.
ation. control. The prevalence and egg output should
The magnitude of the problem is reflected  be determined for all possible egg sources. 
 by the prevalence with an expression of the  In the human population, these indices

r waoter min btuhr edyeonu. nDgetr ear gmeisniastaiom
n oor f etahceciunr caitdeeanncde coanytr vi bar uytea m onr egtahgaengor othu p
m er s.tSoocm
onetgar moiun pastiwonil.l
a more sensitive measure for assessing effects In areas of high prevalence, children aged 5 to
of intervention measures that aim to reduce 14 years old usually contribute more, whereas
transmission since schistosomiasis is a chronic in lower prevalence areas, older children and
infection.  adults are responsible for the bulk of the
A measurement of worm bur den or contamination.  
intensity of infection is done through excretal Transmission of infection requires
requi res contact
egg counts. The incidence may not be reduced  between humans
h umans and other
o ther animal
ani mal hosts with
 but the quantum of infective cercariae per the breeding sites for snails. As part of pre-
exposure may be reduced after therapy so that control studies, the most common water sites,
there is a corresponding decrease in worm and the reasons for water contact and their
 burden. In all endemic communities, the relative importance should be determined and
distribution of excretal egg count per unit of ranked according to relative importance. This
weight of feces is not normal or random so should lead to the provision of appropriate  
that a geometric and not an arithmetic mean is alternate facilities (such as protected laundry
a better expression for community egg count. areas or footbridges) to reduce water contact
For example, in a study in Irosin, Sorsogon, and determine priorities for snail control.  
only a small proportion of the study population Prevention and Control 
(4.1%) excreted 50% of the eggs counted in the
study. Excretal egg counts are therefore useful In areas ofhigh prevalence and transmission,
in determining priority of treatment.   mass chemotherapy to reduce morbidity remains
Use of mapping of “hot spots” of infection/ the main control strategy. School-age children
transmission by the use of Geographic   have been identified as a target group for regular  
 

240   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

chemotherapy against schistosomiasis since the

chemotherapy to improve knowledge, attitudes, and perception
WHO Expert Committee on Bilharziasis first with respect to transmission, diagnosis, and
met in 1953. Treatment in this age group has control of schistosomiasis. Since behavior  
 been shown to reduce significant
significant morbidity
 morbidity is influenced by local culture, knowledge,
in the short-term and prevent the long- attitudes, and practices (KAP) of the target
term sequelae in adulthood associated with area should be taken into consideration. This
chronic infection. Continued transmission of   will permit the design of a more applicable and 
schistosomiasis will depend on how rigorously relevant educational program. Health education
chemotherapy can be applied, as well as on  programs should not only be concerned with
epidemiological factors. In order to achieve a  modifying KAP but should also encourage  
sustainable reduction in transmission, health and promote community participation in
education, attention to the water supply and contributing to schistosomiasis control.  
sanitation, environmental management, and O. h. quadrasiis an operculated fresh water
where appropriate, snail control need to be amphibious snail (Plate 5.6) with separate male
 part of an overall strategy from the very start. and female sexes. These attain sexual maturity
The primary objective of chemotherapy using  by the time the snails measure 3.5 mm. A single
 praziquantel
 praziquant el is the reduction
reductio n and prevention
preventio n of copulation will allow the fertilized female to lay
morbidity. Since it is inevitable that prevalence two eggs every 5 days for 1 month. The usual
will decrease following treatment, itisi s important snail habitats are small clear water streams,
to measure the effect of chemotherapy on water-logged rice fields, swamps, and water
incidence, worm burden, and morbidity of new   seepage areas along mountains or foothills. 

caagsenst. Tlihke  p
usr eaozif qaunanef tf elctr ievqeucihr esmeof tfihceier an ptecuatsice  bInotah sitnr etahme  woar tesm he, b
onamt p
r   anlldsw   sanaikls. aSr neaf iolsuanr de
detection systems and diagnostic tests in order most numerous in areas where the soil is moist.
to optimize priorities for treatment where Those in the water are found in shallower areas,
resources will not permit treatment of all on protruding rocks, or on floating leaves and
infected individuals.   branches. 
Chemotherapy using praziquantel to Twogeneral strategies
strat egies for snail control are
reduce morbidity is the principal thrust of in use: focal and area-wide. The focal approach  
the Philippine program for schistosomiasis
control. However, it should be stressed that
equal emphasis should be placed on control
of transmission and eventual elimination of S.
 japonicum , O. h. quadrasi, or both, as has been
achieved in Japan and in extensive portions of
China.
While effective and safe chemotherapy,
improved environmental management, and
snail control all contribute
schistosomiasis, tosolution
the long term the control of 
to this
 problem requires
re quires sustained
su stained and
an d appropriate
appropr iate
health education and strong community
Plate  5.6.  Onc 
omel ani ah. quad  ,
intermediate
asi 
r 
 participation.
 participat ion. Consequently,
Consequent ly, health education host of Sch sitosomaa (Courtesy of the
 j pon c
ium
must be recognized as an integral part of the Department of Parasitology,
Parasitology, UP-CPH) 
control program. Strong effort should be made  
 

CHAPTER 5: Trematode Infections   241 

may be more feasible where transmission sites implement the necessary environmental changes
and resources are limited, but area-wide control without resorting to large capital expenditure.
is more pragmatic if transmission is spread over a In the Philippines where there is a perennial
watershed or an irrigation system. Focal control shortage of funds, increased community
requires water contact studies to identify the  participation is
is needed tto
o ensure the success
most common transmission sites. Tocontrol an of snail control programs. The advantages of
entire area or watershed unit, all snail
s nail habitats  snail control by environmental methods include  
should be identified
identified and
 and treated. Area-wide the following: (a) it can be incorporated or
control is moredifficult
more difficult  and expensive, but it integrated into regional agricultural and other
is also likely to be longer lasting and ultimately  rural development projects; (b) the results can 
more cost-effective than focal measures.    be made permanent or persistent provided
Environmental control methods involve adequate maintenance is done regularly; (c) it
alteration of the snail habitat to reduce survival results in increased agricultural
agricultural productivity; (d)
and prevent or deter snail reproduction. in the absence of adequate funding, the control
Control of breeding has a more lasting effect measures can be done on a focal basis by the
than killing snails. The more radical the  people themselves;
themselv es; (e) it results in increased land
intervention, the more profound the effect of value; and (f) it does not require foreign aid and
the control measure on the snail population. technology, unlike chemical control.  
Methods of control are based on removal of the  No outstanding novel molluscicide or
environmental requirements of Oncomelania. chemical for killing snails has been developed
These include: (a) drainage of breeding sites   in the past decade. Interest in such research  

r er mo pover almoaf nsahgaedmeeonr t oshf eilr tr eir gaf tr iom
a(  bbn)d p susn;
n styhsetem  br eyseianr dcuhstar nydhdaesvdeliom niesnhet dc b
 pim osetcanudse tohf e hlaigckh
 by clearing vegetation around bodies of water;   of an assured market. Most countries that
(c)  prevention of breeding on the banks of have schistosomiasis cannot afford the cost
streams or irrigation canals by lining these with of deploying molluscicides, and there is
concrete or making them more perpendicular;  increasing concern about the consequent  
(d)  acceleration of flow flow of  of water by proper environmental pollution with pesticides that are
grading and cleaning of the stream bed and not biodegradable or have long half-lives. The
removal of debris; (e) construction of ponds future role of molluscicides may be determined
if the area cannot be drained; and (f) covering  by economic considerations
considerations and the priority
snail habitats with landfills.  afforded schistosomiasis in relation to other
The effectiveness of these alterations  public health problems. 
is lasting if there is proper maintenance.  The objective of sanitary disposal of
Although snail control is usually done on a human feces is to prevent contamination of
focal basis, when possible, it should include   watercourses inhabited by snails. However, this  
entire watershed. All of these methods have has limited value in S. japonicum transmission
 been found
foun d to be effective
effect ive experimentall
exper imentallyy as if animal reservoir hosts represent a significant
early as 1958
limiting in of
factors theenvironmental
Philippines. lOne
environmenta of the rate 
modification source
Theofuse
miracidia for infecting
of properly snails.
constructed and 
of habitat is the cost involved. Japan was able hygienic latrines should be encouraged as this
to afford the large capital expenditure needed contributes to the control of water and fecal-
for cementing canals, reclaiming swampy areas,  borne viral,
vi ral, bacterial,
bacterial , and parasitic
parasi tic infections.
infect ions.
and sustaining the control program. In China, Latrines for use in rural areas have been regarded
the socio-political structure made it possible to   as unsatisfactory because of flies, mosquitoes, 
 

242   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

and maintenance problems. These issues should operational efficiency so that evaluation of the
 be resolved to increase toilet utilization.  effects of control operations will be valid and
The simplicity of diagnostic techniques, will truly reflect the epidemiologic profile of
the safety of praziquantel, the relative facility the disease. 
of focal control of snails, and the availability of A transmission blocking vaccine has been
epidemiologic information for some endemic developed for water buffaloes in China and
areas permit adoption and integration of   represents a major breakthrough in controlling 
schistosomiasis control into primary health animal reservoirs. However, domesticated
care. This stimulates active involvement of animals seem to be the minority reservoir
the community and facilitates the entry into   in the Philippines in comparison to sylvan 
endemic communities of support services and reservoirs and human sources of infection.
schistosomiasis teams of the Department of Development of a human vaccine has proven
Health.  difficult since Schistosoma is well-adapted to
Primary health care workers in endemic evading the immune system in its niche as an
areas should have some basic knowledge of intravascular parasite. Several parasite antigens
schistosomiasis, including major clinical are promising vaccine candidates, including
manifestations, method of diagnosis, treatment,  paramyosin,
 paramyosi n, which has generated
generat ed immunity
immuni ty
transmission, and control. They should be to repeated infection in pilot studies. The
involved in stool collection, surveys, and mapping of the schistosome genome will enable
treatment of patients. They should also  the identification of more vaccine candidate
 be utilized
utili zed as health educators, and
an d asked  molecules and other possible novel mechanisms 
toar etn
 p i cuoluarlaygiencsoam tautinointya p
nim iil actoiontr ,ol. 
ndar stnica p for the treatment and control of this parasite.
References 
The effectiveness of intervention measures
must be monitored and evaluated to ensure Belizario VY, Amarillo ML, Martinez RM,
that the approaches are effective and properly Mallari AO, Tai CM. Resurgence of
implemented to detect any resurgence, and to schistosomiasis japonicum in school
 justify costs. The thrust and components of the children in Agusan del Sur, Philippines:
control program determine the indices that will opportunities for control in the school
 be measured
measured as basis
basis for evaluation. It is essential setting. Acta Med Philipp. 2007;41(2):9 –  
to have adequate baseline data, especially   14. 
for pilot areas, prior to the implementation Belizario VY, Martinez RM, de Leon WU,
of control operations to allow for adequate Esparar DG, Navarro JR, Villar LC, et al.
assessment. Cagayan Valley:
Valley: a newly described endemic
Control programs should have operational focus for schistosomiasis japonicum  
targets and corresponding timetables for each   in the Philippines. Phil J Intern Med.
endemic area. For example, there should be 2005;43:117 – 22.
22.
targets for social preparation of the population Department of Health. Schistosomiasis in the  
for awareness building and participation.   Philippines: conference/worksho
conference/workshops
ps  on
The coverage and timetable for parasitologic schistosomiasis. Manila. 2007.
examination and chemotherapy should be Gryseels B, Polman K, Clerinx J, Kestens  
ascertained. Snail colonies or areas to be treated L. Human schistosomiasis.
schistosomiasis. Lancet.
should be identified. Equally important is 2006;368:1106 – 18.
18.
the standardization of techniques to be used. Legesse M, Erko B. Field-based evaluation
Monitoring and supervision should ensure   of a reagent strip test for diagnosis of  
 

CHAPTER 5: Trematode Infections   243 

schistosomiasis mansoni by detecting Ross AG, Vickers D, Olds GR, Shah SM,
circulating cathodic antigen (CCA) in McManus
McM anus DP.Katayama
Katay ama syndrome. Lancet
urine in low endemic area in Ethiopia. Infect Dis. 2007;7:218 – 24.
24.
Parasite. 2008;15:151 – 5.
5.   Salvana EM, King CH. Schistosomiasis in
Leonardo LR, Rivera P, Saniel O, Villacorte travelers and immigrants. Curr Infect Dis
E, Crisostomo B, Hernandez L, et al. Rep. 2008;10:42 – 99..
Prevalence survey of schistosomiasis in   Steinmann P, Keiser J, Bos R, Tanner M,
Mindanao and the Visayas, The Philippines. Utzinger J. Schistosomiasis and water
Parasitol Int. 2008;57(3):246 – 51.
51. resources development: systematic review,
Li YS, Chen HG, He HB, Hou XY, Ellis M, meta-analysis, and estimates of people at 
McManus DP. A double- blind
 blind field trial risk. Lancet Infect Dis. 2006;6:411 – 225.
5.
on the effects of artemether on Schistosoma Stothard JR, Sousa-Figueiredo
Sousa-Figueiredo JC, Standley C, 
 japonicum infection in a highly endemic Van Dam GJ, Knopp S, Utzinger J, et al.
focus in southern China. Acta Trop.   An evaluation of urine-CCA strip test
test and
2005;96:184 – 90.
90. fingerprick blood SEA-ELISA for detection
Lin DD, Xu JM, Zhang Y YY,
Y, Liu YM,
Y M, Hu F,
F,Xu of urinary schistosomiasis in schoolchildren
schoolchildren
XL, et al. Evaluation of IgG-ELISA for the in Zanzibar. Acta Trop. 2009;111:64 – 770.0. 
diagnosis of schistosoma japonicum in a Utzinger J, N’Goran
J, N’Goran EK,
 EK, N’Dri
 N’Dri A,
 A, Lengeler
high prevalence, low intensity endemic area C, Xiao S, Tanner M. Oral artemether
of China. Acta Trop
Trop.. 2008;107:128 – 33.
33.  for prevention of Schistosoma mansoni
McGarvey ST, Carbin H, Balolong E, Belisle  infection: randomised controlled trial.  
Pse,ctFioer nalnadsseoz cTia,tiJoonse p
 bhetwL,e ent ianl.teCnr siotsys- ldanHc eta.lt2h00O0;r 3g5an5i:1za3t2io0 – 
Wor L n.5.R eview  on  the
of animal and human infection with epidemiological profile of helminthiases
Schistosoma japonicum in Western Samar, and their control in the Western Pacific
Philippines. Bull World Health Organ. Region, 1997-2008.Geneva:
1997-20 08.Geneva: WorldHealth
2006;84(6):446 – 52.
52.  Organization; 2008.
McManus DP. Prospects for development of Van Dam GJ, Wichers JH, Ferreira TM,
a transmission blocking vaccine against Ghati D, van Amerongen A, Deelder AM.
Schistosoma japonicum. Parasite Immunol. Diagnosis of schistosomiasis by reagent
2005;27:297 – 308.
308. strip test for detection of circulating
Mott KE, Dixon H, Carter CE, Garcia E, E, cathodic antigen. J Clin Microbiol.  
Ishii A, Matsuda H, et al. Collaborative 2004;42:5458 – 61.61.
study on antigens for immunodiagnosis Zhou YB, Yang MX, Tao P, Jiang QL, Zhao
of Schistosoma japonicum infection. Bull GM, Wei JG, et al. A longitudinal study
World Health Organ. 1987;65:233 – 44.
44.  of comparison of the Kato-Katz technique 
Ohmae H, Sy OS, Chigusa Y, Portillo GP. and indirect hemagglutination assay
Imaging diagnosis of schistosomiasis (IHA) for the detection of schistosomiasis
 japonica
for field  — theinuse
study theinpresent
Japan and application
endemic area.   japonica in China,
2008; 107:251 4.2001-2006.
 – 42001-2
. 006. Acta Trop.
Trop.
Parasitol Int. 2003;52:385 – 93.
93. Zhou YB, Yang MX, Wang QZ, Zhao
Richter J. The impact of chemotherapy on GM, Wei JG, Peng WX, et al. Field
morbidity due to schistosomiasis. Acta comparison of immunodiagnostic and
Trop. 2003; 86:161 – 83.
83.   parasitological
 parasitological techniques for
for the detection
detection  
 

244   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

of schistosomiasis japonica in the People’s Zhu YC, Socheat D, Bounlu K, Liang YS, Sinuon
Republic of China. Am J Trop Med Hyg. M, Insisiengmay S, et al. Immunodiagnosis
2007;76:1138 – 43.
43. and its role in schistosomiasis control in
China: a review. ActaTrop
ActaTrop.. 2005;96:130 – 66.. 
 

CHAPTER 5: Trematode Infections   245 

Lung Flukes
Vicente Y. Belizario, Jr., Alexander H. Tuliao

Paragonm
i uswesterman i
 

P  aragonimiasis is an infection of humans

and other mammals by trematodes of the  
genus Par
 Paragonimuss. There are 40 known species
agonimu
of Paragonimu
 Paragonimuss, and six are reported to cause
infections in humans.  Parag
 Paragonimu
onimuss west
westermani
ermani
or the Oriental lung fluke causes 90% of
 paragonimiasis in Asia. In the Philippines, P.
 P.
westermani is also the major species that causes
 paragonimiasis in humans. The only other
species in the Philippines is P. siam
siamensis, which
ensis
has only been identified
identified in
 in cats. 
In 1879, Ringer observed the first case of
 pulmonar y paragonimiasi
 pulmonary parag onimiasiss in humans
hu mans during
duri ng Plate 5.7. Paragonm
i uswesterman iadutl
an autopsy in Formosa. A year later, Baelz   (Courtesy of the Department of Parasittology, ology, 

(id1e8n8t0ifi) eind  P  u aonvsaonin(1h8u8m
Ja par aan g oannidmM
 s
0a)in sF pour tmum
os.a UP-CPH)

Musgrave (1907) described the first case of The cercaria is covered with spines, has
human paragonimiasis in the Philippines.   an ellipsoidal body, and a small tail. A stylet
In 1915, Nakagawa discovered that crabs is present at the dorsal side of the oral sucker.
act as a second intermediate host. Two years The metacercaria is round and measures from
later, Nakagawa succeeded in infecting the snail 381 to 457 µm. The oval, yellowish-brown,
yellowish-brow n,
 Melania
 Melani a libertine with Parag
libertine onimus miracidia. 
 Paragonimus thick-shelled egg measures
measures 80 to 118 µm
µ m by 48
Parasite Biology 
to 60 µm, and has a flattened
flattened but
 but prominent
operculum. Opposite the operculum is a
The adult lung fluke (Plate 5.7) is reddish- thickened abopercular portion (Plate 5.8). It is
 brown and measures 7 to 12 mm in length, 4 to unembryonated at oviposition. 
6 mm in width, 3.5 to 5 mm in thickness, and The immature egg embryonates in water,
resembles a coffee bean. It is rounded anteriorly moist soil, or leached feces (Figure 5.3). A
and slightly tapered posteriorly. The tegument miracidium develops within 2 to 7 weeks. It
is covered with single-spaced spines. The two subsequently pushes open the operculum and
testes are deeply lobed and are situated opposite swims freely in search of its
i ts appropriate snail
each other,
sucker andalmost midwayborder
the posterior between ofthe
theventral
body.
host. In the Philippines, the 1st intermediate
hosts are Anteme
 Antemelania
lania asperata and Anteme
asperata  Antemelania
lania
The ovary is located anterior to the testes and dactylus , the former previously known as
 posterior to the ventral sucker, and has six long  Brotia aspera ta (Plate 5.9). Inside the snail, the
asperata
unbranched lobes. The vitellaria are branched miracidium passes through one sporocyst and
extensively.  two redial stages of development. Cercariae 
 

246   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Plate 5.8. Paragon imuswestermane

i gg; note the Plate 5.9. Ant 
eme a i asperata,first
l na
flattened operculum and the abopercular intermediate host of Paragon m i uswest erman i
portion (Courtesy of the Department of (Courtesy of the Department of Parasito Parasitology, logy,
Parasitology, UP-CPH)  UP-CPH) 
 

CHAPTER 5: Trematode Infections   247 

subsequently emerge from the snail to seek Following the ingestion of infected
and infect the second intermediate host, the crustacean tissue by the host, the metacercariae
metacercariae
mountain crab Sundath elphusa philippina of  Paragonimus excyst in the duodenum of
(Plate 5.10), formerly known as Parath
 Parathelphus
elphusaa the host. The immature worm then traverses
 grapsoides. The cercaria penetrates the soft parts through the intestinal wall into the peritoneal
of the crustacean and encysts as a metacercaria cavity, where it wanders about for several days
in the gills, body muscles, viscera or legs (Plate  and embeds itself in the abdominal wall. TheThe 
5.11). The crab may also be infected
i nfected by eating  parasite then returns to the coelom and migrates
infected snails. The definitive
definitive host
 host acquires through the diaphragm into the pleural cavity.
the infection by ingesting raw or insufficiently
insufficiently   A juvenile diploid worm wanders in the pleural  
cooked crabs harboring metacercariae.   spaces until it finds one or several diploid
worms. The pair or group then migrates into
the lung parenchyma to develop into adults in
about 6 weeks, where they mate and lay eggs.
Juvenile triploid worms in Japan, Korea, and
Taiwan can establish themselves in the lung
 parenchym a without a mate. Groups of diploid
 parenchyma diploi d
and triploid parasites have also been observed. 
In the lung parenchyma, a fibrotic capsule
forms around the parasite or their group. The
fibrotic capsule has openings that allow the eggs  

taor eem
scoa p toatnhde or eus p
vedinu p t bir 
yathoer ycitlr iacr yt w
e phiethr  eltihuemy
along with lung exudates. In the pharynx,
they are either coughed out or swallowed into
Plate 5.10. Sundathep
l husap p
hll 
i  na, the
 i pi  second
second
intermediate host of Paragon imuswestermani(Courtesy
( Courtesy
the alimentary canal to be passed out with
of the Department of Parasitology, UP- the feces. The completion of development in
CPH)  the definitive
definitive host
 host takes 65 to 90 days. Adult
worms are known to persist in humans for 20
years or longer.
Cysteine proteases have been found to
 play an important role in the development of
young parasites because of their involvement in
the metacercarial excystment, tissue invasion,
and immune modulation of the host. Cysteine
 proteases with masses of 27 and 28 kD are 
released from the excretory bladder of the
metacercariae during excystment. The proteases
are most abundant in the tegmentum of
newly excysted worms, facilitating migration  
through the tissues of the host. The 27 and 28
Plate 5.11. Paragon imuswese
t rman i
kD cysteine proteases are also found to cleave
metacercaria in crab heart muscle human immunoglobulin G, thereby creating
(Courtesy of the Department of Parasitology
Parasitology,, a zone of immune privilege around the worm.
UP-CPH)  As the juvenile parasite moves actively towards  
 

248   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

the lungs, additional proteases of 15, 17, and result in exudative aseptic inflammation,
53 kD are expressed. Protease activity decreases infarction, hemorrhage, and necrosis in the
as worm matures.   subcortical areas. After invasion, multiple,
conglomerated,
conglomerated, and interconnected
interconnected granulomas
granulomas
Pathogenesis and Clinical Manifestations   form around the parasite, containing abscess
In the lungs, Paragonimusworms provoke
 Paragonimus material and eggs. In the chronic stage,
a granulomatous reaction that gradually gives  liquefaction
liquefacti on necrosisand fibrinous glio
 gliosis
sis occu,r 
occu,r  
rise to the development of a fibrotic cyst and these may lead to cortical or subcortical
containing blood-tinged purulent material, atrophy, and secondary ventricular dilatation.
adult worms, and eggs. The most common Cerebral paragonimiasis may present with 
symptoms of paragonimiasis are chronic cough headache, meningismus, seizures, hemiparesis,
and hemoptysis. Chest pain, dyspnea, low-grade  blurring of vision, diplopia, homonymous
fever,fatigue, and generalized myalgia
myal gia may also hemianopsia, and aphasia.  
occur. 
Diagnosis 
Since it takes several weeks for the parasite
to migrate and mature, the early stages of the Microscopy is the most basic and
infection are usually asymptomatic. Clinical most readily available diagnostic tool for
symptoms are less severe after 5 to 6 years.  paragonimiasis.
 paragonim diagnosis is  based 
iasis. Definitive diagnosis
Occasionally, the disease can have serious on the detection of the characteristic eggs in
sequelae, such as chronic bronchiectasis and sputum, stool, or, less frequently, in aspirated
 pleural fibrosis, secondary to severe parenchymal  material from abscesses or pleural effusions. 
toaugser .oute of  migr ation allows the
and  ppTlheue r cailr cduaim H ow
su b ioincr ionscso p puytuism
o petviemr,alt,hewistehnsoitviavitdyetoef ctm
worms to lodge and mature in different ectopic ranging from 37 to 88%. If initial findings findings  are
locations. These aberrant worms may localize negative, repeat examinations may be helpful.
in the lung pleura, pericardium, myocardium, Sputum concentration with 3% sodium
abdominal wall, omentum, liver, mesenteric hydroxide, with repeated sputum examinations
hydroxide,
lymph nodes, adrenals, urogenital organs, and up to three times on different days, provides the
eyes. Heavy intensity infections can cause both  best sensitivity for microscopic diagnosis. 
 pulmonaryy and ectopic paragonimiasis.
 pulmonar paragoni miasis. Worms Chest radiographs may aid in the diagnosis
that fail to find  a mate in low intensity infections of pulmonary paragonimiasis when combined
may end up in ectopic locations as well.   with a high index of suspicion. Pulmonary
Cutaneous and cerebral paragonimiasis are  paragonomiasis usually presents as lung
the classic known forms of ectopic infection.  parenchymaa lesions which may be infiltrative,
 parenchym
In cases of cutaneous paragonimiasis, a slow- nodular, cavitating, or a combination of
moving, nodular lesion in the subcutaneous these. Pleural effusions occur in almost half of
tissue on the abdomen or chest is the  patients. These radiographic fi ndings ar e not
radio graphic findings
characteristic symptom.   specific, and may also be seen in other diseases,
Cerebral involvement
complication is the most serious
of human paragonimiasis. A  particular
 particularly
ly pulmonary
lung cancer, pul
andmonary tuberculos
tu berculosis
fungal infections. isSince
(PTB),
PTB
 juvenile P. westermani may migrate from the and paragonimiasis are usually co-endemic,
co -endemic,
 pleural cavity
cav ity into
int o the cranial
crani al cavity
cavi ty through
throu gh PTB should always be ruled out.  
the soft tissues along the internal jugular
j ugular vein. The peripheral blood count for
The migration worm can cause congestion,  paragonimiasis frequently reveals
 paragonimiasis reveals eosinophilia
eosinophilia
vasculitis, and capillary rupture, which may   and elevated levels of IgE, which is typical for  
 

CHAPTER 5: Trematode Infections   249 

 parasitic infection
i nfections.
s. The total white blood
bl ood cell In cerebral paragonimiasis, the most
count may be in the normal
norm al to elevated range. characteristicfinding in either cranial Computer
Eosinophilia is more common in the acute stage Tomography (CT)
(CT) scan or Magnetic Resonance
Resona nce
of paragonimiasis, whereas IgE levels have no Imaging (MRI) are conglomerated, multiple,
correlation with the stage of the disease.   ring-enhancing
ring- enhancing lesions (“grape-
(“grape-cluster”
Various immunological methods appearance) with surrounding edema, typically
have been developed for the diagnosis of   in one cerebral hemisphere, most commonly  
 paragonimiasis.
 paragoni miasis. Classic methods
metho ds include the in the posterior part of the brain. On skull
complement fixation (C F) test, intradermal radiographs, patients with chronic disease may
test, double diffusion in agarose gel, and   present with specific s oap-bubble
oap-bubble calcifications. 
immunoelectrophoresis. CF has high sensitivity
immunoelectrophoresis.
Treatment 
for both diagnosis and assessment of cure after
therapy. The intradermal test is simple, rapid, Praziquantel is the drug of choice. It is
cheap and highly sensitive, although it may still highly effective in the treatment of trematode
yield positive results several years after successful infections, particularly lung fluke infection. It
treatment.  induces rapid contraction of trematodes and
The classic methods for serodiagnosis of alters the tegmental surface (e.g., vacuolization).
 paragonimiasis
 paragoni miasis have been gradually
grad ually replaced
repl aced These changes are thought to be linked to
 by more sensitive and specific tests, like the drug-dependent disruption of calcium
immunoblotting (IB) and enzyme-linked homeostasis. Praziquantel is suitable for
immunosorbent assay (ELISA). IB has a  treatment of adults and children over 4 years of  
seincseiti1v9it8y8o. f EuL pIStAo  h9a9s%a, saendsithivaist b
y er eanguinsegd atigme.eU
s asudaalyd, of soer f 2or totr e3adtm hr aeye
ayesn. tAish2ig5hmer gd/kogs,etm
from 96% to 99%, and has been employed  be required in cases of ectopic paragonimiasis.  
widely in various parasitic and non-parasitic
non -parasitic Praziquantel is currently not recommended
infections. For paragonimiasis, most ELISA for the treatment of paragonimiasis during
systems were developed to detect Parago
 Paragonim us-
nimus  pregnancy and lactation, although current
specific IgG antibody. Attempts have also literature has not proven the drug to have
hav e
 been made to detect specific  IgE, IgM, and
specific IgE, mutagenic, teratogenic, or embryotoxic effects.
circulating antigens. The multiple-dot ELISA Treatment should preferably be given after
was developed for field use in developing
d eveloping delivery unless immediate intervention is
countries.  deemed essential. Breastfeeding should be
The loop-mediated isothermal avoided during and 72 hours after treatment.
amplification (LAMP) test is a si mple, rapid, Adverse effects of praziquantel are generally
and cost-effective method currently being mild, and these include abdominal discomfort,
developed for field use in epidemiologic surveys  nausea, headache, dizziness, and rarely,
r arely, fever,
in developing countries. LAMP allows the urticaria, drowsiness, and tachycardia.  
rapid amplification of deoxyribonucleic acid Triclabendazole
Triclabendazole is a benzimidazole
benzimidazole that was
w as 
(DNA) with high specificity under isothermal srcinally used for the treatment for  Fasciola
conditions, using DNA polymerase with   hepatica infections. Recently, triclabendazole
strand-displacement activity. Magnesium has been demonstrated to be an effective drug
 pyrophosphate, the reaction by-product, is against human paragonimiasis.
paragonimiasis. Triclabendazole
Triclabendazole
visible to the naked eye. Only warm water is  probably binds to B-tubulins of trematodes,
required to perform the assay.   leading to depolymerization and disruption of  
 

250   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

microtubule-based processes. These result in meat in Japan. Unhygienic food preparation also
damage to the external plasma membrane and contributes to the transmission of the disease. 
nuclear membrane, with dissolution of some Cultural beliefs and traditions influence the
heterochromatin, mitochondria, and Golgi age and sex distribution of paragonimiasis. In
complex. The cure rate with triclabendazole is Japan,
Japa n, during the 1950s and 1960s, the majority
comparable with that of praziquantel, and may of those infected were children because of the
result in better patient compliance since the    practice of using raw crayfish juice as a treatment 
treatment regimen consists only of a single dose.  for various cutaneous ailments. Similar practices
Bithionol can be used as an alternative   also existed in Korea during the same period.
drug. It is given orally at a dose of 15 to 25 Currently, middle-age Japanese men have the 
mg/kg, twice daily on alternate days, for 10 to highest prevalence due to their conservative
15 days. affinity for traditional dishes. In adolescent
girls in Cameroon, a popular belief existed
Epidemiology 
once among the Bakossi people that c rabs aid
Paragonimiasis has a focal distribution in in fertility, leading to disproportionately high
limited parts of Asia, Latin America (Peru and infection rates in this group.  
Ecuador), and Africa (Nigeria and Cameroon). PTB overlaps with paragonimiasis in
According to recent estimates, 20.7 million  paragonimiasis
 paragoni miasis endemic areas in the Philippines
Philippi nes
 people worldwide are infected, and 292.8 and other developing countries. Since PTB
million are at risk.  and pulmonary paragonimiasis share the same
In the Philippines, paragonimiasis is  symptoms, misdiagnosis and mismanagement 
eLnedyteem, iScaimnaM r oo, aCnagm
o b
r, iZnadm es,oSr toer ,soDgaovna,o
a  adr eiln N ator e enluoct iudnacteom
thm stuisdieasganr oesniseeodf ed
e oinm. pFaucr tthoef r  m
Oriental, Basilan, and Cotabato. Prevalence  pulmonary paragonimiasis and PTB.  
rates vary among the endemic provinces.  
Prevention and Control 
Infection rates in Sorsogon ranged from 16 to
25% in 1997. In more recent epidemiologic The most practical way to prevent
studies done in the municipality of Pres. Manuel acquisition of human paragonimiasis is to
Roxas in Zamboanga del Norte, theth e prevalence avoid ingestion of raw or insufficiently cooked
was 14.8% in 2005.  crabs and other crustaceans, as well as meat
Paragonimiasis has a focal distribution, from paratenic hosts like wild pigs. Safe food
largely determined by local patterns    preparation helps reduce
reduce the
the infectivity
infectivity of food.
of consumption of inadequately cooked Furthermore, it is believed that changing the
crustaceanss and paratenic hosts. Examples
crustacean risky dietary habits of the population, through
of dishes that can transmit disease include  health education and promotion, can control
kinagang (crab in coconut milk), sinugba
 sinugba (grilled this parasitic infection. Elimination of reservoir
crab), and kinilaw (raw crabs in vinegar) in the and intermediate hosts of Parago nimusmay not
 Paragonimus
Philippines, nam prik poo (crab and chilli paste)  be feasible. Capacity buildin
b uildingg of local health
in Thailand,
(drunken crabsininChina,
crabs) brine, kejang
soy sauce orcrabs
(raw alcohol
in
staff on the diagnosis and treatment of this
disease is important for early case detection
soy sauce) in Korea, ceviche (raw crabs in lemon and treatment.
sauce) in Peru, and sashim
 sashimii of wild boar and bear  
 

CHAPTER 5: Trematode Infections   251 

References  Doenhoff MJ, Cioli D, Utzinger J. Praziquantel:

mechanisms of action, resistance and new
Agatsuma T, Hirai H. Genetic variation of
derivatives for schistosomiasis. Curr Opin
 Paragonim
 Para us species. In: Arizono N, Chai
gonimus
Infect Dis. 2008;21:659 – 667.
7.
J, Nawa Y, Takahashi Y, editors. Food- Ikeda T, Oikawa Y, Owhashi M, Nawa  
Borne Helminthiasis in Asia. Vol 1, Asian Y. Parasite specific IgE and IgG levels
 parasitolo gy. Chiba (Japan):
 parasitology. ( Japan): Federation
Federatio n  in the serum and pleural effusion of  
Paar allsair tiolAo,gidstes;L2e0o0n5.W
Belizoaf r iAosiVan,  M  p., 1L5u5 – 
ce6r o5.   paragonimiasis
 paragonimiasis westermani patients.
patients. Am J
Trop Med Hyg 1992;47:104 – 7
7..
A. Assessment of the ef fi cacy, safety
and tolerability of praziquantel and
Infante AC, Jueco AL, Esparar DG, Villacorte
triclabendazole in the treatment of
EA, Pizarro MA. Basilan, a new endemic
 paragonimiasis.
 paragoni miasis. Southeast
Sout heast Asian J Trop foci for human paragonimiasis. Acta Med
Philipp. 1992;28:227 – 3 32.
2. 
Med Public health. 2007;38:97 – 
2007;38:97 – 105.
105. 
Jeon K, Koh W, Kim H, Kwon OJ, Kim TS,
Belizario V, Guan M, Borja L, Ortega AR,
Lee K, et al. Clinical features of recently
Tiri R. Pulmonary paragonimiasis in non- diagnosed pulmonary paragonimiasis in
responding tuberculosis patients in Irosin, Korea. Chest. 2005;128:1423 – 30.
30.
Sorsogon. Phil J Microbiol Infect Dis.
1997;26:13 – 6.
6.
Hotez PJ, Brindley PJ, Bethony JM, King CH,
Cabrera BD. Current status of
Pearce EJ, Jacobson
Jacobson J. Helminth
Helmi nth infections:
infections:
the great neglected tropical diseases. J Clin
 paragonimiasis
 paragoni miasis in the
t he Republic
Repub lic of the
th e Investig. 2008;118:1311 – 21.
21.
Philippines. Arzneimittelforschung.
Arzneimittelforschung.
1984;34(9B):1188  – 92.
92.  SY, K 
KangSW SJ,.K AimcaTsYe ,oYf ocuhnr go-nIlicHcAe,r C
HiomngTK  e bhr oali
Calvopina M, Guderian RH, Paredes W,  paragonimiasis westermani. Korean J
Chico M, Cooper PJ. Treatment of
Parasitol. 2000;38(3):167 – 7
71.
1. 
human pulmonary paragonimiasis with Kaw GJ, Sitoh YY, Yamashima T, Yamashita J.
triclabendazole: clinical tolerance and
Clinics in diagnostic imaging (58). Chronic
drug efficacy. Trans R Soc Trop Med Hyg. cerebral paragonimiasis. Singapore Med J.
1998;92:566-9. 
2001;42:89-91. 
Cha SH, Chang KH, Cho SY, Han MH, Kong
Keiser J, Engels D, Buscher G, Utzinger J.
Y, Suh DC, et al. Cerebral paragonimiasis
paragon imiasis Triclabendazole for the treatment of
in early active stage: ST and MR features. fascioliasis and paragonimiasis. Expert
Am J Roentgenol. 1994;162:141 – 5. 5.
Opin Investig Drugs. 2005;14:1513 – 226.
6.  
Cheng Y, Xu L, Chen B, Li L, Zhang R, Lin
Keiser J, Utzinger J. Emerging foodborne
fo odborne
C, et al. Survey on the current status of
trematodosis. Emerg Infect Dis.  
important human parasitic infections in  
2005;11:1507 – 114.
4.
F20u ji05an;23P:r 2o8v3i – 
nc7e..  Chinese  J  Par asitic  Dis.  Li HZ, Xie FW,
FW, Sun SC. CT findings in ‘‘fresh’
Cho S, Kong Y, Kang S. Epidemiology of cerebral paragonimiasis.
paragonimiasis. No Shinkei
S hinkei Geka
 paragoni miasis in Korea. Southeast
 paragonimiasis Southeas t Asian 1992;20:91 – 7 7.. 
J Trop
Trop Med Public Health. 1997;2
1997;28:32
8:32 – 6.
6.  Mukae H, Taniguch
Taniguchi i H, Matsumoto
Matsumo to N, Iiboshi
Chung Y, Kim T, Yang H. Early cysteine
c ysteine
H, Ashitani J, Matsukura S, et al. Clinico-
C linico-
 protease activity
activity in excretory
excretory bladder trigger
trigger
radiologic features of pleuropulmonary
 Paragonimu
 Parag onimuss wester manion Kyusyu Island,
westermani
metacercarias
metacerc arias excystment of  Parago
 Paragonimus
nimus
Japan. Chest. 2001;120;514 – 20.
20.
westermani . J Parasitol. 2005;91:953 – 4.
4.  
 

252   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 Nakamura-Uchiyama F, Mukae H, Nawa Y. of praziquantel during pregnancy/lactation

Paragonimiasis:
Paragonimiasis: a Japanese perspective. Clin and albendazole/mebendazole
albendazole/mebendazole in children
Chest Med. 2002;23:409 – 20.
20.  under 24 months. Geneva: World Health
Health
 Nakamura-Uchiyama F, Onah DN, Nawa Y. Organization; 2002. 
Clinical features of paragonimiasis cases Yokogawa M. Paragonimiasis. In: Steele JH,
recently found in Japan: parasite-specific editor. CRC handbook series in Zoonosis,
immunoglobulin M and G antibody   Section C: parasitic zoonoses. Boca Raton, 
classes. Clin Infect Dis. 2001;32:e171 – 5.
5. Florida: CRC Press; 1982. p. 123 – 
123 – 6
64.4.
Toyonaga S, Kurisaka M, Mori K, Suzuki   Yoonuan T, Vanvanitchai Y, Dekumyoy P,  
 N. Cerebral paragonimiasis
paragoni miasis-report
-report of
of Komalamisra C, Kojima S, Waikagul J.
five cases. Neurol Med Chir (Tokyo). Paragonimiasis prevalences in Sarabuti
1992;32:157 – 62.
62.   province, Thailand, measured 20 years
Udonsi JK. Endemic Parag onimuss infection in
 Paragonimu apart. Southeast Asian J Trop Med Public
upper Igwun Basin, Nigeria: a preliminary Health. 2008;39(4):593 – 600.600.
report on a renewed outbreak. Ann Trop Zhang Z, Zhang Y, Shi Z, Sheng K, Liu L, Hu
Med Parasitol. 1987;81:57 – 662.
2. Z, et al. Diagnosis of active Paragonimus
World Health Organization. Preventive westermani infections with a monoclonal
chemotherapy in human helminthiasis: antibody-based
antibody-based antigendetection assay. Am
coordinated use of anthelminthic drugs in J Trop Med Hyg. 1993;49:329 – 34.
34.
control interventions: a manual for health Zuazula JN, Roces MC,Fantone J, Belizario VY,
 professionals
 professio nals and programme
pr ogramme managers.
ma nagers.   Cho SY. Chronic cough in San Alfonso,  

ldenHeeval:tW
Wor G r ldr gH
h oO onr g. aR 
a neaizltahtiO zaotir otno; 2f  0t0h6e.
nie p Ca0te0e.l,M
20 ili  ppo pr tien.eIsn):teDr ne palaR 
Danvialao d(Pehl  N  peonr t
r tem
WHO informal consultation on the use   of Health; 2000. 
 

CHAPTER 5: Trematode Infections   253 

Intestinal Flukes
Vicente Y. Belizario, Jr., Percy G. Balderia

Fasciolopsisbuski duodenum and attaches to the intestinal wall,

where it becomes sexually mature in about 3  
his fasciolid digenetic trematode is the months. The adult worm lives in the duodenum,
T  largestintestinal fluke of humans and pigs. 
Parasite Biology 
attached to the intestinal mucosa by its suckers
(Figure 5.4). In heavy infections, the worms
may be found throughout the intestinal tract.  
The mode of transmission of Fascio
 Fasciolopsis
lopsis Immature eggs are released together with feces
buski is by ingestion of encysted metacercariae into the water. The egg, which embryonates
emb ryonates in
from aquatic plants. This can occur when the water, gives rise
r ise to a miracidium
mir acidium in
i n 3 to 7 week.s
week.s
 plant itself is eaten, or when the hull or skin of The miracidium then seeks out and infects
the fruits of these plants is peeled off between its first
first intermediate
 intermediate host, a snail belonging
the teeth. The viable metacercaria excysts in the   to either the genus Segmentina or Hippeutis.

Figure 5.4. Life cycle of Fasciolopsisbuski

 

254   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Inside the snail, the miracidium transforms The egg is large, operculated, unembryonated
into a sporocyst, which subsequently produces when first passed, and indistinguishable from
mother rediae, daughter rediae, and finally, eggs of  F. hepatica and  F. gigantica. It measures
gigantica
cercariae. Cercariae leave the
cercariae. th e daughter rediae 130 to 140 µm by 80 to 85 µm.  
and undergo further development in the snail Pathogenesis and Clinical Manifestations  
tissues. Seven weeks after infection, cercariae
emerge from the snails into water. Cercariae  Pathological changes caused by the  
attach themselves and encyst as metacercariae
metacercariae on worms are traumatic, obstructive, and toxic.
the surfaces of seed pods, bulbs, stems, or roots Inflammation and
Inflammation  and ulceration occur at the site
of various aquatic plants such as Trapa bicornis  of worm attachment, producing an increase
(water caltrop) (Plate 5.12), Elioch
 Eliocharis
aris tubero
tuberosa
sa in mucus secretion, and minimal bleeding.
(water chestnut), Ipomea
 Ipomea obscura(morning glory Gland abscesses are occasionally formed in the
or kangkong ),), and Nymph
 Nymphaea
aea lot us(lotus). These
lotus mucosa. In heavy infections, the worms may
 plants serve as the second intermediate hosts of cause intestinal obstruction. Intoxication results
the parasite. Pigs and humans are the important from the absorption of worm metabolites by the
definitive hosts.
definitive  hosts.  host. The patient experiences generalized toxic
and allergic symptoms, such as edema of the
face, abdominalwall, and lower limbs.
li mbs. Profound
intoxication can result in death of the host. 
Diagnosis 

  is   bby  detection  oef g pgasr ar esisteeme bglges 

in  thDe iastgonools. is Fasci
 Fasciolopsi buski 
olopsiss buski
 Fasciola eggs under the microscope.  
Treatment 

Praziquantel is given in three doses of 25

mg/kg over 1 day. Minimal side effects are
associated with the drug. There may be episodes
of epigastric pain, dizziness, and drowsiness,
Plate  5.12.  T 
apa bc 
r  ni s,  se c ond inter me diate
i or 
which typically disappear within 48 hours. In
host of Fasciolopsisbuski (C (Courte
es
sy of the a study carried out in Central Thailand, 100%
Department of Parasitology, UP-CPH)  cure rates were demonstrated for regimens
of 15, 25, and 40 mg praziquantel per kg
 F. buski is elongated, oval in shape, and    body weight. Until further studies show the
efficacy  of the 15 mg/kg regimen, the authors
inr ews i2d0tht.o C7o5 m pm
memasu gtah s,ciaonlad h8e ptoat 2ic0a
ar eind lteon F  still recommend a dose of 25 mg/kg for the
and F. gigantic
gigantica a, it does not have a cephalic treatment of fasciolopsiasis. 
cone, and its intestinal ceca are unbranched and Epidemiology 
reach up to the posterior end. The two testes
are dendritic, and are arranged in tandem in the Fasciolopsiasis is endemic in the countries
 posterior half of the body. The branched ovary of Southeast Asia, China, Korea, and India.
Ind ia.
lies to the right of the midline.
midlin e. Fine vitelline Its endemicity in the Philippines has not
follicles are situated throughout the lateral yet been demonstrated. No locally acquired
margin of the bo body.
dy. fascioliopsiasis in humans or pigs has been  
 

CHAPTER 5: Trematode Infections   255 

reported. Fasciolopsiasis
Fasciolopsiasis in Filipinos were and consumption could also be prolonged to
 probably acquired abroad.   prevent infection. Washing of the plants to
remove metacercariae, or boiling them to kill
Prevention and Control 
the parasites can also prevent
pr event infection
infection.. Swamps
Since metacercariae are very sensitive to or ponds where aquatic plants are cultivated
dryness, soaking of aquatic plants in water should be protected from pollution by untreated
should be avoided. The time between
b etween harvest  human or pig excreta. 
 

256   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Echn
i ostomao
 li canum
 Artyfechi 
nostomumma layanum

 
he echinostomids are digenetic trematodes wall of the small intestine, where they
t hey develop
characterized
characterized by a collar of spines around   into sexually mature adult worms. 
their oral suckers. There are several species The adult worms live in the small intestine
T 
which infect humans. Two species have been
documented in the Philippines. 
of the definitive host (e.g., humans, dogs, cats,
rats, and pigs). Immature eggs released by the
 parasite are transported
transpor ted to the environment
environ ment with 
Parasite Biology 
the feces. The egg matures in water, and after 6
The mode of transmission of Echino
 Echinostoma
stoma to 15 days, a miracidium hatches from the egg
ilocanum and Artyfechinos tomum malayanum is
 Artyfechinostomum to infect the first snail intermediate host. Inside
 by ingestion
ingestion of metacercariae
metacercariae encysted in snails,
snails, the snail, the E. ilocanum
ilocanum miracidium develops
the second intermediate hosts of the parasites. into mother rediae, which subsequently
When the metacercariae reach the duodenum,  produce daughter rediae and cercariae after 42
they excystand the juvenile fluke attaches to the  to 50 days. The A. malayanum miracidium
miracidiumfirst
first 
 

CHAPTER 5: Trematode Infections   257 

develops into a sporocyst, which subsequently

 produces mother rediae,
red iae, daughter
daught er rediae, and
cercariae. After escaping from the snail, cercariae
swim in water to seek
snail intermediate out
host, inand infect
which theythe second
transform
into metacercariae. The metacercaria is the
infective stage to the definitive host (Figure 5.5). 
In the Philippines, the first snail
intermediate host
h ost sspecies
pecies of  E. ilocanum
are Gyraulus convexiusculus and Hipp  Hippeutis
eutis
umbilicalis . The second snail intermediate  
Plate 5.14. Echinostomailocanumadult
hosts are Pila luzonica (kuhol ) (Plate 5.13) and (Courtesy of the Department of Parasitolog
Parasitology,
y,
Vivipara angularis ( susong pampang ). ). The fisrt UP-CPH) 
snail intermediate host species of A. malayanum
malayanum
in the Philippines has not yet been identified, quarter of the body. The ovary is located just in
 but is suspected to be the same as that of E. front of the anterior testis. Follicular vitellaria
ilocanum. However, it has been confirmed that are located in the posterior half of the body, and
the second snail intermediate hosts are either uterine coils are found between the ovary and
 Lymnaea
 Lymnae a(syn.  Bul
 Bullastra) cumingiana(birabid ) or
lastra the ventralsucker. The intestinalceca are simple. 
 Ampullariu
 Ampul lariuss canaliculatuss (golden apple snail). 
canaliculatu  A. malayanum measures 5 to 12 mm in
length and 2 to 3 mm in width. It has a rounded
 posterior end and has 43 to 45 collar spines.
The two testes are large, each with
w ith six to nine
lobes arranged in tandem. The ovary is small,
rounded or oval, located anterior to the
th e testes,
and pre-equatorial (Plate 5.15). 
The  E. ilocanum egg is straw-colored,
operculated, and ovoid, measuring 83 to 116  
µm by 58 to 69 µm, whereas the A. malayanum
egg is larger, golden brown in color, operculated,
and measures 120 to 130 µm by 80 to 90 µm.  

Plate 5.13. Pi 

l zon ica,second intermediate
l 
au
host of Ech n i ostomall 
o
 i canum
(Courtesy of the Department of Pa rasitology,

UP-CPH)

 E. ilocanum (Plate 5.14) is reddish-gray 

and measures 2.5 to 6.6 mm in length and 1 to  
1.35 mm in width. The worm is tapered at the
 posterior end and has 49 to 51 collar spines. The
The
oral sucker lies in the center of the circumoral
disk, and the ventral sucker is situated at the Plate 5.15.  Arytt fe
 chn
iostomumma layanum adult
anterior fifth
fifth of
 of the body. The two testes are (Courtesy of the Department of
deeply bilobed, arranged in tandem in the third  Parasitology, UP-CPH) 
 

258   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Pathogenesis and Clinical Manifestations   The endemicity of both parasites is related to

the eating habits of the population. E. ilocanum
In heavy infections, inflammation develops infection is endemic in Northern Luzon, Leyte,
at the site of attachment of the adult worm to the  A.
intestinal wall. Ulceration, and consequently, Samar, andinfection
malayanum the provinces of Mindanao.
in the Philippines was first
diarrhea, which is sometimes bloody, as well
documented in humans in 1987, and has since
as abdominal pain may also develop. The  
 been reported in Northern and Central Luzon. 

r a bessuolr  p aleitna btooxlicteastif or nom
t itniognenoef r m .  the worms may   In 2005, a study in Siargao Island, Surigao
del Norte, showed  A. malayanum in 11.4%
Diagnosis  of individuals suffering from gastrointestinal 

disturbance. All infected patients had a history

Diagnosis is by detection of eggs in the of having eaten snails ( kuhol and kiambuay )
stool. Notably, the eggs of echinostomes,
 prepared raw with coconut milk and lime juice.  
la, and Fascio
 Fasciola
 Fascio lopsis buski look very much
 Fasciolopsis
The second snail intermediate hosts are
alike, although the latter two are bigger in
i n size.  abundant in rice fields
fields especially
 especially during the
Treatment  wet months. The rat is probably an important
reservoir host of both echinostomes. 
Three doses of praziquantel may be given
at 25 mg/kg per dose
dos e over 1 day.  Prevention and Control 

Epidemiology  Preventive
avoiding measures
ingestion of raw involve mainly 
or improperly
These two parasites have been reported in
other Southeast Asian and East Asian countries.  coaor akseitdes.econd inter mediate snail hosts of  these 
 p
 

CHAPTER 5: Trematode Infections   259 

Heterophyid Flukes

here are many species of heterophyids that The adult worm inhabits the small intestine
live in the intestines of fish -eating hosts.  of the definitive host. Large numbers of  
The major species are Hetero
 Heterophyes
phyes he
heter
terop hyess,
ophye eggs are produced and passed out into the
T 
 Metagonimus
 Metago nimus yo kogawaii, Haplorchis
yokogawa
 Haplorchis yokogawaii.
yokogawa
 Haplorchis ttai
aichui, and
chui environment together with feces. The eggs
hatch into miracidia after ingestion by the first
snail intermediate host. Inside the snail, the 
Parasite Biology 
miracidia develop further into sporocysts, which
The mode of transmission of heterophyids eventually develop into one or two generations
is by ingestion of metacercariae encysted in fish of rediae that give rise to cercariae.  
(Figure 5.6). When the metacercariae
metacercariae reach the Cercariae that are liberated from the
duodenum, they excyst, liberating young larvae snail encyst as metacercariae on or under the
that attach to the intestinal wall. The
T he larvae scales, in the muscles, fins, tails, or gills of fish
subsequentlyy develop into
subsequentl i nto sexually mature adult species that serve as second intermediate hosts.
worms that have a typically short life span of Metacercariae are frequently found in the
less than 1 year.  muscles at the base of the fin. 
 

260   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

The snail hosts can be freshwater, brackish

water, or marine species. In the Philippines,
P hilippines,
the snail hosts of H. taichui and Procerovum

calderoni
 juncea areThiara
, and the brackish
riquettiwater snails, Melani
 Melania
, respectively. Thea
local snail intermediate host species of other
heterophyid parasites have not yet been
identified.  
identified.
In the Philippines, there are at least 30
known species of fish harboring metacercariae
of 21 heterophyid species (Table 8.2). The
adult fluke is elongated, oval or pyriform,
and it measures less than 2 mm in length. Plate 5.17. Heterophyid egg
(Courtesy of Prof. Winifreda U. de Leon)  
The tegument has fine scale-like spines. Some
species have a gonotyl or a genital sucker that
is located near the left posterior border of the Pathogenesis and Clinical Manifestations  
ventral sucker. Testes,
Testes, variously arranged, are in There is usually inflammation at the sites
the posterior end of the body; and the ovary,
ov ary, where the worm is attached to or burrowed
globular or slightly lobed, is located in the in the mucosa. Excessive mucus production
p roduction
submedian, pre- or post-testicular area (Plate and sloughing off of the superficial layers may
5.16). 
occur. In a study done in Compostela Valley  
in Southern Mindanao, the most common
clinical manifestations observed were consistent 
with peptic ulcer disease (PUD) or acid peptic
disease (APD). These included
i ncluded upper abdominal
discomfort/pain, reported by 42.2% of patients,
and gurgling abdomen, which was found in
24.1% of patients. Colicky abdominal pain and
mucoid diarrhea may also be present.
A report by Africa in 1931 showed that
worms tend to burrow deep into the intestinal
wall, where they become trapped and eventually
Plate 5.16. Heterophyid fluke adult die. Eggs of degenerating worms may be
(Courtesy of the Department of Parasitology,  filtered through
filtered  through the intestinal lymphatics and
UP-CPH)  blood vessels and may be deposited in various 
The egg is light brown in color, ovoid in thiassssvuee bs.eeEnggo  b etr r o a ppnhdy bidr sain  of
sbasenr dveaduinltsthoef   heatr 
shape, operculated,
operculated, and measures 20 to 30 µm Filipino patients who died of heart failure and
 by l5 to 17 µm (Plate 5.17). A fully developed, intracerebral hemorrhage. Eggs lodged in the
symmetrical miracidium is already present spinal cord may result in sensory and motor
within the egg when it is deposited by the adult losses at the level of the lesion.  
worm. The operculum fits
fits into
 into the eggshell
Diagnosis 
smoothly, and it does not have an abopercular
 protruberance, in contrast to Clonorchis and Considering the similarity in presentation
Opisthorchis eggs. of heterophyidiasis with APD, it is important 
 

CHAPTER 5: Trematode Infections   261 

to consider intestinal fluke infection when  Haplorchis

 Haplor taichui. Infection rates were high in
chis taichui
dealing with bowel disturbance and a history of  both males and females, and in all age groups,
group s,
consumption of raw fish. Definitive diagnosis especially the working age group. Children

is by detection
modified of eggs
 Kato thick in the
method, stoolhas
which using the
a higher and the elderly
Intestinal were not spared
heterophyidiasis hasof infection.
since then
sensitivity compared to formalin-ether/ethyl  been recognized as an emerging
emergin g public health
acetate concentration technique (31.0% vs.  concern in the southern part of the Philippines. 
13.6%). The eggs of the different heterophyid Altogether, eight provinces in two regions of
species are difficult to distinguish. Care  must Mindanao have reported thousands of cases to
 be taken to distinguish them from Clonorchis
Clonorchis   date. High prevalence levels were detected in  
and Opisthorchis eggs. Heterophyid eggs have areas where investigations for an outbreak of
also been referred to as Opisthorchid-like eggs intestinal capillariasis were being conducted. 
where the liver fluke
fluke is
 is endemic.  
Prevention and Control 
Polymerase chain reaction (PCR) may be
useful as a sensitive diagnostic tool, particularly Preventive measures include avoiding
for low-intensity heterophyid infections.  ingestion of raw or improperly cooked fish.
It may be difficult to change eating habits.
Treatment 
Capacity building of laboratory staff will help
Praziquantel is the drug of choice, given at in early diagnosis when doing routine stool
25 mg/kg per dose, three doses
do ses in 1 day.  examination. This will facilitate provision of
appropriate treatment. Surveillance
Surveillance in other  
Epidemiology 
The parasite has been reported in Egypt,  br eegcioonnssiwdher eer de.r aw
aw fish (kinilaw
la w) is eaten should 
Greece, Israel, Western India, Central and
References 
South China, Japan, Korea, Taiwan, and the
Philippines. Its worldwide distribution may be Africa CM. Ev idence of intramucosal
due to the fact that heterophyids have adapted invasion in the life cycle of  Haplorchis
to snails belonging to various families, and are  yokogawai (Katsuta, 1932) Chen, 1936
not very specific
specific with
 with respect to their second (Heterophyidae). J Philipp Med Assoc
intermediate hosts. Both intermediate hosts 1937;17:737 – 4
43.
3. 
may be found in different habitats (fresh, Africa CM, Garcia EY. Intestinal heterophyidiasis
 brackish, and salt waters), and in different with cardiac involvement. Phil J Public
climates. Reservoir hosts include dogs, cats, Health. 1935;2:1 – 2
22.
2. 
and birds.  Belizario VY Jr, Geronilla GG, Anastacio MB,
In the Philippines, the prevalence was de Leon WU, Suba-an AP, Sebastian AC,
 previously
 previous ly considered low, and its distribution
distribu tion et al.  Echinostoma malayanum
ma layanum infection,
spotty, as shown by previous parasitologic the Philippines. Emerg Infect Dis.  
surveys. In the 1980s, less than 1% of 30,000 2007;13(7):1130 – 1 1..
stools examined in surveys done nationwide Belizario VY Jr, Bersabe MJ, de Leon WU,
were found positive for heterophyid ova. A more Hilomen VV, Paller GV, de Guzman AD
recent parasitologic survey done in 1998 in Jr, et al. Intestinal heterophyidiasis: an
Monkayo, Compostela
Compostela Valley,
Valley, however, revealed
reve aled emerging food-borne parasitic zoonosis in
31% prevalence with a majority of those Southern Philippines. Southeast Asian J
infected having moderate to heavy intensities Trop Med Public Health. 2001;32(Suppl
of infection. The species was identified as   2):36 – 42.
42. 
 

262   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Centers for Disease Control and infections in a Lao community in an area of

Prevention. Laboratory identification endemicity and comparison of diagnostic
of parasites of public health concern methods for parasitological field surveys.

[Internet]. 2011
Available [cited
f rom 2012www
http:// Mar. 3].
www. dpd.  ClinE.A.
Malek, Microbiol. 2009;47(5):1517
Snail-transmitted  – 23.
23.
parasitic  
diseases.  
cdc.gov/dpdx/HTML/Para_Health.htm  Philadelphia: CRC Press; 1980.  
Cross JH, Basaca-Sevilla V. Biomedical surveys   Markell EK, John DT, Krotoski WA. Markell  
in the Philippines. Manila (Philippines): and Voge’s Medical Parasitolgy. 8th ed.
US Naval Medical Research Unit No. 2; Philadelphia: W.B. Saunders Company;
1984.  1999. 
Drugs for Parasitic Infections.Published
Infections.Published by The Monzon, RB, Kitikoon V. Lymnaea
 Lymnaea ( Bullastra
 Bullastra)
Medical Letter, Inc [Internet]. 2010 [cited cumingiana Pfeiffer (Pulmonata:
2012 Mar 3]. Available from:
from: http://www. Lymnaeidae): second intermediate host of
medletter.com.   Echinostom
 Echinostomamala yanum in the Philippines.
amalayanum
Harinasuta T, Bunnag D, Radomyos Southeast Asian J Trop
TropMed Public Health.
P. Efficacy of praziquantel on 1989;20:453 – 60.
60.
fasciolopsiasis.. Arzneimittelforschung.
fasciolopsiasis Arzneimittelforschung. Tangtronghitr A, Monzon RB. Eating habits
1984;34(9B):1214 – 5.
5 .  associated with  Echinostoma malayanum
malay anum
Lovis, L, Mak TK, Phongluxa K, infection in the Philippines. Southeast Asian
Soukhathammavong P, Sayasone S, J Trop
Trop Med PublicHealth. 1991;22
1 991;22:212
:212 – 66.. 
Akkhavong K, et al. PCR diagnosis of  
Opisthorchis viverriniand Haplo
 Haplorchis taichuii 
rchis taichu
 

CHAPTER 5: Trematode Infections   263 

Liver Flukes
Vicente Y. Belizario, Jr., Raezelle Nadine T. Ciro

Fasciolaspp.  The adult worm lives in the biliary

 passages of the liver. Unembryonated eggs  
hese large digenetic trematode species are carried by the bile through the sphincter
T   belong to
t o family Fasciolida
F asciolidae.
e. They are  
 parasites found in the liver and biliary
biliar y passages
of Oddi into the intestine and subsequently
voided with the feces. The eggs mature in
of humans and herbivorous mammals, especially water within 9 to 15 days optimally at 15
1 5 to 
ruminants. Fasciola hepatica (temperate liver 25°C, forming a viable miracidium that escapes
fluke) and  F. gigantica (tropical liver fluke) through the operculum of the eggshell to seek
are the causative agents of fascioliasis. Reports out and infect the first
first intermediate
 intermediate host, a
of fascioliasis date back to 1379, and the  snail belonging to family Lymnaeidae. Snail
first detailed
first  detailed descriptions of F. hepatica were hosts for  F. hepatica are amphibious which
 published
 publish ed in 1523. The presence of F. hepatica
hepatica are usually found living on mud. Snail species
flukes in humans was first documented in include Lymnaea trunca tula(Europe and North
truncatula
1760, during an autopsy of a female in Berlin, Asia), L. bulmoides (North America), and
Germany.   tomentosa (Australia). Snails from family  
 L. tomentosa
Infections in ruminants result in significant
significant    Planorbidae also act as an intermediate host 

eceor naonm
 p nuicmlostsoer 
su alataegdr iactu3lt.u2 b
tir m r ailllciom mSundiotlileasr s
n U othf e F fi. r hset piant tiecar m peodr iaadteicahlolys.tsOf onr t F 
s p thaenr tihcaanadr e,
h.e  g oi g 
and commercial producers. In tropical countries, aquatic snails, living in slow-moving bodies
fascioliasis is considered the most important of water, which include  L. auriculari auricularia a (Asia), 
helminth infection of cattle with a reported ac uminata (Indian Subcontinent), and  L.
 L. acuminata
 prevalence ranging from 30 to 90%.  natalensis (Africa). In the Philippines, the snail
hosts of Fasciola spp. are L. philippinensis and 
Parasite Biology 
rubiginosa.
 L. auricularia rubiginosa
The mode of transmission of F. hepatica Inside the snail, the miracidium develops
and F. gigantica is through the ingestion of into a sporocyst, followed by one or two
metacercariae encysted on edible aquatic plants
metacercariae generations of rediae which produce cercariae.
or by drinking water with viable metacercariae.
metacercariae. Cercariae leave the snail about 5 to 6 weeks after
Upon ingestion, the metacercaria excysts in the the miracidium entered. After escaping from the
duodenum or jejunum, liberating the juvenile snail host, usually at night, the cercaria swims in
fluke, which, in turn, penetrates the intestinal water, detaches its tail, and encysts in surfaces 
wall to reach the peritoneal cavity where
w here it of aquatic plants forming a metacercaria. The
wanders over the viscera until it penetrates aquatic plants serve as the second intermediate
the capsule of Glisson and enters the liver.   hosts of the parasite. These include  Ipomea
The parasite then burrows through the liver obscura (morning glory or kangkong ) and
 parenchyma,
 parenchym a, feeding and growing
growin g until it finally  Nasturtium officinale (watercress). Cercariae
enters the bile ducts where it becomes sexually can also encyst freely in water. The metacercaria
mature in 3 to 4 months (Figure 5.7). The life is the infective stage to the definitive  hosts.
definitive hosts.
span of the adult worm is 9 to 13 years.   In the presence of sufficient moisture, the  
 

264   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

metacercariae will remain alive for many weeks,

metacercariae to the whole lateral field of the hind body. The
depending on the temperature. They survive intestinal ceca are long and highly branched,
longer at a temperature below 20°C; higher extending to the posterior end of the body.
temperatures and desiccation will destroy the Compared to  F. hepatica, the F.gigantica
metacercariae in a short time.   adult worm is longer (25-75 mm), with about
 F. hepaticahas a large, broad, and flat body
hepatica the same width (3-12 mm), with less developed
which measures 18 to 51 mm in length and 4   shoulders, and a shorter cephalic cone. The 

tdoist1i3ngm f f eiadttuhr e(insetahr etch ph
shiing w
uim ic-  bbcondey)w. hAich
e maild cmeicdalianr e  m
of otrr he  e b
 b brr a ondcyheadndes  ptpheecia
 blr layntcohweasr odf s the
has a marked widening at the base of the cone ovary are longer and more numerous. The
(“shoulder”). The suckers are comparatively average distance between the posterior testes
small and are located close to each other in the and the posterior border of the body is longer. 
conical projection. The two testes are highly The F. hepatica egg (Plate 5.18) is large,
 branched occupying the second and third ovoidal, operculated, and yellowish to brownish
quarters of the body. The
The ovary is dendritic and in color. It measures 140 to 180 µm by 63 to 90 
situated in front of the anterior testis. The uterus µm in size and is released from the worm still
is coiled and relatively short. Vitellaria extend   immature, containing a large unsegmented mass  
 

CHAPTER 5: Trematode Infections   265 

worm causes obstruction and stimulates

inflammation in the biliary epithelium  which
subsequently causes fibrosis. The thickened

fibrousout
 passed ducts,
buildiinngturn,
building cause
up back less bile
pressure. to be
In heavy
infections, atrophy of the liver parenchyma and
concomitant periductal cirrhosis ensue. The 
wall of the bile duct may be eroded allowing
the worms to re-enter the liver parenchyma
and cause large abscesses to develop. Other 
O ther  
Plate 5.18. Fasciola egg complications include obstructive jaundice,
(Courtesy of the Department of Parasitology, 
UP-CPH)
hemobilia, and biliary cirrhosis. Associated
lithiasis of the bile ducts or gallbladder is also
common, as the eggs or fragments of dead
of vitelline cells. The F. giganticaegg is slightly
gigantica  parasites can form nuclei for calculi. Another
Anot her
larger than the F.
 F. hepatica egg (160-190 µm by
hepatica rare complication of fascioliasis is acute
70-90 µm).  pancreatitis.
 pancreatit is. In some cases, this phase is only
onl y
diagnosed during a surgery. 
Pathogenesis and Clinical Manifestations 
During the migration from the intestine to
Two clinical stages are recognizedin human the liver, the parasite may wander or be carried
fascioliasis. An acute stage, which coincides
coincides  hematogenously (after it had penetrated a  

w ar vatailcmtiisgsr uaet,ioanndanad  cwhor or m
thiethhle p nicmsattaugr  iohnicinh
ea, tw , itchesi bter sasiunc, hanasdththeeluonrbgsi,t
 bsul boocdutvaensesoelu)stotisescuteo p
coincides with the persistence of Fasciola worms where abscesses or fibrotic lesions may also
in the biliary ducts.  result. 
The acute or invasive phase of human Another unusual form of fascioliasis can
fascioliasis corresponds to the migration of occur after ingestion of raw  Fasciola-infected
 Fasciola
the juvenile parasite from intestine to the liver liver. Flukes surviving mastication attach to
where it burrows into the liver parenchyma. the posterior pharynx, causing hemorrhagic
The damage caused by the parasite penetrating nasopharyngitis and dysphagia, known as
through the intestinal wall and migrating halzoun in Lebanon and marrara in Sudan. 
towards the liver is not significant. However, Diagnosis 
traumatic and necrotic lesions are produced
when the parasite burrows through the liver In majority of cases, diagnosis of the
 parenchyma.
 parenchym a. Theseverity of the injury depends infection, whether in the acute or chronic phase
on the number of metacercariae ingested by   is difficult because of overlapping symptoms,
the host. Though this invasive phase can be or because of lack of symptoms. This is
asymptomatic, patients have been known to compounded by the intermittent passage of eggs
experience dyspepsia, fever, and right upper  by the adult worm. Determining the phase of
quadrant abdominal pain. Sudden onset of high infection will therefore depend on the clinical
fever, hepatomegaly, and marked eosinophilia suspicion. A history of eating raw, improperly
form a triad of diagnostic significance.  cooked freshwater vegetation or of living in
The chronic or latent phase is asymptomatic or travel to an endemic area is suggestive of
and corresponds to the period when the parasite infection. Selection of adequate serological and
has already reached the bile ducts. The
Th e adult  coprological methods can help determine the 
 

266   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 phase of infection when applied to the acute nodules and tunnel-like branching hypodense
or chronic stages, respectively.   tracts. Hepatic sonographic findings have been
Differentials for human fascioliasis described as small clustered hypoechoic
hypoechoic lesions
include diseases which
similar symptoms such as may
acutepresent with
viral hepatitis, with poorly
nodular The contours
defined
lesions. andofhypoechoic
biliary phase the disease
schistosomiasis, visceraltoxocariasis, biliary occurs in the presence of parasites in the biliary
tract diseases, and hepatic amebiasis.  system. Sonography is the useful method in the  
Parasitological diagnosis may be made detection of biliary lesions. The oval shaped,
through the identification of eggs in stool, leaf-like, or snail-like echogenic structures
duodenal contents, or bile, or the recovery of   with no acoustic shadowing in the gall bladder  
adult worms during surgical exploration, after or common bile duct have been described
treatment, or at autopsy.However, the eggs
egg s may as characteristics of fascioliasis.
fascioliasis. Endoscopic
 be present in very small numbers at irregular retrograde cholangiopancreatography (ERCP)
intervals and thus may be difficult to
to find. Eggs can also be used in diagnosing fascioliasis in the
may also be transiently present in the
t he stool after  biliary phase, since it
i t can demonstrate
demon strate biliary
bi liary
ingestion of poorly cooked liver from infected
i nfected obstruction or filling defects.
defec ts. 
animals (spurious or false fascioliasis). This Treatment 
situation, with its potential for misdiagnosis,
can be avoided by having the patient follow a Triclabendazole is the drug of choice
liver-free diet several days before a repeat stool for treating fascioliasis because of its efficacy,
examination.  safety, and ease of use. The first report of  

 pr eseAnlcteh ouf  egghgsteinchsntoi oqlus ehs avf oe r losnhgo bweien g utshede swuictce ula btr eenadtm

h stsr f icl azeonlet  doaf tehsum
 baacnk  f taosc1i9ol8ia6s.isThe
to confirm
confirm the  the diagnosis, these methods have recommended treatment is a single 10 mg/
limitations in determining human fascioliasis kg oral dose of triclabendazole following food
 because parasite eggs are not found in feces until intake. For individuals with heavy infections,
three to four months after infection, and due the recommended treatment is two doses  
to low sensitivity in low-intensity infections. of 10 mg/kg spaced by 12 hours. Mild and
Because the release of  Fascio la coproantigens
 Fasciola transient abdominal pain, biliary colic, fever,
fever,
takes place before egg shedding, immunologic nausea, pruritus, vomiting, weakness, liver
methods are preferable to egg examination for the enlargement, and mild, limited
l imited disturbances
detection of acute infections. Immunodiagnosis in liver function have been observed as adverse
including enzyme-linked immunosorbent
immunosorbent assay events associated with the drug. Liver flukes
(ELISA) and Western blot are now widely resistant to triclabendazole have been found
applied as alternative methods of confirming in livestock, probably due to the widespread
early and extrabiliary human fascioliasis.   use of the drug. Resistant
R esistant F. hepatica
hepaticahave been
Radiological examinations may also help reported in Australia, Ireland, the Netherlands,
in the diagnosis of fascioliasis. Radiological Scotland, and recently, in Spain. No resistance
findings of fascioliasis, mainly on sonography in Fasciola infecting humans has been reported
 Fasciola
and computed tomography (CT), have been  so far. 
described in several reports. In the hepatic Bithionol may also be used to treat
 phase of the disease, parenchymal
parenchy mal lesions are fascioliasis. The fasciolicidal activity of bithionol
due to migration of the parasites through the was first described in the early 1960s. Cure
liver. The characteristic features on CT are rates ranging from 58 to 100% have been
described as multiple confluent,
confluent, hypodense
 hypodense  reported. Although bithionol is no longer  
 

CHAPTER 5: Trematode Infections   267 

commercially available for human use in many  patients are estimated torequire treatment each
countries, it is still used for the treatment of year. There
There has been an increase in the number
fascioliasis (e.g., in the United States by the of cases reported, in response to the availability
Centers the
 because for drug
Disease Control
is often moreand Prevention)
readily available of treatment.
linked Transmission
to eating to humans
raw water-grown is highly
highl y
vegetables
than triclabendazole. Adverse events including that harbor F. gigantic
giganticmetacercariae. Washing
anorexia, nausea, vomiting, and abdominal  vegetables with water, vinegar, or lemon  
 pain are mild and transient. A key drawback  juice is not sufficient
sufficient to
 to remove the encysted
of bithionol is that long treatment duration is metacercariae.
metacercariae. Use of contaminated kitchen
necessary. Bithionol is given at 30 to 50 mg/kg  tools in preparing other foods can also cause  
 body weight on alternate
alt ernate days to complete
complet e 10 the metacercariae to be transmitted.
to 15 doses. In Asia, most human cases have been
Peroxidic compounds, such as semi- reported in Iran, especially in Gilan Province,
synthetic artemisinins and synthetic trioxolanes, on the Caspian Sea. In parts of eastern Asia,
which are known for their antimalarial and human fascioliasis appears to be sporadic. Few
antischistosomalproperties,havebeenreported cases have been documented in Japan, Korean
to show trematocidal activities. Single 200    peninsula,
 peninsul a, and Thailand.
Thai land. In the
th e Philippines,
Phili ppines, no
to 400 mg/kg oral doses of artesunate and case of human fascioliasis has been documented.
documented. 
artemether completely cured chronic  F.
 F. hepatica In Europe, human fascioliasis mainly occurs
infections in rats. in France, Spain, Portugal, and the former
USSR. France is considered an important  
Epidemiology 
Fascioliasis has a worldwide distribution hu
avme b or idceadr f er ao. mAntiontealFr oef n5ch,8h6o3s  ppciatsaels
aneeenr decm
and is of great economic importance in from 1970 to 1982.
livestock-raising countries. The prevalence in Prevention and Control 
animals in Central and Latin America is about
25% but may reach 70% in cattle, goats, and Preventive measures include thorough
sheep in other countries. In the Philippines, washing or cooking of vegetables, and boiling
the dominant species affecting cattle and of water in areas where the infection is endemic.
water buffaloes is  F. giga
gigantica. Examination of
ntica Cilla et al. in 2001 reported the decrease in
cows, carabaos, and horses in South Cotabato infection over the years in Gipuzkoa, Spain
in 2007 showed a fascoliasis prevalence of which is probably related to a change in dietary
89.5%. Human fascioliasis is typically sporadic. habits. Control measures include elimination
However, clinical casesand some outbreakshave of the snail intermediate host through the
recently occurred. The estimated number of application of copper sulfate, and killing the
 people with
wit h fascioliasis
fasciol iasis is 360,000
36 0,000 in Bolivia,
Bolivi a,  parasite in the reservoir host by chemotherapy.
chemoth erapy.  
830,000 in Ecuador, 10,000 in Islamic Republic Spitfill and Dalton in 1998 demonstrated
of lran, 742,000 in Peru, and 37,000 in Yemen. that animals can be significantly protected
The total estimated number of people infected against infection by vaccination with defined
is 2.4 to 17 million, in 51 countries, from five  Fasciola antigens. These include a fatty-
continents. The number of persons at risk is acid binding protein (FABP) termed Fh12,
more than 180 million worldwide.  glutathione- S-transferase (GST), cathepsin
Fascioliasis due to F. gigantica is typical of
 F. gigantica L (CatL) proteinase, and hemoglobin (Hb).
rural areas of Vietnam, but is not infrequent in Apart from reducing fluke burden, some
areas around urban centers as well. About5,000   vaccines have elicited concurrent reductions
reductions  
 

268   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

in parasite egg production. It was also noted Haridy FM, Morsy TA, Gawish NI, Antonios
that in those vaccinated with cathepsin L2-Hb,  TN, Abdel
Ab del Gawad
Ga wad A.The
A.The potential res
reserv
ervoir
oir
>98% of the eggs recovered did not embryonate role of donkeys and horses in zoonotic

to miracidia.
hepatica A juvenile
cathepsin protease
B2 (FhCB2) known
was also as F.
recently Jfascioliasis
EgyptSocin Gharbia2002;32(2):561
Parasitol. Governorate,
Governorate, Egypt.
 – 770.
0. 
validated as a vaccine for fascioliasis using the Ishii Y, Nakamura-Uchiyama F, Nawa Y. A
rat model. The FhCB2 vaccine was shown to be    praziquantel-ineffective
 praziquant el-ineffective fascioliasis
fascioliasis case 
highly immunogenic, induced a 60% reduction successfully treated with triclabendazole.
triclabendazole.
in fluke burden, and a 63% reduction in the size Parasitol Int. 2002;51(2):205 – 9
9..
of the recovered flukes. Vaccination
accination with FhCB2
FhCB 2  Kabaalioglu A, Ceken K, Alimoglu E, Saba R,
also led to significantly reduced liver damage Cubuk M, Arslan G, et al. Hepatobiliary
H epatobiliary
(61%), suggesting a killing effect on young fascioliasis: sonographic and CT findings
 parasites before extensive
extensiv e damage occurs in the in 87 patients during the initial phase and
liver. A commercially feasible vaccine that might long-term follow-up. Am J Roentgenol.
also reduce parasite transmission and reduce the 2007;189:824 – 88..
chances of liver damage in the
t he field is a realistic Kabaa lio lu A, C ubuk M , Sen ol U,
goal. Alternative adjuvants, routes of delivery,as Cevikol C, Karaali K, Apaydin A, et al.
well as the production of a recombinant protein Fascioliasis: US, CT, and MRI findings
that mimics the protection of the native protein with new observations. Abdom Imaging.
are among the latest developments.   2000;25:400 – 44..
Keiser J, Utzinger J. Emerging foodborne  
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 Fasciola
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States and treatment with triclabendazole.
triclabendazole. G. The definitive and intermediate host
Clin Infect Dis. 2001;1(1):331 – 5.
5. of Fasci
 Fasciola
ola hepatica in natural watercress 
hepatica
 

CHAPTER 5: Trematode Infections   269 

 beds in central
cent ral France. Parasitol
P arasitol Res.
R es. Vignoles P, Dreyfuss G, Rondelaud D. Larval
2001;87(6):475 – 8.
8.   development of  Fasciola hepatica in
de Souza CP, Magalhaes KG, Passos LK, Pereira experimental infection: variation with

dosthe
of Santos GC, Ribeiro
maintenance F, Katz
of the N. Aspect
life cycle of  populations
Helminthol. of  Lymnaea truncatula
trunc
2002;76(2):179 atula
 – 83. . J
83.
 Fasciola hepatica in  Lymnaea coluntella
colu ntella in Vignoles P, Dreyfuss G, Rondelaud D. Redial
Minas Gerais, Brazil. Men Inst Oswaldo   growthandcercarialproductivityof  Fa  Fasci
sciola 
ola
Cruz. 2002;97(3):407 – 10. 10. hepatica on three species of young lymnaeid 
Tran VH, Tran TK, Nguye HC, Pham HD, snails. J Helminthol. 2002;76(3):269 – 772.
2.
Pham TH. Fascioliasis in Vietnam. Vignoles P, Menard A, Rondelaud D, Chauvin  
Southeast Asian J Tro
Tropp Med Public Health.
Heal th. A, Dreyfuss G.  Fasciola hepatica
hepatica : the
2001;32(2):48 – 50.
50. characteristics of experimental infection in
Valero MA, Ubeira FM, Khoubbane M,  Lymnaea
 Lymna ea truncatulasubjected to miracidia
truncatula
Art igas P, Muiñ o L, Mezo M, et al . differing in mammalian srcin. Parasitol
MM3-ELISA evaluation of coproantigen Res. 2001;87(11):945 – 9 9..
release and serum antibody production WHO Western Pacific Regional Office.
in sheep experimentally infected with Review on the epidemiologic profile
epidemiologic profile  of
 Fasciola
 Fasciola hepatica and Fascio
hepatica  Fasciola
lagigant ica. Vet
gigantica. helminthiases and their control in the
Parasitol. 2009;159:77 – 81.
81. Western Pacific Region 1997 – 2008.
2008. 2008. 
 

270   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Co
l norch s
i sn
i ens s
i
 

Opisthorchisfelineus Parasite Biology 

Opi 
sthorch s
ivi 
ver ini  The liver  flukes, C .  sinen si s, O. f el ineu s, and
O. viver r ini , have similar   lif e cycles (Figur es

T hese small digenetic trematodes belong to

family Opisthorchiidae, and are parasites
of the bile duct and gallbladder of humans and
 
5.8 – 5.9).
5.9). The usual mode of transmission is
via ingestion of the metacercaria of the parasite
 present in infected raw or undercooked fish.
fish-eating mammals. Infections of humans by Viable encysted metacercariae have been
Opisthorchis felineus and O. viverrini were first
reported in salted, dried, or pickled fresh
recorded in 1892 and 1911, respectively. The water fish. Metacercariae from decomposing
liver fluke Clonorchis sinensis was first reported fish could potentially be ingested by drinking
in India in 1874, during an autopsy of a 20-year contaminated water. 
old Chinese patient.

Figure 5.8. Life cycle of Clonorchissinensis

 

CHAPTER 5: Trematode Infections   271 

The metacercaria excysts in the duodenum, the feces. The miracidium hatches only after the
and the young fluke moves through the ampulla egg is ingested by the first
first intermediate
 intermediate host.
of Vater to the common bile duct, and then to The first
first snail
 snail intermediate host of C. sinensis
the distal biliary capillaries where it matures  belongs to the following genera: Parafo
 Parafossaru
ssarulus
lus
into an adult worm. The adult fluke
fluke attaches
 attaches  ( P. manchouricus , P. anomalos
manchouricus piralis , and P
anomalospiralis  P..

nduc boysaeomf  btehded binilge  idtsueclf t  biny  sutsicinkgy

itseslf uctoketr hs,e am r 
 st 
 A m s)a,  B
rl o act iunl u ( Au.l il nonu g  si B uhl ui sa)r ,aS (eT 
(cor . snt i sr i)a,  t T   sul co s
m.i g   peir r aa),
rani f 

mucus
of without causing
the epithelial permanent
lining. The ulceration
flukes may also be and O. felineus( M.
 Melanoides
hand,  and O. viverrini).require
M. tuberculatus On thesnails
other
found in the pancreatic ductand the gallbladder.  belonging to the genus Bithynia.
The worm feeds on tissue fluids, red blood cells, Upon entry into the snail host, the
and mucus.  miracidium transforms into a sporocyst, which
The egg is fully mature when it is released subsequently produces rediae. Each redia, in
from the worm. It passes with the bile to the turn, produces cercariae that are released into
intestine, and escapes into the environment with  the surrounding water. Upon contact with the 
 

272   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

second intermediate host, a fresh water fish, the

cercaria attaches
attaches itself to the host epithelium
with its suckers, and encysts as metacercaria
under a scale
There are or in afish
many muscle.   that serve as
fish species
 species
intermediate hosts of these parasites, but the
majority belongs to family Cyprinidae. A total  
of 31 species in seven families of freshwater fish,
and one species of freshwater shrimp, have been
recorded as second intermediate hosts of C. C.  
 sinensis. Metacercariae of Opisthorchis spp. have
 been recorded in 23 species and 2 subspecies of
Cyprinidae family,
family, and 11 species of Cobitidae
family.  Plate 5.19. Opistorchi sviverrini adult (Courtesy
of the Department of Parasitology, UP-CPH)
The metacercaria is the infective stage to
the definitive host. One study in northeast
Thailand showed that seasonal variations in Eggs of these parasites are yellowish brown,
metacercariae was a common phenomenon in
metacercariae ovoid, and measure 26 to 30 µm by 15 to 17  
areas with both high and low endemic infection. µm. There is a distinctly convex operculum that
The metacercarial load in fishfish was
 was shown to fits  into the thickened rim of the eggshell, and 
 be positively
positi vely associated
associ ated with
wit h infection
infecti on levels  
idaellt p
aInsm  biesr anwc ella-tdethveloa  p
 hper oetgug b  bpeo p r ciur alacr ideiunm
d em d.
.  s  ar e  also  f ound  in  the  bile
amonAgduhlutmwaonr sm that has asymmetrical features. Eggs of the
ducts of cats, dogs, pigs, and six other
oth er species three species of liver flukes are difficult to
of mammals, which can act as reservoir hosts. differentiate. 
Adults of the three parasites are leaf-like in
Pathogenesis and Clinical Manifestations  
shape, with transparent tegument. The C.
 sinensis adult is 10 to 25 mm long and 3 to 5 In clonorchiasis, metacercariae reaching the
mm wide, while Opisthorchis adults are slightly  biliary system mature and provoke pathological
patholo gical
shorter, being 8 to 12 mm long and 1.5 to 3 mm changes as a result of local trauma and irritation.
wide. The main similarity between C. sinensis Although the morphologic features vary with
and Opisthorchis spp. is the location of the duration and severity of the infection, they
vitellaria, which are found in the middle
mid dle third are sufficiently distinctive and characteristic to
of the body at the level of the uterus; whereas allow classification into phases. These phases are
the main differences are in the morphology
m orphology as follows: (a) desquamation of epithelial cells;  
and arrangement of their testes. C. sinensis (b) hyperplasia and desquamation of epithelial
adults have two large, highly branched testes cells; (c) hyperplasia, desquamation
desquamation of epithelial 
arranged in tandem in the posterior half of the cells, and adenomatous tissue formation; and  
 body. Opisthorchis adults, however, have lobate (d) marked proliferation of the periductal
testes, which are arranged obliquely. The O.
O.   connective tissue with scattered abortive acini
viverrini adult can be differentiated from theO. of epithelial cells, and fibrosis of the wall of the
 felineus adult on the basis of testes morphology.
 felineus  biliary duct. 
The testes of O. viverrini, which are positioned In general, light infections with C. sinensis 
close to each other, are more deeply lobulated (<100 flukes) are asymptomatic, or have  ffew
ew  
(Plate 5.19). 
 

CHAPTER 5: Trematode Infections   273 

non-specific clinical signs, such as diarrhea and upper quadrant abdominal pain, nausea, and
abdominal pain. Infections with a moderate emesis have been reported. Chronic symptoms
 parasite load (101-1,000
(101-1,000 flukes) may cause fever, include biliary tract obstruction, inflammation,
diarrhea, loss
 blindness, swollofenappetite,
swollen abdomenrash,
abdomen, , and edema,
enlargemnight
enlargement
ent of and fibrosis, aand
 pancreatitis, s well as liver abscess
suppurative formation,
cholangitis.  
the liver. Patients with a very high worm burden  A. Correlation of Opisthorchiasis and
(up to 25,000 flukes)
flukes) may
 may also present with   Clonorchiasis with Cholangiocarcinoma 
Cholangiocarcinoma  
acute pain in the right upper quadrant. Often,
the acute symptoms subside after a few weeks, Opisthorchis and Clonorchis parasiti
 parasitize
ze the
and are followed by chronic complications. In   bile ducts of millions of individuals
individ uals in the Far
the chronic stages, liver malfunction can occur.
occur. East. The most important aspect of infection
Calculi, acute suppurative
s uppurative cholangitis, recurrent with these flukes is their role in carcinogenesis.
 pyogenic cholangi
c holangitis,
tis, cholecystitis
chole cystitis,, hepatitis,
hepatiti s,  Numerouss studies have shown that these flukes
 Numerou
and pancreatitis are among the more severe late are closely associated with the development
complications.  of cholangiocarcinoma. The link between C.
Anincreasedriskofdevelopi
Anincreasedr iskofdeveloping
ng hepatocel
hepatocellular
lular is and cholangiocarcinoma is supported
 sinensis
 sinens
carcinoma and cholangiocarcinoma are among  by epidemiological data. In 1956, it was
the most significant
significant sequelae.
 sequelae. C. sinensis has estimated that 15% of primary liver cancers
 been classified
classified by
 by the International Agency in Hong Kong were cholangiocarcinomas
for Research on Cancer (IARC) as a probable associated with C. sinensis. A study of 2,635
carcinogen (group 2A).  necropsy cases in Thailand showed that 

la.r llyyvivther or sieniof  alr ieghotf ten
ctiaotnics,  pwaitr hticuO
Intf oem
asym p 7w8it% ocf f eacr rct  iono.mIans cwer etr aeinasasr oecaisated
h  loivf ecrr  hf olulaknegin
intensity. Flatulence, fatigue, dyspepsia, right of Korea with an extremely high prevalence
upper quadrant abdominal pain, anorexia, and of Clonorchis , fluke infection increased the
mild hepatomegaly occur in approximately 5 relative risk of cholangiocarcinoma six-fold.
to 10% of infections. Severe infections, which Experimental studies in animals have confirmed
are rare, might cause obstructive jaundice, the carcinogenic potential of these parasites.  
cirrhosis, cholangitis, acalculous cholecystitis, Studies carried out in the northeastern
or bile peritonitis.  part of Thailand found a positive correlation
Cholangiocarcinoma is the most serious  between the endemicity of opisthorchiasis
complication of infection with O. viverrini . and the frequency of cholangiocarcinoma.  
Studies carried out in the northeastern part
p art The highest incidence of cholangiocarcinoma
cholangiocarcinoma
of Thailand found a positive correlation has been reported for areas where O. viverrini
 between the endemicity of opisthorchiasis is highly endemic. Sakol Nakhon (upper
and the frequency of cholangiocarcinoma.    Northeast Thailand) has the highest
hig hest national  
Although the pathophysiology is not entirely mortality rate of liver and bile duct cancer, at  
understood, many factors are likely involved 61.4 attributed deaths per 100,000 people. A  
in carcinogenesis, including mechanical and similar association between opisthorchiasis and
 bile duct cancer has been observed in Lao PDR,
chemical irritation of the tissue by the flukes,  
and host immune responses.   where the prevalence of O. viverrini is high. 
In contrast to infections with C. sinensis 
sinensis  The pathogenesis of Clonorchis and
and O. viverrini, many patients infected with   Opisthorchis -associate
-associatedd cholangiocarcinoma
O. felineus suffer from fever and hepatitis-like   involves several mechanisms. Chronic irritation
symptoms in the acute stage of infection. Right   and inflammation caused by the fluke can result  
 

274   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

in hyperplasia and adenomatous changes of and coproovoscopy are concurrently used to

the biliary epithelium. Hyperplastic cells are define the spread of clonorchiasis in certain
define the
vulnerable to carcinogens that can easily induce regions in Russia. It shows the efficiency
efficiency  of

DNA damage
Liver during active
fluke infection
fluke  infection resultscell pr oliferation.
proliferation.
in endogenous EIA in seroepidemiological
 possibility of it surveys
itss use in endemic andThe
areas. the
formation of N-nitroso compounds in the area assay is recommended for wide application in
around the bile ducts, which in turn may lead  clinical and epidemiological practice in the foci 
to neoplastic transformation. Furthermore, of the disease. 
macrophages and other inflammatory cells, A polymerase chain reaction (PCR) method  
activated by parasite-specific T-cells, synthesize
synthesiz e  developed with 100% sensitivity has been
nitric oxide, which is a potential carcinogen. It used for detecting a single O. viverrini egg
is likely that several of the above mechanisms are in artificially inoculated feces. The method is
involved in the carcinogenesis process.  useful for specific identification of O. viverrini
Mucin-producing activity is also a frequent eggs in stool samples without the risk of false
feature reflecting the neoplastic transformation  positiv es. A single,
 positives. singl e, one-step
one-s tep multiplex
mult iplex PCR,
PC R,
of goblet cells in the bile duct lining. Application targeting mitochondrial DNA, permits the
of various carcinogens to liver fluke -infected detection and discrimination of Clonorchis
animals has been shown to increase the  sinensis and Opisthorchis viverrini in different
incidence of cholangiocarcinoma.   life-stage forms, from fish intermediate hosts,
and from infected patients. This multiplex
Diagnosis 
PCR technique produced no cross reaction  

egg  iD e osstiosoils.  bC yl ondoer tcehciti,onO poif t thhoer c phiar , aasnitde
n iathgn  s  s  s
 bmeettwaecenr caC r i.aeinoef noithaenr  dtr O
 s  s  s
em.  avtiovder er sincio, mor m  w
onitlhy
heterophyid eggs are difficult to differentiate found in fish,
fish, or
 or eggs from mixed infections
under an ordinary light microscope. Eggs, in humans. 
when stained with potassium permanganate Treatment 
and examined under 400x magnification, show
distinct melon-like ridges on the surface of O. Praziquantel is given at 25 mg/kg, three
viverrini eggs, while there is a light striae pattern times a day for 2 days. It may also be given at
on Haplorchistaichui(heterophyid) eggs. 60 mg/kg in three doses for 1 day. The latter
Cholangiography is a very useful diagnostic regimen has been found to have a 96% cure rate
tool. Several radiological features of biliary and 99% egg reduction rate. 
clonorchiasis have been described, including The therapeutic effect of albendazole is
saccular dilations of the intrahepatic bile comparable to praziquantel. It has the advantage
ducts, and rapid ductal tapering toward the of clearing various intestinal helminthiasis
 periphery (referred to as the “arrowhead sign”).
sign”). simultaneously, with very low toxicity, excellent
Less dramatic ductal wall irregularities may tolerance, and relatively
relati vely low cost. However, the
also be seen, such as indentations, a scalloped seven-day treatment course is longer than the
appearance,
appearance, and, occasionally, linear or elliptical course for praziquantel.  
filling defects representing free-floating worms.  A study has shown that in cases of light to
ELISA with crude extracts of adult C. moderate infection, a praziquantel-albendazole
praziquantel-albendazole
 sinensis has been reported to have a high combination is more effective than praziquantel
degree of sensitivity and a moderate degree alone. The combination was also found to be
of specificity for the serodiagnosis of highly effective for treating cases of co-infection
co-infection
clonorchiasis. Enzyme immunoassay (EIA)   with Ascaris , Trichuris, and hookworm. 
 

CHAPTER 5: Trematode Infections   275 

Agents and biologically active fractions Korea, Japan, Vietnam, and India; and O.
derived from medicinal plants grown in viverrini in Thailand, Laos, Malaysia, and
Siberia have been tested in vitro and in vivo. in immigrants to North America. A case of

The extract
highest from
activity the aspen
against bark displayed
Opisthorchis the
. The results aAustralia
Chinesehas
immigrant with clonorchiasis
been reported. in  
The patient was
of chemical and chromatographic studies have said to have harbored the parasite for 26
indicated that active fractions contain salicin  years without developing neoplasia. A case  
and its derivatives. The aspen bark produces of opisthorchiasis has been reported from the
no substantial toxic effect in laboratory animals Davao Medical Center in the Philippines.  
and belongs to the class “low toxic substances.”   The parasite was recovered during a surgical
The artemisinins and synthetic peroxides operation of the bile ducts.  
(i.e., OZ78) also possesstrematocidal properties O. viverriniinfections remain a major public
against schistosomes, C. sinensis, and Fasci
 Fasciola
ola health problem in Northeast Thailand, where
hepatica in vivo. Tribendimidine also shows approximately one-third of the population 
activity against the intestinal trematode is infected. The northeast region is largely
cap roni , C. sinensis , and O.
 Echinostoma caproni  populated by Thais and people of Laotian
viverrini . A single 150 mg/kg of body weight descent who eat raw fish,
fish, which
 which harbor the
oral dose ofeither artemether, artesunate, infective stage of thefluke.
the fluke. 
or tribendimidine resulted in worm burden The distribution of liver fluke disease
reductions of 99 to 100% in rats harboring is related, in part, to the distribution of
adult C. sinensis. OZ78, at a single 300 mg/kg   intermediate hosts and animal reservoir hosts.  
o9r 8a.l5d%osaeg, aicnhsitevaeddulat wC o. r m
 s in b
enuir dien ra
 s  s
etdsu. ction of   f Tisr had
, iatniodnailncdoisncsr uim p
intaitoen doef f iematir o pn ehr lay bcitosoked
c p
among rural inhabitants are significant factors
Epidemiology 
that determine the high prevalence of liver fluke
Transmission of clonorchiasis and infection in an area. 
opisthorchiasis is by consumption of raw,
Prevention and Control 
undercooked,
undercooked, salted, dried, or pickled freshwater
fish that harbor encysted metacercariae.  The main strategies for liver fluke control
Reservoir hosts are fish-eating mammals such consist of three interrelated approaches,
approaches, namely:  
as dogs, cats, and rats.   (a) stool examination and treatment of positive
Current global estimates for C. sinensis cases with praziquantel in order to eliminate
infection is 35 million, with 601 million people human host reservoir, (b) health education for
at-risk of acquiring the infection. The estimated the promotion of cooked fish consumption
number of persons infected with O. viverrini is in order to prevent infection, and (c) proper
9 million, with 68 million people at-risk, while human waste disposal in order to interrupt
about 1.2 million are estimated to be infected transmission.  
with O. felineus, and 12.5 million at-risk. An alternative approach to control  
O. viverrini and C. sinensis chronically transmission is by making the fish iintermediate
ntermediate
infect over 30 million people in Southeast host safe for consumption. A study suggested
Asia, resulting in significant  morbidity and
significant morbidity that irradiating fish at a dose of 0.15 kGy
 predisposition
 predispo sition to cholangiocarcinoma.
cholangiocarci noma. C. could control the infectivity of C. sinensis
 sinensis is endemic in China, Korea, Japan, metacercariae. Freezing or storing infected
and Vietnam; O. felineus has been reported in freshwater fish in heavy salt may not be effective
Europe, Turkey, the former USSR countries,  in the prevention of clonorchiasis. Acetic acid  
 

276   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

(3-6%) pretreatment for four hours

hour s increases Khandelwal N, Shaw J, Jain MK. Biliary parasites:
the salt penetration rate into the muscles
mus cles of diagnostic and therapeutic strategies. Curr
fish, which accelerates the death of O. felineus Treat Options Gastroenterol. 2008;11:85 –  
metacercariae.  
In the Philippines, only two cases of 95.
Kuznetsova VG. Pathogenesis of chronic and
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imported, had been diagnosed at the College   (Mosk). 2001;21 – 3 3.. 
of Public Health, University of the Philippines Le TH, De NV, Blair D, Sithithaworn P,
Manila.  McManus DP. Clonorchis sinensis and
Opisthorchis viverrini: Development of a
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against Clonorchis sinensis: a comparative (Mosk). 1997(1):9 – 12.
12.
in vivo study. Acta Trop. 2006;106:54 – 9.
9. 
 

278   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

CHAPTER 6  

 Arthropods and Mollusks

of Medical Importance 
Importance 

Introduction to Arthropods of Medical Importance  

Lillian A. de las Llagas

O  f all the major divisions or phyla

which make up the animal kingdom,  
Phylum Arthropoda is certainly one of the
There are two types of metamorphoses:  
•  Gradual or incomplete
inc omplete metamorphos  .s
metamorphosii s
In this type of metamorphosis, an
most important. Eighty-five percent of all
arthropod undergoes three stages:
known animals are arthropods. These are
egg, nymph, and adult. The young
 bilateral ly symmetrical
 bilaterally symmet rical invertebra
i nvertebrate
te animals
resembles the adult except for the
with segmented bodies, jointed appendages,
smaller size and sexual immaturity.
and hard outer coverings or exoskeletons. No
Examples of arthropods exhibiting
other animal group demonstrates such a great
diversity in structure, life cycle, and habits. The  this include cockroaches, grasshoppers, grasshoppers, 
arthropods range in size from the Atlas moth •
licoem,  panl edt e bmuegt sa. mor  pho i .  In  this  ty pe
  C   s  s
with a wingspread of 12 inches, to the small 
of metamorphosis, an arthropod
follicle mite, less than l/250 of an inch long.  
Some arthropods are parasitic, while most undergoes
undergoes four stages: egg, larva, pupa,
pupa,
and adult. There is a great difference
d ifference
are non-parasitic. Some prefer to live in highly
 between the immature stages and
organized and complex environments in which
the adults. Examples of these are
each member contributes something to others
mosquitoes, flies, butterflies, moths,
in a symbiotic relationship.  
ants, bees, wasps, fleas,
fleas,  and beetles.  
Many arthropods have complicated life
histories. In some, the entire life cycle is not Arthropods are found everywhere, whether
completely known. Some demonstrate little it is in mountains, swamps, deserts,
deserts , cities, or
change in morphology throughout the different countryside. Their presence in any environment
life stages, while others pass through a complete reflects  their capability to adapt, propagate, and
metamorphosis having egg, larval, pupal, and   establish colonies. 
adultMsteatgaems.orph
phoosisrefers
refe rs to the change
chan geiinnfform
orm Ar th r o po ds ar e  pr ovi de d wi h s p ec ia l
mechanisms which they use against their 
or
thestructure
period ofofdevelopment.
an arthropod that occurs during enemies: the chitinized exoskeleton, primarily
A few primitive a nitrogenous polysaccharide which makes the
insects develop without metamorphosis. In integument impervious to water; appendages
these insects, the young is the exact replica of which may be lost and later regenerated; hairs,
the adult differing only in size.  scales or spines; and body fluids which may be
used effectively for their survival.  

278 
 

CHAPTER 6: Arthropods and Mollusks of Medical Importance  279 

Classification of Arthropods 

Phylum Arthropoda comprises at least

740,000 species. The majority of medically
important arthropods can be grouped into two
classes: Insecta and Arachnida. Other classes,
which are also important, are Chilopoda, 
D ia blole po6d.1a),. Cr ustacea,  and  Pentastomida 
(T p

Table 6.1. List of immediate diagnostic features

of arthropods  

Figure 6.1. A generalized diagram of an adult

Class Legs
Cyclorraphan fly (From Baltazar CR, Salazar NP.
Philippine insects: an introduction. Quezon City:
University of the Philippines Press; 1979.)  

 A. Head  

The head bears the eyes, antennae, and the

mouthparts. The antennae are located in the

front portion
por tion of the
t he head between
between the eyes. They  
are greatly modified,  often having characteristic
shapes, and are provided with chemoreceptors 
(Figure 6.2).

Class Insecta (flies, mosquitoes, bees,

wasps, butterflies,
 butterfl ies,  bugs, etc.) is considered the
largest, representing approximately 70% of the
 phylum. It also typifies the arthropod’s external
and internal structures. Class Insecta is the
most important group of arthropods from the 
medical viewpoint. It includes many species that
directly and indirectly affect humans.  
External Anatomy  Figure 6.2. Parts of an insect head  
(From Baltazar CR, Salazar N P. Philippine insects:
an introduction. Quezon City: University of the
The body of an insect is divided into Philippines Press; 1979.)
three major regions: the head, thorax, and
abdomen (Figure 6.1). In many insects, these Two types of eyes occur in insects: simple
 parts are clearly well-differentiated,
well-differentiat ed, as in flies and compound. Simple eyes or ocelli consist of
and mosquitoes, whereas in some, they are less single eye units or facets. Compound eyes are
distinct as in fleas.  usually very large and maybe round, oval, or  
 

280   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

kidney-shaped. The outer face of thet he compound soluble foods. The mandibles are absent, and
eye is composed of many small six-sided lenses the maxillae are represented only by the
t he palps.
called facets. In general, the active flying insects The labrum and labium
l abium fuseto form a proboscis
pro boscis
have large eyes with many facets, while the with a spongy
sp ongysaliva
tip
ti p called the
th e labellu
labellum.
walking types have fewer facets. Some parasitic regurgitates to dissolve them.food.
The Then,
insect
insects have poorly developed eyes, as in some the capillary grooves at the base of the labellum
fleas.  carry the liquefied food to the food canal inside 
Insects have an upper lip or labrum, a lower the proboscis (Figure 6.4).
lip or labium, a pair of maxillae or upper jaw,
and a pair of mandibles or lower jaw.The shapes  
and sizes of these structures vary according
to the insects’
insects’ feeding
 feeding habits. There are four
 principal types of mouthparts:  
1. Chewi 
ngmouthparts
 
These are exemplified by cockroaches and
silverfish, which use their mouthparts to grind
solid food. The mandibles are useful in cutting
or tearing food apart. The maxillae, labrum, and
labium are used in handling food before it is

swallowed. The palpi are used to feel, smell, and  Figure 6.4. Sponging type of mouthparts  
thasitr es f w r i pouens dseangseessaar er  p
oohder .eTtheseva p e cr onvicdeendtr watiethd
(From Baltazar CR, Salazar NP. Philippine insects:
an introduction. Quezon City: University of the
Philippines Press; 1979.)
(Figure 6.3). 
3. Pe
i rc ing-suckn
 i gmouthparts
 
These are exemplified by mosquitoes,
 biting flies, sucking
sucking lice, fleas, an
andd kissing bbugs.
ugs.
The mandibles, labrum, and maxillae are long
and slender. The labium forms a stout sheath,
which holds these structures, and the entire
structure is called the proboscis (Figure
( Figure 6.5).  

Figure 6.3. Chewing type of mouthparts

(From Baltazar CR, Salazar NP.
NP. Philippine insects:
an introduction. Quezon City: University of the 
Philippines Press; 1979.)

2. Spongi 
ngmouthparts Figure 6.5. Piercing-sucking type of mouthparts
 
(From Baltazar CR, Salazar NP. Philippine insects:
This type, as exemplified by houseflies, an introduction. Quezon City: University of the
is adapted for sucking up liquid or readily   Philippines Press; 1979.)
 

CHAPTER 6: Arthropods and Mollusks of Medical Importance  281 

4. Chewn
i g- a
l pp n
i gmouth
 parts Wing veins running from the base to the
th e
 
An example of an insect having this type
apex of the wings are called longitudinal veins.
Cross veins connect the longitudinal veins. The
of mouthparts is the honeybee. Mandibles and
maxillae are of the chewing type and are used arrangement and number of these veins are
important in the classification of insects. Areas
for grasping prey or for molding wax or nest
in between veins are called cells. Some veins
material (Figure 6.6). 
may be closed. Each vein contains a nerve cord, 
trachea, and hemolymph. The leading edge is
called the costa, and short subcostal veins are
numbered 1, 2, 3 and so on. 
2. Leg  
 
The leg is divided into the coxa, trochanter,
femur, tibia, tarsus, and pretarsus (Figure 6.7).
The femur and tibia correspond to the human
thigh and shin, and the tarsus has
h as a function
similar to that of the foot. The last tarsal
segment usually terminates into a pair of claws
or pulvilli, which help the insects in walking on
smooth surfaces. 

Figure 6.6. Chewing-lapping type of mouthparts

(From Baltazar CR, S alazar NP
NP.. Philippine insects:
an introduction. Quezon City: University of the
Philippines Press; 1979.)
1979.) 

B. Thorax  

This is the second main body region which

is connected to the head by a membranous
region, called the neck or cervix. This part bears
three segments, namely: prothorax, mesothorax,
and metathorax. Each segment bears a pair of
walking legs. Wings, when present, are attached
to the mesothorax and metathorax.  
1. Wi 
ngs
 

 bodyThese
wall are
andmembranous
and consist of an extensions of the
upper and lower
Figure 6.7. Walking leg of an insect  
layer. These layers are supported by reinforcing (From Baltazar CR, Salazar NP. Philippine insects:
structures, which appear as distinct lines called an introduction. Quezon City: University of the
veins.  Philippines Press; 1979.)
 

282   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

C.  Abdomen
 Abdomen   Internal Anatomy 

The third body region, which bears the  A. Circulatory System 
System 
spiracles and the external reproductive organs,
is made up of 11 segments. The spiracles(Figure Insect blood
hemolymph. is usuallyhemocytes,
It contains colorless and is called
which are
6.8) are the external openings of the respiratory  blood cells
cel ls that are mainly phagocytic.
pha gocytic. Blood
B lood
system, and some insects have a pair on each  
circulation is maintained by the hemolymph  
alesnext. oTr ghaen8stuhsaenddf o9r thco p
 ba beadr otmheineaxltser gnm segum
lateinotns which flows through small valve -like openings
in the male and serve as an egg-laying device or called ostia (Figure 6.10). The heart is located
dorsally and blood from the heart is forced  
ovipositor for the female. Some bear a pair of forward through the aorta to the brain. The
finger -like -like processes called cerci (Figure 6.9) on main function of the heart is to carry nutrients
the 11th segment which are more conspicuous to the tissues, and waste products to the
in females. 
Malphigian tubules for excretion (excretory
organ). The entire body cavity is called the
hemocoel. 

Figure 6.8. Spiracle

(Courtesy of Dr. Lilian de las Llagas)  

Figure 6.10. Diagram of an insect showing the

arrangement of the circulatory system  
(From Baltazar CR, Salazar N P. Philippine insects:
an introduction. Quezon City: University of the
Philippines Press; 1979.)

B. Respiratory System  

Oxygen reaches the tissues by direct gaseous

exchange. The spiracles, which are circular
openings in the cuticle, allow air to enter the
 body (Figure 6.11). Spiracles are located on
the mesothorax, the metathorax, and the first
Figure 6.9. Cercus
eight abdominal segments. Air passes through
(From Baltazar CR, Salazar NP. Philippine insects: a small tube called the trachea. Oxygen diffuses
an introduction. Quezon City: University of the across the tracheoles into the cells, while carbon
Philippines Press; 1979.) dioxide from the cells enters the tracheoles and  
 

CHAPTER 6: Arthropods and Mollusks of Medical Importance  283 

the body, especially sensory organs like the

compound eyes, ocelli, antennae, halteres, palpi,
and hairs, serving as sensory receptors.  
D. Digestive
Digestive System  

The foregut starts with the mouth

mo uth
and includes the pharynx, esophagus, and
 proventriculus
 provent riculus (Figure
(Figu re 6.13). The posterior  
 part of the esophagus, called the crop, serves 
as an area for temporary storage of food
 before it is passed to the midgut for digestion.
The muscular proventriculus acts as a valve
 preventing the food from being regurgitated
and may have teeth or spines to aid in the
disintegration of food particles. A pair of
Figure 6.11. Diagram showing an insect spiracle
and trachea (From Baltazar CR, Salazar NP.
salivary glands is situated in the thorax. The
Philippine insects: an introduction. Quezon Ci ty: composition of saliva varies according to the
University of the Philippines Press; 1979.) type of insect. In blood-sucking ones, it often
contains anticoagulins, which may be allergenic. 
goes out via spiracles. This tracheal system also The midgut or stomach serves as an area

regulates water.   for food storage in the process of digestion  

C. Nervous System   aenzdymaeys   bneceosm
saer ygr f eoar tliynsdeicst em
ndeeadl  .dIitgessetcir oente. s
The central nervous system consists of a The beginning of the hindgut is marked by the
 brain connected
connect ed to a nerve cord, with ganglia
gangl ia  presence of opaque tubules called Malphigian
occurring at intervals, often one ganglion per tubules. The anterior part is called the ileum,
 body segment (Figure 6.12). Nerves arising while the more distal part is called the rectum,
from these ganglia reach various parts of   which terminates in the anus. 
E. Excretory System  

Malphigian tubules act as excretory filters

and discharge waste products (Figure 6.13). 

Figure 6.12. Diagram of an insect showing

the arrangement of the nerve cord   Figure 6.13. The digestive and excretory systems
(From Baltazar CR, Salazar NP . Philippine insects: (From Baltazar CR, Salazar NP. Philippine insects:
an introduction. Quezon City: University of the an introduction. Quezon City: University of the
Philippines Press; 1979.) Philippines Press; 1979.)
 

284   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

They are milky white to opaque in appearance Because of the chitinized cuticle, the
due to deposition of waste products within insect’s skin is not sensitive to contact. The
insect’s skin
their cells.  sense of touch is made possible by b y sensory
F. Reproductive System   hairs
whichconnected to a nerve
is stimulated (sensory
if hairs nerve cell),
are disturbed.  
Insects are dioecious; the male and female  Nerve endings
endi ngs are usually
usu ally concentrated
con centrated in the
must mate before eggs are produced. Insects  mouthparts, antennae, and tarsi.
which lay eggs are called oviparous, while those Tastee is usually perceived by
Tast b y the mouth and
an d
which deposit larvae are called viviparous.   mouthparts, by the palpi or even by the protarsi.
The reproductive organs of the female Palps also bear olfactory organs. The sense of  
(Figure 6.14A) consist of a pair of ovaries which smell is highly developed in insects and is used
 produce eggs and pass them into the oviduct, for locating food, finding a mate, and locating
where they may be fertilized by sperm cells a suitable oviposition
o viposition site
site.. 
stored in the spermatheca. Some species have Insects generally respond only to specific
accessory glands which secrete an adhesive noises, such as the sound made by the wings of
coating for the eggs.  a female mosquito. Sound waves may be picked
The male reproductive organs (Figure up by fine sensory hairs or by an auditory drum
6.14B) consist of a pair of testes in which sperm located on the lower part of the insects’
insects’ front
 front
cells are developed. The seminal vesicle serves legs. Only some insects, like grasshoppers,
as storage for spermatozoa until mating occurs. cicadas, crickets,
crickets, and other species of moths
The accessory glands secrete a liquid su substance
bstance  have “ears” or tympanic membrane. Flies and  
 pder 
as assveedhinclteo f tohr ethveass p
taor esethr veen  p m ells,
f er ens anw
c   d hinictho m os-qliukiet oer sganr eo bnetlhi evsedcotnodhaenar te bnynaml seeagnm
cu p s  eonf  ta,
the penis or ejaculatory organ.   which responds to sound waves picked up by
the rest of the ante
antennae.
nnae. 
The principal organs of sight are the
compound eyes and ocelli. Insects cannot move
nor focus their eyes. It is not possible for insects
i nsects
to see a sharp clear image, and they are only able
to see blurred images. These eyes are provided
with nerves, which transmit stimuli to the brain. 
Because of these different senses, insects
are able to react to their environment. Their
responses arise from simple stimuli, such as
Figure 6.14. Reproductive systems of an insect
(From Baltazar CR, Salazar NP. Philippine insects:
light, heat, gravity, hunger, and smell. Their
an introduction. Quezon City: University of the reactions consist of more or less fixed behavioral 
Philippines Press; 1979.)   patterns and they react similarly to the same
stimulus. This is called automatic behavior,
G. The Senses 
Senses  which does not involve reasoning. With insects,
 behavior al reactions
 behavioral reaction s are usually
usuall y immediate.  
Insects also possess the senses of touch, Although the brain is located in its head, each
taste, smell, hearing, and sight. They also of the body regions act independently, or in
 possess other auxiliary senses such as the sense a semi-autonomous manner, because pairs of
of balance, and possibly orientation.   nerve centers called ganglia are located along  
 

CHAPTER 6: Arthropods and Mollusks of Medical Importance  285 

the bottom side of the insect’s

insect’s body
 body and are D. Ca
l ssCho
l 
l i poda(cen
 p
t i edesorhundred-e
l ggedworms)
connected to the brain by a nerve cord.
Arthropods can cause direct and indirect
These arthropods are terrestrial, elongated,
and have many segments. The body is
injuries
importantto humans.
classes Below is the list
and orders underof medically
Phylum dorsoventrally flattened with a pair of legs on
Arthropoda. Discussion of their important
each body segment. The appendages of the first
first  
features and roles in human disease are given   bcl
cloadwys.segment ar e modified to ser ve as  ppoison 
in the next two sections.
E. Ca
l ssD
 p
 i o
l poda(m
 p
i 
l 
l i edesorthousand-e
l ggedworms)
 A. Ca
l ssInsecta
 
These are terrestrial, elongated and have
Order Diptera (mosquitoes and flies)
many segments. The body is cylindrical with
Order Siphonaptera (fleas) 
(fleas) 
two pairs of legs per body segment. There are
Order Hymenoptera (bees, wasps, and ants) no poison claws. They do not bite humans, but
Order Lepidoptera (moths and butterfli
 butterflies)
es)  
secrete substances that are irritants to human
Order Hemiptera (bed bugs and kissing
skin. 
 bugs) 
Order Anoplura (sucking lice) F. Cl 
assPentastom d
i a(tongueworms)
 
Order Coleoptera (beetles)  
Adults have elongated bodies which are  
B. Ca
l ssCrustacea either flattened (e.g.,  Linguatula in dogs) or  
cylindrical (e.g.,  Armillifer in pythons). In  
These arthropods are aquatic in nature.    Armillifer , the body is divided into a series of  
(  heeaidr   banod itehsoaraexdf iuvsiededtoignetothtewr )oa:cne ph
T d a baldothmoer nax.
unusually conspicuous rings, which are not true
Respiration is either by means of true gills or
segments. This characteristic raises questions
directly through the body wall.  
on whether this class should be under Phylum
Phylu m
Arthropoda. The larval stage, however, is
Therearetwoordersofmedicalimportance: i mportance:  segmented. The adults usually live in the lungs
Order Copepoda (cyclops)   or air passages of their hosts, while larvae live
Order Decapoda (macrocrustaceans,
(macrocrustaceans, e.g., free or encysted in the viscera of some other
crabs, lobsters, and shrimps)   hosts. 
C. Ca
l ssArachn ida References 
 
These arthropods are both aquatic and Baltazar CR, Salazar
Sal azar NP.
NP.Philippine
Philipp ine insects: an  
terrestrial in nature. Their bodies are divided introduction. Quezon City: University of  
into a cephalothorax and abdomen. The
cephalothorax bears six pairs of appendages:   de  latsheLP i p pLAin.esStPur deyss;g1u9id7e99..in  medical
lahgials p
entomology. 1987. Located at: College of
aonf  twer ailokr incghleelgicse. r ae,  ppedi p  lps, and f our   p
 pa p pair s Public Health Library, University of the
There
are of are three
medical orders of  arachnids
importance: which   de lasPhilippines
Llagas LA,Manila.
Abong  J. Identification and
characterization
characte rization of local
l ocal house dust mites:
Order Scorpionida (scorpions)  potential for native allergen production
product ion for  
Order Araneida (spiders)
Order Acarina (mites and ticks)  
 

286   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

experimental, diagnostic, and therapeutic Philippine Islands. San Francisco: USAF

use in the local setting. 2003. Located
L ocated Fifth Epidemiological Flight, PACAF,
at: College of Public Health Library, technical report 70-l; 1970. 
University of the Philippines Manila.  Service MW. A guide toThe
medical entomology.
Borror DJ, Delong DM, Triplehorn CA. An 1st ed. Hongkong: MacMillan Press
introduction to the study of insects. 4th ed. Ltd.; 1980. 
USA: Holt, Rinehart and Winston; 1976.  Taboada O. Manual of medical entomology.  
Cagampang-Ramos
Cagampang -Ramos A, Darsie RF Jr. Illustrated USA: US Government Printing Office;
keys to the  Anopheles mosquito of the  1968. 
 

CHAPTER 6: Arthropods and Mollusks of Medical Importance  287 

 Arthropods as Direct Causes of Injury

Lilian A. de las Llagas

Ways by which Arthropods Affect Humans   follow repeated exposure to various venomous
arthropods. Arthropods that cause direct injury
h ndir r aect ef f aectisfiof  aar th(r ao) ponds noon hui ma ar 
e
ge e lly cl ss ed s: e ve m zation;   through envenomization are described below. 
n s 
T 
(b)  ectoparasitism
ectoparasitism;; (c) ingestant and inhalant
allergens; (d) food, water, and house pests; (e)
 A. Order Hymenoptera (bees, wasps, and
ants)  
ants)

myiasis; and (f) entomophobia and delusory The name of the order comes from the
 parasitoses (Table 6.2).  Greek word hymen meaning membrane and
 pter y meaning wing. These are, therefore,
Table 6.2. Specific injuries and their causative membranous-winged arthropods. Their
agents  mouthparts have strong jaws, which are
adapted for biting. Typically, there are two
 pairs of wings, with the hind pair being smaller
than the front pair. The wings are folded back
over the abdomen when at rest. The body is
divided into three segments: head, thorax, and  
a bdomeina.lTsheegm
a bednotm enuits  f usr utahlelyr   doivnildyedsixinotor
s,   b
eight are evident. The last abdominal segment
is a modified ovipositor, the stinging stingin g apparatus
of a female hymenopteran. This modification
of the egg-laying tube enables it to function as
a very efficient
efficient weapon
 weapon for both offense and
defense. The sting is withdrawn into the body
when not in use. The presence of an ovipositor
serves to identify the female since the sting is
absent in the male.  
The stinging hymenopterans are divided
into two distinct groups: those that kill their
 prey by stinging, and those that sting only to
 paralyze their prey
prey..
Envenomization  Formic acid, which causes the paralysis,
Venoms are poisonous substances, which can be found at the base of the stinger of  
certain animals secrete and introduce by biting some hymenopterans. The apparatus of the
or stinging. Arthropod venoms are usually hymenopteran that kills has an acid gland
g land
 poisonous
 poisono us when they are injected through the opening directly into the poison sac, and an
integument, or come in contact with injured alkaline gland, which is comparatively small.
skin. The toxic effect of the injected venom It is the combination of these acid and alkaline
depends upon its chemical composition and fluids that results in the death of the prey or
fluids that
the amount injected. Allergic reactions may   causes extreme pain. 
 

288   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Stinging hymenopterans, which have 1. TheSt ii 

n gn
i gApparatus(mod ifi 
e do p
v i osti 
or)
 been found responsible for adverse reactions in  
The venom apparatus consists of three
humans, are members of superfamilies Apoidea
 parts: the
th e piercing apparatus, the
t he lateral plate
p late
(bees) (Platejackets)
and yellow 6.1), Vespoidea (wasps,
(Plate 6.2),and hornets,
Formicoidea and appendages, and the poison sac and glands.
(ants). 
If the ovipositor stinger stays in the
t he wound, one
can be sure it is from a honeybee. The stinger of  
the hinosneecyt b
, ethe eis b e hlolendeyf  br ro em
hoanrbeye bde; ewdhiens.itTihs  pu e,
therefore, is not capable of multiple stings,
unlike the hornets, wasps, and bumblebees,
which all have unbarbed stingers (Plate 6.3).  

Plate 6.1. Bee (Bombussp.)

(Courtesy of Dr. Lilian de las Llagas) 

Plate 6.3. Bee stinger

(Courtesy of Dr. Lilian de las Llagas)

Among ants, the bite may be supplemented

 by the sting. Formic acid of the formicine ants
may reach intra- or sub-dermal tissues only
through wounds made by the mandibles. Some
ants bite and sting simultaneously. The bite
b ite is
a necessary mechanical advantage for inserting
the sting. Salivary secretions are not introduced.  
2. TheNatureandActionoftheV
heVenom
Venom secretion in worker honeybees
 begins just
ju st prior to emergence
emergen ce and increases
incr eases
slowly toward a maximum amount between
the 10th and 16th
1 6th day. This amounts to 0.3
0.3
mg of liquid or 110 pg of venom. Secretions
cease after 20 days. Protein food, mostly pollen,
Plate 6.2. Wasp is required for the full production of venom.
(Courtesy of Dr. Lilian de las Llagas)  Electrophoretic and chromatographic studies  
 

CHAPTER 6: Arthropods and Mollusks of Medical Importance  289 

have shown thatbee venom contains histamine,

which is released in the tissues. Histamine,
His tamine,
however, is not the major pharmacological
component. Bee
cholinesterase
cholinesteras e orvenom appears to contain
5-hydroxytryptamine, butnoit
does contain low molecular weight ninhydrin-
reacting compounds, the action of which is not  
completely understood. 
Toxic
Tox ic effects of bee venom result from the  
combined actions of mellitin, phospholipase
pho spholipase
A, and hyaluronidase. These account for
 both the local and general reactions such as
 pain, inflammation, swelling, and redness.
Phospholipase
Phospholipase is also known to indirectly cause
hemolysis of red blood cells.  
The initial response to the venom is a wheal
and flare
flare at
 at the site of the sting, then itching Plate 6.4. Kissing bug (Triatomasp.)
and flushing follows. As the venom circulates (Courtesy of Dr. Lilian de las Llagas)  
in the blood, more widespread symptoms
occur. Vascular effects (hypotensio
(hyp otension),
n), and then  bloodsuckers. Members include the genera  

 pulmonar y effects, with asthma or angioedema

 pulmonary angioede ma   Arilus and  Reduvius.
in thTe haeir ewff aeycst,saor f esot bser 
v ed .
ings ar e two-f old: the dir ec
ect  positTior niatoof mainteesnanr ael dinif sf eer r teinotni.atIend  b
 b Ryhtohd eniu s ,
toxic effect, and the anaphylactic shock, which the insertion is at the top of the head. In
may develop in those who become sensitized Triatoma , the insertion is midway between
to it. Many beekeepers become desensitized the compound eyes and the tip of the head,
to bee venom as a result of repeated stings. while in Panst
 Panstrongylus, the insertion is near the
rongylus
The sera of beekeepers contain antibodies to compound eyes. 
 phospholipase A.  Genus Triatomahas been reported to inflict
B. Order Hemiptera 
Hemiptera 
 painful bites
b ites (Plate
(Pl ate 6.4). Triatomarubrofasciata
 bite was first
first reported
 reported in the Philippines by
by
Family Reduviidae consists of insects Africa in 1934. There have been periodic
described as “cone -nosed” because they have complaints from patients bitten by this bug.
narrow pointed, cone-shaped heads. They are Major complaints include swelling in the area of
known as “assassin” bugs or “cannibal” bugs the bite, nausea, vomiting, irritation, and pain.
which prey upon soft-bodied insects, and   The extent of reaction to these bites appears to 
“kissing” bugs because some biting species depend on the sensitivity of the host and on
attack the face.  
Subfamilyy Triatominae
Subfamil Triatominae feeds on the blood reactions
the amountareofprobably
antigen due
injected.
to theSymptomatic
p henomenon
phenomenon
of vertebrates, including humans. Members of sensitization rather than a response to a
of this subfamily include the genera Rhodn ius,
 Rhodnius  primary irritant. Bugs usually bite at night and
Triatoma, and Panstrongylus (Plate 6.4).
 Panstrongylus the lesions are usually in the exposed parts of
Subfamily Haspactorinae also inflict the body. The venom is probably the same as
 painful bites, but they are not necessarily  the venom of bees and wasps.
 

290   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 Arilus is called the wheel bug because of

a cog-like crest found on its thorax, which is
its distinct feature. The proboscis has three
long and stout joints. When not in use, the
 probosci s is bent ventrally
 proboscis ventrall y under the head. This
 bug is usually found in vegetation, near rocks,
other outside debris, and inside buildings when 
raining. This bug is known to feed on
o n other
arthropods.
The wheel bug attacks humans as a form
of defense, particularly when its resting place is
disturbed. Its bite inflicts severe and immediate
 pain. 
C. Order Lepidoptera  

The larvae of moths and butterflies

and butterflies are
 are Plate 6.6. Caterpillar head and thorax, lateral
called caterpillars (Plates 6.5 – 6.6).
6.6). They usually view (Courtesy of Dr. Lilian de las Llagas) 
have a cylindrical, worm-like body which is
divided into 12 segments: the first three make mechanical effect, similar to that of glass fibers.
up the thorax, and the other nine the abdomen. The hairs are of several kinds and many of them
The well-developed head bears a mouth, 12   are barbed, so that they tend to stick to the skin.  
tminoyutehy peas r atsnodf  thweolavr evr aye csohnosr itstaonf testnr noaneg. b
  Tithineg ct,utr hneinsgusecne psati b
expoenr iecnocneta b
U tiolen  ionditvhieduaaff lem
cteady
 jaws and mandibles adapted
adapted for biting. This skin, which may show redness or inflammation.
differs from the adults, which have sucking Other areas may show urticarial wheals. 
mouthparts. Some larval species have spines If the hairs get into clothing, widespread
or hairs, which may contain toxin. In some
som e dermatitis may occur. Wind-blown hairs in
instances, irritation seems to be largely due to a  drinking water can also cause inflammation of
the mucous membrane of the mouth.
D. Class Chilopoda 
Chilopoda 

Centipedes are terrestrial arthropods that

are dorsoventrally flattened, and have one
 pair of legs per body segment (Plate
(Plat e 6.7). The
head bears a pair of long antennae, a pair of  
mandibles, and two pairs of maxillae (Plate 6.8).  
The first body segment bears a
bears  a pair of
modified legs found just ventral and lateral to
the mouth. These modified
modified legs
 legs form claws,  
the terminal joints of which are curved, sharply
 pointed, horn-like fangs that connect to the
venom glands. 
Plate 6.5. Caterpillar, dorsal view Large species of centipedes can grow up to
(Courtesy of Dr. Lilian de las Llagas)  25 cm in length and are considered venomous. 
 

CHAPTER 6: Arthropods and Mollusks of Medical Importance  291 

 brain where
wher e marked congestion
con gestion was observed
indicating the concentration effect of the
 poison, and (b) thinness
thinnes s of the skin in the region
of theamount
large bite, which allowed
of poison andthe
itsdeep
rapidinjection of a 
absorption.
E. Order Scorpionida (scorpions) 
(scorpions) 

The body is divided into a cephalothorax

and an abdomen. The cephalothorax is
unsegmented and covered by a dorsal plate,  
called a carapace which contains 2 to
t o 12 eyes.
The abdomen is segmented with the terminal
five segments ending in a bulbous sac and a
five segments
conspicuous stinger. The sac contains two
 poison glands which are connected to the
terminal stinger by ducts. Scorpions have no
Plate 6.7. Centipede
(Courtesy of Dr. Lilian de las Llagas) 
antenna but their bodies and legs are covered
with sensory hairs (Plate 6.9). 
Scorpions are nocturnal creatures. During
the day, they remain hidden under stones, logs,
 piles of lumber,
lumber, closets, shoes, folded
folded blankets,
blankets, 
folded papers, and other debris. They come out  

Plate 6.8. Centipede head

(Courtesy of Dr. Lilian de las Llagas) 

Small types, about 2 to 5 cm long, are harmless,

since they do not have well-developed
well -developed fangs
for biting. The amount of venom introduced
depends on the size of the centipede. 
The bite is characterized by local pain at
the site of puncture, hardening of the skin,  
formation of papules, rash, swelling, and
 purple patches. However, each sign or symptom
sympto m 
subsides within 24 hours if the wound remains
uninfected.
Pineda, in 1934, reported a death due
to a centipede bite in the Philippines. The
immediate reactions noted after the bite were
 pain, numbness of the affected area, and a
minute, reddish puncture wound. Noteworthy Plate 6.9. Scorpion
were the following: (a) proximity of bite to the  (Courtesy of Dr. Lilian de las Llagas)
 

292   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

of their hiding places at night to obtain food, and  Loxos celes (brown widow/recluse spider).
 Loxosceles
consisting mainly of insects and other arachnids.   The females of both spiders destroy or kill the
Although scorpions rarely sting humans, males after
aft er mating.
mating . Thus, they are call
called
ed“widow
they are considered dangerous since they spiders.” 
 produce hemolytic and neurotoxic venom.
1. Latrodecu
t s
Investigators have described the venom to be
 protein in
i n nature, and
an d its toxicity
tox icity is
i s dependent   The mature female black widow spider is 
on sulfhydryl groups. Hemolytic venom causes deep black in color. It has red markings in the
 painful swelling
swell ing at the site of the sting, which
whi ch form of an hourglass on the underside of its
diminishes within 30 minutes. Neurotoxic  abdomen. It is approximately 1.2 to 5.1 cm in  
venom may produce numbness at the sting size (Plate 6.10).  
site, profuse sweating, salivation, nausea, and
 paresthesia of the tongue. Drowsiness may
follow the immediate sharp pain. It has been
observed that if the victim is alive for three hours
after the sting, survival is probable. No other
oth er
arthropod produces these symptoms.  
 A. Order Araneida (spiders) 
(spiders)  

The body is divided into a cephalothorax

and an abdomen joined by a slender “waist,” “waist,”  
commonly has eight sim ple eyes andostihxo pr axir s
a lled  a  pedicel o r  st alk . T h ce phal
ofappendages.The first pair of appendages, the 
chelicerae or fangs, are claw-like and utilized by   Plate 6.10. Black widow spider (Latrodectushassett 
)i 
 l 
the spider to capture its prey. The second pair (Courtesy of Dr. Lilian de las Llagas)
of appendages is a pair of six segmented palpi 
or pedipalps, which are found in front of the   A bite from the black
black widow spider is often
legs and are sometimes mistaken for legs. The   inconspicuous. Slight local swelling and two
other four pairs of appendages are walking legs.  tiny red spots may appear, with local redness
The chelicerae are segmented appendages usually evident at the point of attack. Within
and have hollowed tips, through which the a few minutes after the bite, latrodectism
venom is injected from the modified  salivary develops, characterized
characterized by severe pain which
or poison glands.  spreads throughout the extremities and the
The spinning organs are located near the trunk. Within a few hours, chills, vomiting,
 back of the abdomen and on the underside.   cramps, delirium, and spasms may occur.  
There are usually six spinnerets used for Abdominal pains are frequently severe. These
spinning the web.  symptoms may be mistaken for appendicitis,
Spiders are cosmopolitan in distribution colic, or food poisoning. In 1987, Grace and 
and nocturnal in habit. They prefer quiet, cool DaÔgo reported a case of spider bite by a spider
shelters and dimly
d imly lit areas.   popular ly known as “gagambang gubat.” The
 popularly
Most spiders are harmless. Few have  patient exhibited
exhibite d contraction
cont raction of leg muscles,
m uscles,
chelicerae that are strong enough to penetrate
chelicerae high fever, hemoglobinuria, and jaundice. 
human skin. Among the dangerous species are The venom apparatus consists of two
ectus (black widow spider or “katipo”)
 Latrodectus
 Latrod “katipo”)   glands, located on the cephalothorax, which are 
 

CHAPTER 6: Arthropods and Mollusks of Medical Importance  293 

connected by ducts to two curved fangs, located a. Family Culicidae (Mosquitoes)

on the distal segments of the chelicerae. The
venom is a complex protein with a neurotoxic Among the mosquitoes, only females bite,
 but both sexes feed on nectar and juices. The
lipoprotein fraction. sexes can be easily differentiated by looking at
2. Loxosce les the antennae. The male has a hairy or plumose
antenna, while the female has pinnose antennae 
This species may be distinguished from 
other forms by its three pairs of eyes arranged withM lesosqhuair to. es have scaly wings, the thir d vein
in a semi-circle fashion on the forepart of of which is simple, while the second and fourth
the head, and a dark violin-shaped marking  
veins are branched. The mouthparts belong to
immediately behind the simple eyes. This is
the piercing-sucking type. Mosquitoes are about
more commonly found inside houses than the 4 to 6 mm in length. Some small-sized
small- sized species
 black widow spider. 
measure about 2 to 3 mm in length, while the
Loxoscelism is caused by this spider’s  bite. larger-sized species can be as long as 10 mm.
Although symptoms are localized, it differs from Mosquitoes have two compound eyes that are
the bite of the black widow in that the initial
thick wheal may become necrotic. In 1987,
made up of many facets. Just below the antennae
is a pair of palps, dilated or pointed at the tips,
Barrion reported two cases of loxoscelism. Two depending on the species. 
 boys were bitten on their hands by a spider
The thorax is slightly humped and is
while climbing a mango tree. The immediate covered dorsally and laterally with scales. The
reactions were localized swellings at the bite   abdomen is composed of 10 segments but 
sLiatetes,r,hnigehcr f oesviesr a, nan gr ter ancetiwoner seof  blesegr m
ddgacnon veudscolnes. only the first 8 are visible. The last abdominal
the bitten areas. The venom of Loxosceles may segment of female mosquitoes terminates in
contain a spreading factor and this may be a small pair of cerci, whereas, in the males, a
 prominent pair of clas
claspers
pers is present. 
responsible for the necrotic effect.  
Two major divisions of Family Culicidae
Ectoparasitism and lesions due to arthropod are Anophelinae and Culicinae. Anophelines
bites  include the Anoph eles mosquito, whereas Aedes,
 Anopheles
 A. Order Diptera (Class Insecta: mosquitoes Culex, Mans onia, and Armig
 Mansonia eres mosquitoes are
 Armigeres
and flies) 
flies)  culicines. 

This order is characterized by the presence i. Mechanism of Bite Reaction 

of a single pair of wings. The second pair is Some species bite during the day, while
reduced to small knob-like
knob-lik e structures called others hide and become active at night, dusk
halteres, which are used during flight as   or dawn. Bites are usually inflicted on exposed  
 bima p
lanor ctear ns.cT
ee::her e ar e thr eeee su bor der s of  medical   beiothdeyr s bur ef aice
mms.  eTdhiaeter eoacr tidoenlatyoedthoer ses bit  estimaeys
om
1. SuborderNematocera(e.g.m
ba
l ckfe
i 
i l s,md
, osquto
 i ges,andsande
i 
l 
lf  s).
i es,  both,
Theredepending
deare
pending on the types
three general frequency of contact.
contact  .
of reactions:
r eactions:
Insects under this suborder possess a pair of •   Hemorrha gic macule . There is a
thread-likeantennaeofsimilar segments.There  punctum seen at the site of the bite,
are about 11 to 15 segments for the long type of which may develop without symptoms
antennae. These antennae are longer than the of irritation; in the course of several
head and thorax combined. The mouthparts are days, these marks become darker and
adapted for sucking
su cking blood.
blood.  eventually disappear.
 

294   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

•  Delayed reaction
reaction papule. This may be c. Family Ceratopogonidae (Leptoconops,
Culicoides, midges, “nik
“nik--nik”)
nik”)  
observed from a few hours up to 2
weeks after the bite; there is swelling These insects are small, about 1.5 to 5
accompanied by intense irritation.  mm long. The antennae are long, consisting of
•  Immediate reaction wheals. These about 15 segments. The wings are spotted and
appear within a few minutes of the covered with hairs. The mouthparts are short, 
 bite, but do not last long, usually less 
than an hour; these cause moderate f r oel
elrr a wtiavr edly(Pinlactoen6s p.1ic2u).ouMs,aalleensd aor ennoto t  p
 p.1 apkr eo j belcotoed
irritation. meals. Females stay around vegetation, cow
sheds, muddy debris, and shaded trees. The
The reactions to mosquito bites are
eggs are laid on the surface of mud, wet soil,
associated with the trauma produced by the
cow dung, and other habitats that are moist or
mechanical insertion of the proboscis by the
mosquito. The initial cutaneous reaction is  partiall y submerged in water. Midges
 partially Mid ges usually
due to the sensitizing effect of the saliva. The swarm over the head, biting the face and neck,
n eck,
saliva chemically consists of histamines and and exposed body parts. Lesions are usually in
5-hydroxytryptamine, or kinin.
the form of multiple vesicles, which produce
intense itching. 
b. Family Simulidae (Si
(Simuliumor “black
“black  flies”)
flies”)  

These are humpback dipterans measuring  

1.5 to 4.0 mm long. They are usually black in
color, but may sometimes be gray. They have
short legs and short antennae. The mouthparts
are short and relatively inconspicuous (Plate
6.11). Only the females bite, though their
mouthparts do not penetrate the host’s deeper
tissues. These dipterans usually stay near
vegetation. Its intermediate stages breed in fast
flowing streams. 
flowing streams. Plate 6.12. Midge (Culicoidesspp.)
The lesions produced are characterized (Courtesy of Dr. Lilian de las Llagas)  
 by localized swelling and inflammation,
accompanied by an intense irritation, which d. Family Psychodidae (Phlebotomus, sandfly,
mothfly)
lasts for several
s everal weeks. 
These flies are small, about 2 to 5 mm
long. The body and wings are entirely covered
with hairs, thereby giving them the appearance
of small moths. The wings are lanceolate in
shape and have simple wing venation. The
antennae have 12 to 16 segments. The legs are
long and slender. The mouthparts are short and
inconspicuous (Plate 6.13). Only the females
 bite, feeding at night. They hide in dark corners
during the day. They usually attack the face and
the neck, and produce vesicles or wheals. Intense
itching, pain, heat, and swelling occur. A blue
Plate 6.11. Blackfly (Simuliumsp.)
(Courtesy of Dr. Lilian de las Llagas) 
scar often remains. 
 

CHAPTER 6: Arthropods and Mollusks of Medical Importance  295 

Plate 6.13. Sandfly (Phlebotomus

(Phlebotomus spp.) Plate 6.14. Horsefly (Tabanusspp.)
(Courtesy of Dr. Lilian de las Llagas) (Courtesy of Dr. Lilian de las Llagas) 

Eggs require a moist environment with habitat, where the environment is moist. Most
high humidity, such as holes in the ground and species are aquatic or semi-aquatic.  
leaf litters. Because of their mouthparts, these flies
inflict very painful bites, resulting in erythema  
2. SuborderBrachycera(e.g.,horse ii 
e
fl sand 
deer flii 
e s) and swelling. Their attacks are usually persistent,
 produci ng multiple
 producing multipl e painful non-pruritic
non-pru ritic lesions  
The antennae are shorter than the head on exposed areas. 
and thorax combined, and is composed of
3. Subor 
er   C 
d  o
c 
y 
l rr   apha
  / 
O t   hor 
/ r  e.g 
apha ( g,.h ousef 
e omo
l i s,St  s,“ 
y 
 x 
 x bt 
n housey 
i g  ”,l 
f 
three segments. The third segment is enlarged andotherbti ngf iles)
and bears a terminal bristle called the style. The
mouthparts belong to the cutting-sponging The antennae consist of three segments.  
type. The third segment is enlarged and carries
a. Family Tabanidae (Tabanus and Chrysops) 
a conspicuous bristle called the arista. The 
mouthparts are of the sponging and piercing
These flies  vary in size depending on the
flies vary types.
species. They can be smaller than a housefly, or This fly  resembles the housefly
fly resembles housefly  ( Musca)
they can be very large, measuring 5 to 25 mm. very closely, but differs from the housefly by
Tabanus (horse fly)  is uniformly black but has
fly) is having a piercing-sucking type of mouthparts.  
whitish markings on the thorax and abdomen. It has four brown-black longitudinal bands on
Its wings
fly)
fly)  are clear
 is smaller (Plate
than the 6.14).
horse (deer
Chrysops
fly  and has a more
fly
its thorax, and its antennae are of the aristate
type. It breeds in moist, rotting, and fermenting
rounded head. The middle part of its wing is vegetable matter, such as grass, hay, or horse
 patterned with a brown coloration. Males of manure. Both males and females suck blood.
these flies
flies do
 do not bite. Eggs are deposited on They are active at daytime and bite outdoors.
the underside of leaves, twigs, stems, stones, They inflict very painful 
painful bites. 
and rocks overhanging or adjacent to their larval  
 

296   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

B. Order Anoplura (sucking lice) 

lice)  further development. Severe infestations may
These are wingless permanent ectoparasites
result in the hair becoming matted with eggs.
Itching is usually the predominant symptom.  
of mammals.
length. Theyis measure
The body 1.5 to 3flattened
dorsoventrally mm in The itching is attributed to the injection
and usually gray in color. Lice are strictly
of the saliva, and may also be a reaction to lice
host-specific.
host- specific. Head lice and genital lice, for  
feces. The intensity of itching varies from one
 person to another,
another, and this is highly correlated 
nf les,t adr eom
enxoatmi p ets. aTnhdeyotdhoer
seesnticonhloyuisne houldm pan with the degree of infestation.  
pubis (genital louse, pubic/crab
 Phthirus pubis
animals. Both species belong to the family
Pediculidae, having mouthparts adapted for louse) has a crab-like body. It is nearly as broad
as it is long and measures about 1.5 to 2 mm.
 piercing-sucking. 
The middle and hind legs are stouter than the
 Pediculus humanus capitis is also called the
first pair. Pubic lice infestation is more common
head louse. The male measures 2 to 3 mm and
in adults rather than in children (Plate 6.16).
the female 3 to 4 mm in length. Its head is
Transmission usually results from intimate
small compared to its body size. It is narrow and contact. Ordinarily, the pubic louse confines its
 pointed in front, and has antennae with four to
five segments.
five  segments. Its legs are of the clinging type
activities
activiti es to pubic
pu bic hairs,
hairs , but it may also be foun
foundd
in other parts of the body where hair is coarser,
and are of equal size. It is found on the scalp
(Plate 6.15). 
such as axillary hair, eyebrows, or eyelashes. 
Patients with pubic lice infestation
Head lice infestation is very common in
the Philippines. Children are most commonly   were found to be concomitantly infected  
affected. This condition is very much associated w . I-ntf r easntasm
goitnhor sr ehxeuaa)lly d itihnf tehctisiolnosus(e .igs.,
tioitntew
with warm weather, as the lice require this for   commonly associated with complaints of
intense pruritus in the affected region due to
the presence of nits or eggs.  
Other lice include  Haematopinus (hog
louse), Trichodectes canis (dog biting louse),  

Plate 6.15. Louse (Ped c i uu s )

l shumanuscapt ii  Plate 6.16. Pubic louse (Phthiruspubis )
(Courtesy of Dr. Lilian de las Llagas)   (Courtesy of Dr. Lilian de las Llagas)  
 

CHAPTER 6: Arthropods and Mollusks of Medical Importance  297 

athus (cattle louse),  Menop

 Linognathus
 Linogn on (chicken
 Menopon time. Any change in humidity, temperature, or
louse), and Columbicola (pigeon louse). These vibration stimulates the pupae to escape from
are lice of domestic animals, and they do not their cocoons and enable them to emerge
emer ge as
attack or infest humans.
All lice have similar life histories. The adult adults. As fleas suck blood from their
inject saliva to prevent the host’s
hosts, they
host’s blood
 blood from
lays eggs, which are called nits. These appear as clotting. This secretion contains amino acids,
white or gray oval bodies which are glued to the    peptides , ketones, low molecular weight sugars,  
 peptides,
hair by the head, or by the gonopod, as seen  polyhydric
 polyhyd ric alcohols,
al cohols, phenols, aldehydes, and
in pubic lice. The young resemble the adults,  phosphates, all of which are capable of inducing
inducing
except in size. They require at least 1 week to   sensitivity in the host. 
complete development.  Bites appear as small punctures, which
C. Order Siphonaptera (fleas) 
(fleas) 
represent areas probed by the fleas. Initially, the
flea explores the exposed skin area completely,
These are wingless insects measuring less frequently stopping to probe the surface without
than 4 mm, usually l.4 to 2 mm in length. necessarily feeding at each probe site. Once a
The body is laterally compressed and covered suitable site is selected, the flea bites and remains
with spines which enable them to move freely. attached. It then moves along, biting and feeding
The antennae are short, three-segmented, in a grouped but irregular pattern, resulting in
club-shaped, and embedded in a deep groove. multiple lesions. Grouping, therefore, is one
The legs are adapted for jumping, allowing of the most distinct descriptions of the lesions.
them to jump as far as 28 cm vertically or 32  Appearing immediately around the probe 
r oghr oesr si b
cm
 p talelayn.  sOonf   shsm
zoynm or ot jouthm psusr af ancdesr ,utnhneiyng. seir tyethisem e  if tr homor thwei p
a  aw. hAesaildw thr oeusetnacec om maunlty p
f    p iinlge
Both sexes feed on blood. The mouthparts are zigzag lesions, the diagnosis of flea bites is also
adapted for piercing and sucking. Compound confirmed by previous exposure to animal hosts. 
eyes are lacking. Some species, however, possess D. Order Hemiptera (bed bugs) 
bugs) 
degenerate eyes without distinct facets, while
others are completely blind. In some specie
species,
s, Cimex hemipterus is common in tropical
a conspicuous row of spines or a “comb”  climates. Bed bugs inflict  very irritating and
inflict very
is present. This is useful in recognizing the itchy bites. On examination, multiple bite
different species of fleas.  lesions are found with erythematous wheals
The most common s p r et enoce phal id e s
 pecies aC  of uniform size with red punctate centers that
canis (dog flea),
flea),  C.
C. felis (cat flea),  
flea),  Pulex irritans  persist for many days. The skin condition
conditi on caused
(human flea), and  Xenop
 Xenopsylla heopiss (rat flea).
sylla ccheopi  by a Cimex bite is called cimicosis. Bed bugs are
Although Ctenocephalides preferably feed on generally nocturnal feeders (Plate 6.17).  
dogs and cats, they can also bite humans when   The bug uses its beak-like proboscis,  
their preferred hosts are not around.   with its mandibles and maxillae, to pierce or

thanFleas
lice do.
remain
Female
on their
fleas,hosts
 after less
bloodconstantly
feeding,  puncture the skin ofThe
from the capillaries. the host. It feedsof
combination directly
initial
lay their eggs on the fur of the hosts, in dust, skin piercing, and the subsequent probing for  
on debris, in floor  cracks,
 cracks, and under rugs and  blood, results in swelling and irritation. It is
carpets. The larvae feed on organic debris. They reported that the amount of saliva injected
usually avoid light. Pupae emerge after 10 to  by the bed bug is around 0.16 µL. This saliva
12 days and may remain inactive for some   contains an anticoagu
anticoagulant.
lant.
 

298   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

1. Mi 
tes
 
a. Chigger infestation

Chigger infestation is caused by the larval

stage of Leptotrombidium species. The larvae
feed on the host’s epidermal cells. Infestation
usually occurs when one walks through long 
grass, or when one sits or lies on infested
ground. Chigger bites cause intense pruritus 
and severe reactions may also occur.  
The larval chigger is very small, about 0.15
to 0.3 mm long depending on the t he species. The
larva may increase its size six-fold after feeding.
It is usually reddish-orange, but may be pale
or yellow. There are three pairs of legs covered
with fine hairs. It does not burrow into the host
Plate 6.17. Bedbug (Cimex sp.)sp.)
(Courtesy of Dr. Lilian de las Llagas)  
skin; but merely attaches itself using its large,
segmented palps and blade-like chelicerae. It
E. Order Acarina (mites and ticks) 
ticks)  secretes powerful digestive enzymes, which
liquefy epidermal cells, and the resultant fluid
The majority of mites and ticks (Table   serves as its main m ain diet. 
f 6f o.3r ) asr ewr iothuntdhoe r hoevadl , dtohr osr oavxe,natnr adllya bded por mesesned
r m host Asoltohnouaf gther tf heedcihnig,gtehr elahr ovsat r 
der soposnoseff mthaye
fused together, lacking visible segmentation.  persist for
f or weeks. Itching
Itch ing begins
beg ins a few hours
h ours
The anterior portion is modified to form a after the chigger has attached itself to the
capitulum, made up of a central hypostome, and skin, which transforms the affected area into
 paired chelicerae and palpi, used for attachment a wheal. In heavy infestations, a patient may
and obtaining food.  find  it almost impossible to sleep because of the
intense pruritus, since the heat of a warm
w arm bed
Table 6.3. Principal differences between mites
and ticks 
may intensify the itching. Pruritus gradually
decreases and resolves after 5 to 14 1 4 days. The
chigger usually attacks the legs, or attaches itself
to skin in areas where skin meets clothing, such
as the edges of a brassiere, the waistband of
underwear, and the tops of socks.  
Diagnosis of chigger infestation can usually 
Size Usuallysmall  be made on the basis of a history of previous
outdoor exposure, and typical skin lesions in  
areas where clothing is snug.  
b. Scabies

Scabies (“galis-aso”) is caused by Sarcoptes

 scabiei . It is a contagious skin infection. 
Infestation with this mite is seen in all age  
 

CHAPTER 6: Arthropods and Mollusks of Medical Importance  299 

groups, and is very common in crowded stumpy legs, and the abdomen is annulated.
dwellings. The usual transfer of the mite is by Other than Demodex, infestation may also
direct contact. The variety of S. scabiei that  be caused by  Derma nyssuss (red poultry mite),
 Dermanyssu
causes sarcoptic mange in dogs can also burrow Ornithonyssus (tropical rat mite), Pyemotes (grain
in human skin but stays only for a limited itch mite), and Acarus (cheese mite).
duration. The mite causes intense pruritus
that is more severe at night and may persist for   •   Dermanyssus . This mite is known 
some time.  
The female mite is 0.3 to 0.45 mm
asaitnes,o bf  uwt iilds   b
taocnk  phaur m
tcomatm acitr udasl.lyIta
feeds on blood, causing irritation
in length. It is whitish, disc-shaped, and
and discomfort. Its common name
flat
flattened
tened ventrally. The mite is covered with
is derived from its ability to thrive in
membranous,
membrano us, small, peg-like protuberances,
protuberances, has  poultry houses. The adult is about 1
a few bristles, both dorsally and ventrally. The mm long and its red color is due to
mite has a few lines across the body, giving it a
ingested blood. The mouthparts are
striated appearance. 
modified  for piercing and sucking.  
modified
The female mite favors places on the body •  Ornithonyssus. This mite attacks people
where the skin is wrinkled, such as wrists,
living in rat-infested buildings, like
elbows, feet, penis, scrotum, breasts, axillae, dormitories, restaurants, warehouses,
and in between fingers.
fingers.  Using its short, stout,
sharp pincer-like chelicerae,
chelicerae, the mite digs and and granaries. It is capable of inflicting
a bite that is irritating and painful.
eats its way through the surface of the stratum  Ornithonyssus generally resembles  D. D.  
caotr unenum
el .tIhte bnuf r ei esdistsoenlf , leiqxcuaivdasteoso, zaindg cf reoamtes
 gallinae, and is also red after a blood
meal.
dermal cells. During the mite’s  progress along
•   Pyemotes . People handling infested
the tunnel, it lays about four to six eggs and
grain, cotton, and hay may develop
sometimes defecates while feeding. 
dermatitis due to this mite. The adult
Definitive diagnosis is by demonstration
is about 0.2 to 0.3 mm, and is whitish
of the female mite. Physical examination of the
 patient reveals mite burrows.
burrow s. In chronic
chroni c cases, or yellowish. The female has a pair of
the skin becomes eczematoid.  
club-shaped setae between its first and
second pair of legs. The male is about 
c. Demod 
e oc 
l i ul or 
 x f 
 x  umand Demod 
e ev 
si  
 x br  0.16 mm, has a broader body, and has
no club-shaped setae on its thorax.  
 Demodex folliculorum (on face) and
•  Glycyphagus ,  Aca rus , Tyrophagus .
bre vis (on face and trunk) cause
 Demodex brevis
These stored product mites cause
follicle mite infestation. These mites are found dermatitis in humans often called  
in the hair follicles and sebaceous secretions of  
humans. They are sometimes present on the skin r asilhle, r dse, pger nodcienr gs,ocno pthr ae, mor atewr oiar lker s
m ’ ’ ’

mites,
and usually
especially
cause D.nofollicu
severe
folliculorumsymptoms.
lorum , are associated
These  being handled. These parasites can
also precipitate an attack of bronchial
with “black  heads.”
heads.”  On rare occasions, the mites  
asthma. These mites are about 0.4 to  
 produce an erythematous
erythemat ous follicular
folli cular eruption in 0.5 mm long. They are whitish or pale
the beard area of men. 
yellow in color and resemble Pyemot
 Pyemotes
es
The adult mite is usually less than 0.5 mm mites, though their chelicerae are large,
in length, and is worm-like and elongated
elong ated in
and the setae on their bodies are longer
appearance.. The thorax bears eight very short, 
appearance and more conspicuous. 
 

300   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

2. Ti 
cks Inhalant Allergens 
 
Two types of ticks bite humans: soft Decomposed and pulverized arthropods,
or Argasid,
ticks, which and hard or  to
are difficult Ixodid ticks.
remove, areHard
more  cast skin, scales,
 permeate the airhairs,
via spines,
upwardcocoons, and webs
air streams and
frequently encountered. Ticks are readily convection currents, and are thus considered
distinguished from insects by their strongly   inhalant allergens of humans (Plate 6.18). Their  
f aunsdedistchao pr a bxlaenodf ga b
r edaot m ena.nTsihoen b, p
ex p  odar 
ytiscuolvaor ilydianl r deilsaetaisoenhshas p
i  b n jt-er cets p
p eteon itnhheaslua b of ir ianttoer r yesat lolef r m
giacny
females. There are six legs in the larval stage, and workers in the field of allergology.  
eight in the nymphal and adult stages. Ticks are
 bigger than mites and are usually more than 1
mm in length. The head bears the mouthparts,
which consist of two small, retractile mandibles
or chelicerae, a pair of short palpi, and a well-
w ell-
developed hypostome armed with teeth. 
Generally, ticks pass through
thro ugh th
thee egg, larval,
larval,
nymphal, and adult stages over months or years.
Eggs are usually laid on the ground in batches
of 100 to 18,000. The larvae emerge and climb
up any available object in order to reach passing
hosts. Ticks
Ticks of some species remain on the same  
host until they reach maturity, but others find
two or more hosts for their blood meal. Females
take prolonged blood meals lasting for 8 to 10
days. Males, however, remain attached to the  
host only for a few hours in order to mate with
w ith
females. 
Plate 6.18. Butterfly scales
Once the tick comes in contact with a host, (Courtesy of Dr. Lilian de las Llagas)
the hypostome and chelicerae are inserted into
the skin. Using their recurved teeth, a firm
hold is maintained, reinforced by a cement-like Despite the close association between
secretion. The tick can detach quickly once it arthropods and respiratory allergy, there is
is fully engorged without the host noticing still no direct evidence available to justify this.
it. Forceful removal of the tick may result
r esult in Evidence has stemmed from positive skin tests
granuloma formation which may persist for days  utilizing arthropod extracts, the inability to find
find  

omr aeyv bene dmuoenttohesiathf ter athr ea bcittioe.nTtohim
s gor uatnh p
ulaor m osytm iosl,ogaincdal tf haect porsesteoncex polr aina br uens  ppdiar nactoer y
er teotm
tsa,
h p

or to injected salivary secretions. The granuloma of arthropods

coinciding withinthe
thepatients’
immediate environment
allergic symptoms.
measures 0.5 to 2 cm.
Tick paralysis is an acute disorder of the The work of Agbayani et al . in 1989 showed
central nervous system, and is believed to be this relationship. 
caused by a neurotoxin secreted by the salivary House dust mites ( Dermatophagoides) have
 Dermatophagoides
gland of many species of ticks in the process of also been implicated as a source of allergens
 prolonged feeding.   by some investigators.
investig ators. A study on house dust
du st 
 

CHAPTER 6: Arthropods and Mollusks of Medical Importance  301 

mites (HDM) by de las Llagas and Abong spp., Cheyletus malaccensis , and Suidasia
(2002) on the association between mites and  pontifica (Plates 6.19 – 6.22).
6.22).
respiratory allergy showed the presence of six Winged insects such as mayflies
species of HDM in dust samples collected from (Order Ephemeroptera), caddisflies (Order
houses of patients with a history of bronchial Trichoptera), moths and butterflies (Order
asthma and allergic rhinitis. These mites   Lepidoptera), and aphids (Order Hemiptera),
are  Dermatophagoide
 Dermatophagoidess pteronyssinus ,  Blomia have been observed to be the most common  
tropicalis, Glycyphagus spp.,  Austr
 Austroglycyphagus 
oglycyphagus arthropods inducing
inducing respiratory allergy. 

Plate 6.19. Dust mite (Bol ma

i tropc
ia lis) Plate 6.20. Dust mite (G
(Glycyphagussp.)
ssp.)
(Courtesy of Dr. Lilian de las Llagas) (Courtesy of Dr. Lilian de las Llagas)

Plate 6.21. Dust mite (Dermatophagoides eronyss inus)

pt  Plate 6.22. Dust mite (Chey letus
sm
mal accens s
i)

(Courtesy of Dr. Lilian de las Llagas)   (Courtesy of Dr. Lilian de las Llagas)

Ingestants   pathogenicc to humans. Diarrheal diseases have

 pathogeni
long been associated with these arthropods.  
The feces of cockroaches and the vomitus of Various mites and their eggs, either living
non-biting flies are the best examples of harmful or dead, have been found in various parts of the
ingestants of man. These ingestants are highly human body, such as the alimentary canal and
contaminated with microorganisms, which are   urinary tract. The presence of mites has been  
 

302   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

found to be contributory to various conditions

including enteritis, nocturnal enuresis, and
hematuria. The evidence, however, is notdirect
 because in many cases, the mites are quite
harmless.
The most common mites present on food
include species
speci es in the generaTyrophagus, Acarus
 Acarus,
and Glycyphagus . 
Food and Water Pests 

Food and water adulteration/contam

adulteration/contamination
ination
due to insects and mites may be incurred in any
of six stages: storage, transport, preparation,
 processing , packaging,
 processing, packagin g, and serving.
serving . The insects Plate 6.23. Maggots
and mites discussed in this chapter are classified (Courtesy of Dr. Lilian de las Llagas)  
as pests because of the damage done on food and
water and the potential risk to humans upon
u pon this occurs accidentally, but for some
s ome species,
consumption (Table 6.4).  parasitis m is necessary. Obligatory
 parasitism Obligat ory myiasis
myias is is
the condition wherein larvae need a host to
Table 6.4 Arthropods as pests of stored products, complete their development. Facultative myiasis
food and water sources identified at the   occurs when free-living larvae become parasitic.  
Medical Entomology
Entomology Laboratory, UP-CPH Clinically, myiasis may be classified
according to the part of the body invaded.  
Aural, nasal, ophthalmic, cutaneous, and
intestinal myiases have been reported. In the
Philippines, myiasis is caused by the following
species of fly larvae.
fly  larvae. 
•  Obligatory  
(Podainerpuncela)lttil (Chrysomya ,  Boopunus , Stomoxys ,
 Lyperosia) 

Animals primarily
primaril y affected include
include
carabaos, cattle, and other domestic
animals. 
•  Facultative
Phoridfly
 Phaenicia

 Lucilia
(Blatellagermanica) •   Accidental
Sarcophaga
 Pericoma
Myiasis 
Identification of Myiasis-Producing Larvae 
Myiasis is the infestation or invasion of
tissues or organs of humans and animals by The identification ooff fly larvae is important
dipterous larvae (Plate 6.23). Sometimes,   for prevention and control. In forensic medicine, 
 

CHAPTER 6: Arthropods and Mollusks of Medical Importance  303 

identification of the species and age of the References 

larvae can help establish the time of death of a
victim. Identification is done by examining the Baltazar CR, Salazar NP.Philippine
Philip pine insects:
insects : an
morphology of the posterior
p osterior spiracles and the introduction.
the Quezon
Philippines Press;City: University
1979.   of
of
cephalo-pharyngeal skeletons. 
Maggots, the larvae of muscoid diptera, are de las Llagas LA, Abong J. Identification and
legless, worm-like and more or less cylindrical.
cylindrical.  characterization
characterization of local house dust mites:  
They are usually tapered anteriorly and broad iael nf otar ln, adtiavgenaollsetr igce, na p
exo ptenr itm
 p ndr otdhuecr ta p
ioenuf toicr
 posteriorly. The spiracles are situated on the
use in the local setting. 2003. Located
 posterior end (Table
(Table 6.5). 
at: College of Public Health Library,
University of the Philippines Manila.  
Table 6.5. Identifying characteristics of some
myiasis-producing larva 
Borror DJ, Delong DM, Triplehorn CA. An
introduction to the study of insects. 4th ed.
Larva USA: Holt, Rinehart and Winston; 1976. 
Cagampang-Ramos
Cagampang- Ramos A, Darsie RF Jr. Illustrated
keys to the  Anopheles mosquito of the
Philippine Islands. San Francisco: USAF
Fifth Epidemiological Flight, PACAF,
technical report 70 – 1;
1; 1970. 
Jueco N, de Leon W. A case of aural myiasis.  
Acta Med Philipp. 1984;20(2):18 – 2
20.
0. 
Service MW. A guide to medical entomology.
1st ed. Hongkong: The MacMillan Press
Ltd.; 1980. 
Taboada O. Manual of medical entomology.
USA: US Government Printing Office;
1968. 
 

304   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 Arthropods as Vectors
Vectors of Disease
Lillian de las Llagas

Arthropods as Transmitters of Pathogenic their bodies. Some vectors (e.g., fleas, beetles,

Agents  crabs, and copepods) serve as intermediate hosts
rthropods which are capable of acquiring to some parasites. 
A   and transmitting pathogens that cause  
diseases are called vectors. There are two types
Most of the arthropods which are classified  
as vectors of diseases belong to Class Insecta,
subclass Pterygota (winged insects such as
of vectors: biological vectors and mechanical
or passive vectors. Biological vectors, (e.g.,
mosquitoes, flies, and cockroaches) and Order
Acarina (mites and ticks). 
mosquitoes and biting flies),  acquire pathogenic
agents in the act of blood-feeding. These
Several arthropod-associated diseases in
agents undergo multiplication, propagation,
the Philippines are summarized in Table 6.6.
The diseases listed have varying degrees of
and development inside the arthropod’s body.
After some time, the pathogens assume their
importance. Based on morbidity and mortality,
infective form and are then transmitted from
the most important diseases are the mosquito-
one host to another. Mechanical vectors, on
 borne diseases. Others do not rank high among
national health care priorities, but they have
the other hand, transmit pathogens by way of
their oral secretions (vomitus of flies)
flies) and
 and the  significant public health implications implications.. Diseases 
contaminated external surfaces of their body a(es.sgo.c,iadtieadrr whietah acnodckr aomaec bhieassaisn)danr eonim
- b
 b pitoinr tganflti,es
(feet, wings, etc.). Mechanical vectors serve although evidence linking diseases to the
as mere contaminators; the pathogens do not  filthy behavior of these arthropods is purely
undergo multiplication or development inside  circumstantial.  

Table 6.6. List of arthropod-associated diseases and their corresponding agents and vectors  

Disease

Filariasis

Dengue/DengueHemorrhagicFever   Denguevirus   Mosquito 

JapaneseEncephalitis JvEirus Mosquito  

Scrub typhus  Rickettsia Chigger Mite  

Babesiosis Babesia Tick 

Paragonimiasis   Paragonimus Crab 

Diphyllobothriasis Diphyllobothrium Copepod 

Dracunculiasis  Dracunculus Copepod 

Hymenolepiasis   Hymenolepis Flea 

Dipylidiasis Dipylidium Flea 

Raillietiniasis Railletina Flour or Rice Beetle 

 Amebiasis  Entamoeba  
Entamoeba Flies and Cockroaches  

DiarrhealDisease  Entericpathogens   FliesandCockroaches  

Miscellaneous
Miscellaneous Intestinal Parasitoses    Ascaris,Trichuris Flies and Cockroaches  
 

CHAPTER 6: Arthropods and Mollusks of Medical Importance  305 

The succeeding topics describe the most organ called the siphon, which extends from
important vectors of tropical diseases in the the eighth abdominal segment. The culicine
Philippines:mosquitoes, flies, and cockroaches.  larva therefore hangs down from the
th e surface of
Mosquitoes  the water by the tip of the siphon in order to
 breathe. The Culex larva has a long and slender
There are two important divisions or siphon, with many ventral hair tufts. Aedes has
tribes of mosquito vectors. The anopheline   a short and stout siphon with only one pair of  
mosquitoes, consisting of Genus  Anopheles , hair tufts. Mansonia breathes through
 Mansonia throu gh a siphon
which are vectors of human malaria and human modified for piercing and adhering to stems of
filariasis; and the culicine mosquitoes, vectors aquatic plants. 
of dengue, Japanese encephalitis, and human C. Pupa  
filariasis, which includes the genera  Aedes ,
Culex, and Mansonia. Mosquitoes undergo a This is the non-feeding stage, found on the
complete type of metamorphosis. Fertilized surface of the water sources. The pupa is mobile
eggs go through four larval stages, develop into and is able to dive rapidly when disturbed. It
the comma-shaped pupae, and then emerge as  breathes through
throug h a pair of respiratory
respirato ry trumpets.
adults. The immature stages require an aquatic Culicine pupae have longer trumpets than
environment, while the adult, an aerial and anophelines. 
terrestrial one.  D.  Adult  
 A. Egg  
Generally, the wings of anophelines have  
alhlyeloi nver s  tlahye  tshuer f fia r ce
indivAidnuo p  booaf t -wshaat per e,deaecghgs uan p
d edalweinar gesa. sA, nwohther eer avsiscualicdiinsetisnchtaivoen is
r katatner dn p
having lateral air floats to keep it buoyant.
buoyan t. that, at rest, the body of an anopheline mosquito
Culex lay their eggs in rafts. Each Culex egg is forms an angle nearly vertical with the surface
cigar-shaped, and is provided with a corolla at (i.e., the head, thorax, and abdomen are in a
the end. Manso nia lay their eggs under leaves of
 Mansonia straight line). The culicine mosquito, on the
aquatic plants. Aedes
 Aedes eggs are laid individually, other hand, lies almost parallel to the surface,
often in artificial containers, and dry hollows, sometimes appearing as “hump
“hump-- backed.”
 backed.” 
which become flooded
flooded after
 after the rain. These The abdominal tip is pointed in the
“dry-laid” eggs are able to retain their viability female Aedes, and blunt in Culex. Mansonia has
 Mansonia
for long periods without water.  speckled legs with asymmetrical brown, yellow,
and gold scales. 
B. Larva  
Larva
Palpi of female Anopheles are as long as the
 Anopheles
Eggs of mosquitoes generally hatch after 2  proboscis. Palpi of its males are club-shaped,
to 3 days of contact with water. They are about each with rounded scutellum. Palpi of female 
1 to 1.5 mm long when newly hatched and grow culicines are not as long as the proboscis (usually
to
itsaskin
fullfour
length of about
times. 8 mm.
The stages The larva
between casts
molts are a quarter
are of the proboscis);
not clubbed, male culicine
and the scutellum palpi  
is trilobed.
known as instars. The mosquito larva breathes E. Mosquito Bionomics  
through two openings called spiracles. The
spiracles of the anopheline larvae are situated Bionomics deals with the relationship
on the eighth abdominal segment so that in  between a species and its environment. An
order to breathe, the larva rests in a horizontal understanding of mosquito bionomics is
 positionn at the surface of the water. In culicines,
 positio important in the epidemiology of mosquito
the spiracles are situated at the end of a tubular    borne diseases, and in planning methods of  
 

306   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

mosquito control. The environment consists F. Seasonal Prevalence  

of the climate, the water habitat of immature
In tropical countries, such as the
stages, and the hosts for the adults. The
environment of immature and adult mosquitoes Philippines,
fluctuations inwhere there areand
temperature no extreme
humidity,
is interdependent, because the female mosquito rainfall is the most important factor affecting
must have access to water for egg-laying.
the mosquito population. The rise and fall of the 
The adult environment is largely aerial and  
terrestrial, the former for mating and dispersal, queintodednetnosintyt,hcealalevdailsa b
is  odse p
m atlieon,
eaisloitnyalof flusucittu b
and the latter for feeding and resting.
aquatic environments, which can support the
The Environment and Habits of the Adult multiplication of the mosquito.  
Mosquito  The Philippines has four types of climate
 A. Mating  
 based on monthly rainfall. Typ
Typee I areas have two
 pronounced
 pronou nced seasons, dry and wet; Type
Type II areas
Mating usually occurs within 24 to 48 have no dry season, but with a very pronounced
hours after emergence. In some species, the rainfall; Type III areas have seasons not very
males form a swarm, usually at dawn or in the  pronounced;
 pronou nced; and Ty
Type
peIV,where rainfall
rainfal l is more
evening. Females entering the swarm are seized, or less evenly distributed throughout the year. 
and the resulting pairs drop out of the swarm. With these types of climate, it is possible
Insemination then follows. to expect the following: 

•
B. Dispersal     In Type I areas, it is possible to
The male is a much weaker flyer  than
 than the
female. Most mosquitoes fly within a range of 1   anedakths:e oontheedr   bur eif nogr e
inatveer mtwitotendtenr asiintys  p
h

to 2 km. Strong winds carry mosquitoes along the onset of heavy rains. 
greater distances.  •   In Type II areas, more breed ing
grounds are expected  
C. Biting Habits  
•   In Types III and IV areas, there will be
Host seeking and feeding generally take no peak months; thus, mosquito
 place in a warm, humid environment. Biting  populations
 populati ons are maintained at certain
hours vary from one species to another. Culex, levels.
 Mansonia , and Anopheles prefer to bite at night G. Extrinsic Incubation Period and Longevity  
while Aedesduring daytime. Mosquitoes which
feed while inside human dwellings are described The climate in which the mosquito lives
as endophagic, while those that feed outdoors dictates its capability for disease transmission.
are called exophagic.  The climate influences the rate of development
of the parasite within the vector, and the
D. Resting Habits   longevity of the mosquito. 
After feeding, adult mosquitoes may rest The blood
infected periodmeal
between
and itsthe mosquito’s
mosquito’s 
transmission of 
inside dwellings, referred to as endophily or may
rest outdoors, referred to as exophily.   the infective agent in a subsequent feeding is
called the extrinsic incubation period. It varies
Host Preference  
E.
in length in response to the temperature of the
Mosquitoes that feed on humans
hu mans are called host mosquito’s environment. For example,
anthrophilic, whereas those that feed on animals the development of the malaria parasite,
are zoophilic.  Plasmodium is retarded at 19°C down to 15°C  
 

CHAPTER 6: Arthropods and Mollusks of Medical Importance  307 

and below, but completed at 20 to 30°C. Also, outside human dwellings. This may indicate
the growth of the filarial
filarial parasite
 parasite Wuchereria that An. flavirostris exhibits certain degrees of
flavirostris
in Culex quinquefasciatus is inhibited at mean exophily and exophagy. These observations
o bservations
temperatures below 24°C and above 34°C.   deserve serious attention, as the current indoor
Temperature and humidity affect the residual spraying of insecticide may no longer
survival of mosquitoes. At extremely high or low  be effective. 
humidities, mosquitoes are unable to regulate  Deviations in the characteristics of this  
their water loss. They thrive best at 70 to 80% mosquito have been observed, and this may
relative humidity and at a temperature of 20 disqualify the claim that  Anophe
 Anopheles
les fla
flaviros
virostris
tris
to 30°C. is made up of one or two species.  
Major Mosquito-Borne Diseases  2.  Anopheles litoralis

 A. Malaria  This small- to medium-sized mosquito

The vectors of malaria in the Philippines
Philippines is a secondary vector (supplementary role in
include:  Anophe les fflav
laviros tris , the primary
irostris
transmission but would be unable to maintain  
vector of malaria;  Ano phe les li tor aliss and
torali
an epidemic in the absence of primary vector) of
malaria. It has palps with three pale bands: the
 Anopheles
 Anopheles b
balabacensis. Anoph
alabacensis  Anopheles
eles fl
flavirostris is
avirostris
 pale band at the tip is broad, the next is narrow,
narrow,
found in the entire national territory, except
in areas with elevations of more than 4,000 ft. and the third very narrow. Its legs are speckled,
 Anopheles litoralis has been described in Basilan,
the hind tarsi possessing apical distinct narrow
various Luzon
L uzon provinces,
provinc es, Southern
Southern Samar, Sulu,
Sulu,   pale bands. They prefer to breed in water with  
Surigao, and Zamboanga.  
 Anopheles
Anoph eles balabacensis
balabacensis 
  a salinity of 2.5 to 3.0%.  
has been reported only in Palawan.   3. Anopheles balbacensis 

Morphologc
i alCharacteristics,Breedni gPl aces,andHabt isofVectorsofMaa
 lra
i  This is also a secondary vector of malaria.
1.  Anopheles flavirostris
flavirostris
It is a small- to medium-sized mosquito having
 palps with narrow pale bands. It has a dark
This is the most important vector of  probosci s and wings with multiple dark spots.
 proboscis
malaria in the Philippines. It is a small- to It also has speckled legs, with wide bands on the
medium-sized mosquito, measuring 2 to 6 mm tibiotarsal joint of the hind legs. This mosquito
in length. It has a proboscis with a pale golden  breeds in clear ponds and pools in deep forests
 patch that is usually confined to its apical half. and jungles. 
The basal third of its costal vein is usually dark
B. Filariasis  
or has a single pale
p ale spot. 
 An. flav irostr is usually breeds in slow 
iro stris The vectors of Bancroftian filariasis in
flowing, clear, partially shaded streams with the Philippines include  Aedes poecilu
poeciluss, which 
vegetation. It also breeds in foothills and in    breeds in abaca-rais
a baca-raising
ing areas, and  Anoph
 Anopheles
eles

wells. During
collect the larvae
the rainy
from season,
rice fields
it is and
possible
trapped
to  flavirostris
streams. The, which breeds
vectors in clearfilariasis
of Malayan mountain in
waters.  the Philippines include Manso
 Mansonia bonneae and 
nia bonneae
This mosquito is widespread in  Mansonia uniformis , which breed in swampy
distribution. It has been reported to be and forested areas.
endophagic, endophilic, and anthrophilic.  Aedespoe
poecilus has been reported in the Bicol
cilus
Recent observations by field entomologists region, Masbate, areas of Mindanao, Mindoro,
showed that female mosquitoes prefer to rest   Quezon and Sulu. Anopheles
 Anopheles flaviro stris  has
 flavirostris has been
shown to transmit the parasite in Mt. Province 
 

308   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

(Bontoc), Palawan and Sulu.  Mansonia has to golden in color. Its legs have many pale
 been found in Agusan del Sur. Eastern Samar, markings, and its wings have white and dark
Palawan, and
a nd Sulu.  broad scales, many of which are asymmetrical.
asymmetri cal.  
Morphologc
i alCharacteristics,Breedni gPl aces,andHab itsofVectorsatF ia
l 
l ra
i ss
i  C. Dengue/Dengue Hemorrhagic Fever  

1.  Aedes poecilus The vectors of dengue in the Philippines

This mosquito is associated with
include Aedes aegypti, which is associated with  
Bancroftian filariasis. It breeds in the axils urban dengue, and  Aedes albopictus
albopic tus , which
of plants like abaca (  Musa textiles ), banana is associated with rural dengue. There is a
( Musa
 Musa sapientum), pandanus, gabi (Colocasia
sapientum
widespread distribution of these vectors in the  
esculentum), and biga ( Alocasia
 Alocasia ma
macrorr hiza). 
crorrhiza
Philippines. 
The adult Aedespoecilu
poeciluss has scutellar scales MorphologicalCharacteristics,BreedingPal ces,andHab itsofVectorsofDengue
that are mostly broad and white. The dark scales 1. Aedes aegypti 
are found on the mid-lobe and form
for m a distinct
dark central patch. A variable number of white This is primarily known as the “tiger
scales are also present at the base of the first four mosquito.” It is black in color, and small to
tarsal segments.  medium in size. It has characteristic lyre-shaped,
This mosquito is a nocturnal feeder.   silvery markings on its mesonotum. The fore-
However, it is possible to
t o find  it seeking a blood and mid-pairs of legs have white narrow bands
meal during the day. It is highly anthrophilic but  at the base of the tarsi. The hind
h ind pair of legs has 
it may feed on animals like birds, bovids, and five broad white bands, hence the name “tiger
dogs. The highest density of these
t hese mosquitoes  mosquito” (Plate 6.24).  
is observed from 10 p.m. to 12 a.m.,
a.m ., which This mosquito breeds in clear water
coincides with W. bancrofti periodicity. The collecting in indoor and outdoor containers
density of these mosquitoes is also related
r elated such as old tires, vases, jars, and bottles.
b ottles. 
to rainfall patterns in endemic areas. This
T his
mosquito is endophilic and partially exophilic.  
2. Mansonia

A vector of the Malayan type of filariasis,

 Ma. bonneoe, is a forest swamp mosquito. It
 prefers fresh water swamps
swam ps with an extensive
growth of giant pandanus. Ma. uniformis also
 breeds in swamps containing other aquatic 

 pl
 plaantTs.hese
hese mosquitoes are exophagic and
exophilic. The peak of biting is observed at 1:00  
a.m. to 2:00 a.m.
The population density of  Aedes mosquitoes
and  Mansonia is related to rainfall patterns.  
3.  Adult Mansonia

It is a medium-sized, robust-built mosquito, Plate 6.24. Ae

 Aedesaegypti mosquito
usually light to dark brown, or light yellow   (Courtesy of Dr. Lilian de las Llagas) 
 

CHAPTER 6: Arthropods and Mollusks of Medical Importance  309 

2. Aedes albopictus  human food. Anatomically, these flies are well

adapted to carry and disseminate pathogenic
The most important diagnostic
agents because of the following structures:  
characteristic
characte
of risticlongitudinal,
a single, of this mosquito is thestripe
silvery presence
on 1.  Sponging mouthparts. The expanded
the mesonotum. This mosquito breeds in labellum has hairs that are capable of
clear water collecting in indoor and outdoor   sweeping or picking up the agents. 

con s   beam
cotaniunter shesullsc,hsoam r  b
tifiocoiasltucomn ptas,inem s,  taynd
r  p 2.  M anner  of  inges ing f ood. A dr o p of
saliva is r egur gitated in the pr ocess and
tree holes. It is not unusual, therefore, to see this contaminates the food.
 both Aedes species sharing a common habitat.  3.  Hairy body and appendages. 
D. Japanese Encephalitis (JE) 
4.  Footpads. These are also contributory
to their pathogen-carrying potential
The proven vector of Japanese encephalitis  because of their sticky secretion. 
in the Philippines is Culex tritaeniorynchus.
Potential vectors include Culex vishnui, Culex Pathogenic agents acquired and carried
 gelidus, and Culex fuscocephalus. The vectors are  by these flies include  As ca ri s , Trichuris
widely distributed in ricefields.  Most cases of JE and hookworm ova. The extent of disease
are from Luzon, particularly from Nueva Ecija.  transmission by adult flies under natural
conditions is difficult to determine. The larvae
Morpho logi 
caCl haract ers
ic
it s,Breed ingP laces of flies may also affect humans. These larvae
 
andHab tisofVectorsofJapaneseEncephai 
ts
i l  or maggots invade living tissues, producing a  
1. Culex tritaeniorynchus
tritaeniorynchus condition called myiasis.  
This is a small mosquito. The mesonotum   A. Muscado mestica (The common housefly) 
is uniformly covered with dense, very small, This fly is dark gray in color and measures
 brown to dark brown scales, which are curved   about 6 to 9 mm in length. It has four
and narrow. Its proboscis
probosci s has a pale band. This  conspicuous longitudinal black bands or stripes
conspicuous
mosquito is usually associated with rice fields.   on its thorax. The arista has dorsal and ventral
Activity is greatest from 6:00 p.m
p.m.. to 7:00  hairs. The wing venation is characterized by
 p.m. The mosquito feeds on man and animals, Vein 4 (V4) bending
bendi ng sharply
sharp ly at the end of Vein
specifically pigs. Pigs serve
s erve as amplifying hosts.  3 (V3). The two veins are therefore very close
Flies   at the edge of the wing.  
The eggs of the commonhousefly
common housefly  are laid
There are different species of non- in masses of about 75 to 150 eggs. A single
 bloodsucking flies that are commonly female is able to lay as many as 21 batches
encountered in our environment. These flies
flies   within a month after emergence. Hatching
that coexist with humans over an extended takes place in about 20 to 24 hours under warm
 period of time
t ime are described
descri bed as synantrophic
synantro phic  
species. The most common representative is the conditions, and the
and eyeless larva, resulting
or the legless,
maggot, headless,
undergoes three
common housefly ( Musca domestica ).  stages of development. The maggot completes
Synantrophic flies are associated with its development in about 5 to 9 days then it
gastrointestinal diseases such as amebiasis, migrates to drier habitats and changes into a
salmonellosis, and shigellosis. This association  pupa. The pupal state requires 4 to 7 days before
stems from their filthy  habits; they feed on
filthy habits; an adult emerges, making a total of about 10
human and animal excreta, then freely feed on  to 17 days of development from egg to adult. 
 

310   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Other species of synantrophic

synantrophic flies include: Cockroaches 
Sarcophaga (flesh fly), Calliphora (blue-bottle
fly), Lucilia
fly), 
  Lucilia (green-bottle fly),
fly),  Muscina
  Muscina (non-
Cockroaches,
Cockroaches, like non- blood
 blood sucking flies,
 biting stable fly),
fly), and
 and Fannia (latrine fly).  are
Thealso
bestcarriers
exampleofofsome
their pathogenic
filthy habitsorganisms.
is feeding
B. Sarcophaga  on human feces and then on human food. 
At least 16 species of cockroaches are  
The adult fly
fly measures
 measures 11 to 15 mm long  
and is gray in color. It has three prominent black cthor neseidmer oesdt ccoam
rr m
ier osnoaf r  p gemntesr .icTanhae,
atehr io  ppgl eanniect aa A
e P 
longitudinal stripes on the dorsum of its thorax. germanica , and  Blatta orientalis .
 Blatella germanica
The abdomen is distinctly marked with squarish  Cockroaches are nocturnally active, but they
dark patches on a gray background, giving it a may be seen crawling at daytime. Cockroaches
“chess - board”
 board” appearance. Adults do  not lay
are much bigger than flies
flies and
 and thus enabling
eggs. Larval development is about 3 to 4 days, them to carry more pathogens.
pat hogens. Transmission of
while stage lasts about 7 to l4 days.  
 pathogen s is facilitated by their hairy chewing
 pathogens
C. Calliphora  
Calliphora mouthparts, which enable them to pick up
 pathogens easily, and their habit of dropping
The face or genae of the adult is covered
their feces while walking or feeding. A study
with yellow hairs. The fly is bluish in color, and conducted in the University of the
t he Philippines
its thoracic hairs are well-developed. The life Manila-College of Public Health in 1981
cycle of this fly requires 16 to 35 days, usually recovered the following parasites and pathogens
pathogens
22 days.  from  Periplaneta
 Periplaneta america
americana
na :  Ascaris
 Ascaris, Trichuris, 
D. Lucilia   and parasites underFamilyThelastomatid
underFamilyThelastomatidae ae and
This fly
fly is
 is greenish in color and has white
Superfamilies Spiruroidea and Tylenchoidea.
Ty lenchoidea.
genae. Its thoracic bristles are well developed, Other pathogens include  Proteus,  Esche richia,
 Escherichia
Salmonella, and Citrobacter .
and there are two pairs of acrostichal bristles on The extent of disease transmission by
its mesothorax. The life cycle of this fly is similar cockroaches under natural conditions is not
to that of Calliphora . A very similar species is
clearly known. 
 Phaenicia (bronze-bottle fly). 
 A. Periplaneta americana (American
E. Muscina  
Muscina
cockroach)  
cockroach)
This fly is slightly larger and more robust This cockroach is chestnut brown to dark
than the housefly. It is dark gray to almost black reddish-brown in color. It is the largest species
in color. It has four longitudinal black bands on among the three most commonly encountered
the thorax,
thorax , and its arista bears setae. Vein
Vein 4 (V4) domestic cockroaches. It measures up to 40  
is notmuch angled, and is clearlyseparated from 
Vein 3 (V3) at the wing margin. mam
h lyngdtehv,ealon pde b
veif nulely  bdowthinmgsa.lleeTahnedf f emalellee,  ainduhletr s
Fannia  
F.
lifetime, lays about
each containing 50 egg
about 15capsules orlength
eggs. The ootheca,
of
This fly
fly resembles
 resembles Musca domestica very the life cycle is from 6 months to a year
y ear (Plate
closely but it is smaller and more slender. The 6.25). 
arista is bare; V3 and V4 are broadly open.  
 

CHAPTER 6: Arthropods and Mollusks of Medical Importance  311 

Plate 6.25. American cockroach (Perp i  laneta Plate 6.27. Oriental cockroach (Bl ataore s )
 i nta lii 
iana)(Courtesy of Dr. Lilian de las Llagas)  
amer c (Courtesy of Dr. Lilian de las Llagas)  

B. Blatella germanica (German cockroach) 

cockroach)  
The Oriental
mm long. It is darkcockroach measures
brown to black
bla 22 toand
ck in color, 27
The German cockroach measures 10 to  
 both sexes show wings that are very short. The 
. Ir toim
1co5lomr.mItinhalesntgwtoh p gitsuhd- b
pinaelenyt ellolonw
s  p  binr aolwdnar ink length of its life cycle is l2 months (Plate 6.27). 
 bands on its pronotum. The female carries the References 
ootheca, which protrudes from the tip of the
Borror DJ, Delong DM, Triplehorn CA. An
abdomen, until hatching time. Its life cycle takes
from 2 to 3 months (Plate 6.26).
introduction to the study of insects. 4th ed.
USA: Holt, Rinehart and Winston; 1976. 
Cagampang-Ramos
Cagampang- Ramos A, Darsie RF Jr. Illustrated
keys to the  Anopheles mosquito of the
Philippine Islands. San Francisco: USAF
Fifth Epidemiological Flight, PACAF,
technical report 70 – l;
l; 1970. 
Service MW. A guide to medical entomology.
1st ed. Hongkong: The MacMillan Press
Ltd.; 1980. 

a,: OU.SMGanovuear lnomf  emnet dPicr ainl teintgom
Ta boUadSA Oof filocgey;. 
1968.

Plate 6.26. German cockroach (Blatela

 ia)((Courtesy
germanc Courtesy of Dr. Lilian de las Llagas)  
 

312   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Medical Malacology 
Lydia R. Leonardo 

ollusks are the second most numerous The medically important snails belong to
animals on earth. They include snails,   Class Gastropoda. They are distributed into  
slugs, clams, oysters, chitons, squids, octopods, two subclasses, namely, Prosobranchiata and
M 
and nautili. One class, the Gastropoda, contains
groups that are directly injurious to man, or
Pulmonata. The prosobranchs are operculate
snails with well-formed shells and gills. They
are essential intermediate hosts of helminth  have a snout-like head-foot, one pair of retractile
 parasites. The poison cone shells have stinging
stingin g tentacles, and one pair of eyes. The sexes are
apparatus that are capable of discharging highly separate, and eggs are usually laid in capsules. 
toxic substances. Trematodes require specific Some are ovoviviparous. On the other
o ther hand,
species of mollusk as their
th eir intermediate hosts.  pulmonates
 pulmon ates are air-breathin
air- breathingg snails and
an d slugs
The astrongyliid nematodes use the ordinary with shells that are reduced or even absent,
garden snails and slugs as intermediate hosts and with a head-foot that bears two pairs of
to complete their life cycle. Some 350 snail tentacles. All pulmonates are monoecious, and
species are estimated to be of possible medical most are oviparous.  
or veterinary importance because of their The distribution of the medically important
involvement in the life cycle of human parasites.  snails in the two subclasses is as follows:
axaolancoom
gye,daincadl tm
ecoloM thse b
loygyof d esnalasilwgir thou p  thiaotloagr ey,  A. Subclass P rosobranchiata
rosobranchiata  

of medical and public health importance. This 1. OrderNeogastropoda

fundamental knowledge is an important basis Family Conidae – 
Conidae –  species
 species Conus
Conus  
for designing control and prevention programs
for helminth parasites with snail intermediate 2. OrderMesogasrt opoda
 
hosts. This section provides a list of snails of
a.  Family Thiar idae  –   Thiara spp .
medicalimportance, including their taxonomic (intermediate host of  Paragonimus
classification, their biology, and ecology. The
westermani,  Metag
 Metagonimu
onimuss yokoga
yokogawai,
wai,
effect of parasites on snail intermediate host
and other heterophyid flukes
flukes in
 in the
is also given. Lastly, snail control in relation
Orient)
to the control and prevention program for
b.  Family Pleuroceridae –  Semisulcospira
schistosomiasis is discussed. 
spp. (intermediate host of  Parag
 Paragonimus
onimus
Taxonomy of Snails of Medical Importance   westermaniin the Orient) andGoniobasis 

Mollusks are divided into six classes, namely:  pl ici f er a  sil icul a (inter m ediat  host of
T r o g l ot r ema  sal mincol a  in th e  Pacific
the
oneClass
livingMonoplacophora
genus Neopilina, represented
 Neopilina by only
with a few species;  Northwest in the United States)
c.  Family Potamidae  –  Piron
 
 Pironella
ella conica,
conica
the Class Amphineura, the chitons; the Class Cerithidia cingulata , and  Pyrazus
Gastropoda, the most numerous, represented ebeninus (intermediate hosts of
 by snails and slugs; the Class Cephalopoda, the  Heterophyes
 Heterophyes heterophyes and hosts
heterophyes
squids, cuttlefish, the octopods, and the nautili; of cercariae causing schistosome
the Class Scaphopoda, the marine tooth or tusk dermatitis)
shells; and the Class Pelecypoda, the bivalves.  
 

CHAPTER 6: Arthropods and Mollusks of Medical Importance  313 

d.  FamilyPilidae – 
 –  Pila spp. (intermediate in the United States and Mexico)
host of  Paras
 Parastrongy
trongylus
lus cantonensisand
cantonensis and  Planorbariu
 Planorbariuss metidjensis
 Echinostoma ilocan um)
ilocanum (intermediate host of Schistosoma
e.  Family Synceridae  –   Syncera luteola haematobium in Portugal and
(intermediate host of  Paragonimus Morocco)
iloktsuenensisin rodents in China) iii.  Subfamily Segmentininae – 
Segmentininae –  
f.  Family Hydrobiidae  Segmentina spp . and Hippeutis
i.  Subfam ily Hydrobi inae – 
inae  –   spp. (both intermediate hosts of  
buskiand Echinosto
 Fasciolopsis buski  Echinostoma
ma
Oncomelania spp. (intermediate
ilocanum in the Orient)
host of Schistosoma japonicum )
iv.  SubfamilyBulininae – 
 –  Bulinusspp.
and Pomatiopsis lapidaria
lapidaria
(intermediate host of Schistosoma
(intermediate host of  Parag
 Paragonimus
onimus
haematobiumin Africa, Near East,
kellicoti)
Middle East) and  Indoplanorbis
ii.  Subfami ly Bulim inae (syn . exustus (intermediate host of
Bythiniinae) –  Paraf
 
 Parafossar ulusspp.
ossarulus
Schistosoma spindale, S. nasale in
and Bulimus spp. syn. Bythinia
India, Malaysia, and Sumatra)  
and Bithinia (intermediate hosts
c.  Family Ancylidae  –   Ferrissia
 Ferrissia tenuis
of Opisthorchis felineus, Clonorchis (intermediate host of Schistosoma
 sinensis,  Metag
 sinensis  Metagonimus
onimus yokog awai,
yokogawai
haematobium in India)
and Echinochasmus perfoliatus) 
d.  Family Phys idae –  idae –  Physa
 Physa sp p .  
B. Subclass Pulmonata   (ienvtoel ur m
r  diateinhotsht eof Or  E 
tuem iencht inaon sdt oma
1. Ord
deerBasommatophora
  schistosome cercariae producing
a.  Family Lymnae idae – 
idae  –   Lymnaea,
Lymnaea, dermatitis from freshwater and marine
 Fossaria ,  Pseudosuccinea ,  Radix , shoreline snails) 
Stagnicola (first  intermediate hosts of
2. OrderSy
t o
l mmao
t phora
 Fasciola
 Fascio la hep atica , Fascio
hepatica  Fasciola
la gig
gigantica,
antica  
several species of  Echinostoma , a.  Family Achatinidae –  Achatina
  Achatina fulica,
fulica
 Plagiorchis, and freshwater dermatitis- also known as giant African land snail
 producing schistosome cercariae)  (intermediate host of  Paras
 Parastrong
trongylus
ylus
cantonensis ) 
 b.  Family Planorbidae   b.  Family Helice llida e – 
e  –   Helicella
Helicella
i.  Subfam ily Plan orbi nae nae  –   candidula (intermediate host of
 Biomphalar
 Biomp ia spp. (intermediate
halaria de ndriticum in Europe
 Dicrocoelium dendriticum
host of Schistosoma mansoni in and Western
W estern Asia)
Africa and Near East and in c.  Family Cionellidae –  Cionella lubrica 
tropical America) andhost
sp p . (intermediate
Gyraulus
of
(intermediate
in the Unitedhost of D. dendriticum
States)
 Echinostoma ilocanum in the d.  Family Limacidae –  common
 common slugs
Orient)  Limax and  Deroceras (intermediate
ii.  Subfam ily Helis omati nae – 
nae –   hosts of lungworms of domestic
 Helisoma spp. (intermediate mammals and experimentally of
host of  Echinostoma revolutum
revolutum    Parastrongylus canto nensis) 
cantonensis
 

314   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

3. OrderSysteo
l 
l mmatophora status. Further and more distinct classification
 
of Oncomelania spp. will require advanced
a.  Family Veronicellidae
Veronicellidae –  several species genetic, morphological, and biochemical
in South
area, Pacific
Australia, andIslands, China
Cuba, and Sea
are hosts studies. Snail intermediate hosts of S. mansoni
and S. haematobium are also reported to
of Par
 Parast
astron
rongyl
gylus
us can
canton
tonensis; species in
ensis
 possess physiological
physiological differences
differences affecting host-
American tropical areas are hosts of  
 parasite relationshi
rel ationship.
p. Similarly,
Similar ly, the alpha
al pha race  
ngyluss costaricencis. 
 Parastrongylu
 Parastro and gamma race differ from one another in
The specific identity of gastropod morphology of the x-chromosome of  Neo
 Neotri
tricul
cula
a
intermediate host is important, especially aperta . 
in appreciating the susceptibility and non-   Efforts to clarify the taxonomy and
susceptibility of snail hosts and various aspects of  phylogeny
 phylog eny of the genus Schistosomaand its snail
host-parasite relationships.
relationships. Malek suggested that intermediate host, one of which is the genus
the only way to understand issues in taxonomic Oncomelania, continue. In the Philippines,
identification is to be aware that species vary in research on the proper classification of S.
space and time; hence, intraspecific variations  japonicum and O. quadrasi are sporadic and
as evidenced by discrepancies in susceptibility sketchy.
to infection is observed between certain local Distribution of Snail Intermediate Hosts 
races of snails and races of parasites.  
Snail identification based on shell features Snail intermediate hosts are found in
and soft parts has been fraught with problems,  almost all types of habitats. These range  
sainndceevthene sthellq vuaar lietys w
of itwhaatgeer ,inthaetqy p a biittaatt.,
uaetiocf hha b f lar or gme  lsam
keasll atnem  r iovr ear r sy.  p
d p Tohner 
des aar nedim r eoar mtasnto
st p
In addition to morphology, new approaches factors that influence
influence these
 these habitats, such as
to resolve issues in taxonomy and systematics the amount of sunlight that penetrates the
have involved cytological studies, biochemical
biochemical water, food availability, strength of the current,
studies, serological methods, and molecular nature of the substratum, ionic composition of
means. These studies have focused mainly on the water, extent of growth of aquatic weeds,
snail intermediate hosts of schistosomes found and the presence or absence of parasites and
in endemic countries in Asia, South America,  predator s. Ponds, pools, swamps, ditches, and
 predators.
and Africa. For the main Asian schistosome, the canals are usually shallow enough for the snails,
snail includes various species of Oncomelania.  and allow sunlight, favoring photosynthesis of
In the past, the amphibious snail  phytoplankton and plant organisms. Water
intermediate host of Schistosoma japonicum currents and other movements may aerate
was considered to be one species, Oncomelania water, but could also detach snails from their
hupensis , with six subspecies with separate anchorage.. Members of families Pleuroceridae
anchorage Pleuroceridae
geographic distribution. These ar
areeO.h. hupensis
hupens is and Thiaridae are able to hold up in swift,
sw ift, but
from mainland
O. h. chiui China; O.
from Taiwan; h. formosana and
O. h. nosophora from not torrential
the family water, better
Hydrobiidae. than members
Buliniids of
are stronger
Japan; O. h. quadrasi from the Philippines; than the biomphalariids when it comes to
and O. h. lindoensis from Sulawesi, Indonesia. withstanding water currents. Larger snails are
Results of biochemical, antigenic and genetic  better anchored compared to smaller snails,
studies suggest that O. hupensis, O. formosana,  while those snails with larger aperture are
O. nosophora, O. quadrasi, and O. lindoensis observed to fare better than those with smaller
should be elevated to independent species aperture.
 

CHAPTER 6: Arthropods and Mollusks of Medical Importance  315 

Temperature and altitude affect snail  protectio n from increased water velocities
 protection velocit ies and
habitats by changing the rate of photosynthesis
pho tosynthesis  predators,
 predator s, such as fish  and birds, and maintains
and the rate of decomposition, as well
w ell as the a suitable temperature and humidity. Aquatic
rate of reproduction of the resident snails. species die when they get trapped on dry land
Permanence and stability of the habitat are during the dry season. Amphibious species
critical factors affecting the presence of snails. like the oncomelanids can survive dessication
Water levels affect
affec t the balance in the ecosystem,
ecosyst em,   by burying themselves in mud while sealing 
 particularly those involving the producers, their apertures with their operculum.
o perculum. They
consumers, and reducers. Small- or medium- can withstand longer periods of drought
sized habitats are less stable than the bigger ones.  in the temperate zone than in the tropics.  
Snails naturally prefer to build large populations Oncomelanids are found both in and out of
in permanent habitats where they can reproduce the water in moist areas, such as poorly tilled
and establish more secure colonies. Snails that rice fields, sluggish streams, secondary and
find  themselves in non-permanent habitats take tertiary canals of irrigation systems, swamps,
swamps,
advantage of favorable periods by reproducing and roadside ditches.  
rapidly.
rapidly. They also resort to estivation to survive
Snail-Parasite Interaction 
adverse conditions of drought.
Aside from physico-chemical
physico-chem ical factors,there Host specificity
specificity is is noted to be very high
are biological factors that affect snail distribution in the choice of snail intermediate hosts by the
in a potential habitat. Aquatic vegetation can digenean parasites. Out there in the aquatic snail
serve as anchorage, and microflora provide  habitat, a schistosome miracidium can most  
soauyr  b
f tohoatd m cees. dBeatcr itm
er ia
enatanldtof unsngaiialsr .e p
 Pr aetdhaotgoer ns s emeniceatlr atdea potahteir ons  ppteociiets coof ms p
 bliikoeclyh p i ,  b
naaitls b leustnaitisl
such as insects, crabs, crayfishes, other snails, species will determine its fate in the tissues of
fishes, amphibians,  birds, and mammals can the snails. In a compatible snail species, the
feed on the snails. Lastly, snails are susceptible miracidium is able to develop with the slightest
to parasites like digenetic trematodes and of problems into the cercariae. There might be
nematodes. Snail distribution is usually patchy; slight or restricted encapsulation, which causes
therefore, habitats should be examined at little damage to the parasite. In other species
different sites. Seasonal variations also affect however, they are walled off and unable to
snail densities.  develop further as a result of the strong host
Aquatic snail hosts of schistosomes inhabit reaction brought about by the innate cellular
shallow water near the margins of lakes, ponds, defense mechanisms. These capsules that trap
marshes, streams, and irrigation canals. They are the parasites eventually result in the latter’s
found creeping on water plants and mud that destruction. 
is rich in decaying organic matter, or on rocks,   While the chemical basis for the death of
stones or hard objects covered with algae, or on the parasites in incompatible snail hosts remains
various typesplants
where water of debris. They
thrive, andabound in waters
where the water unclear, encapsulation
fibroblasts by leukocytes
 resulting in death and/or
is the simplest way
is moderately polluted with organic matter,   of explaining the most effective form of innate
such as feces and urine, as is often the case near resistance in mollusks against incompatible
human habitations.  trematode larvae. This shows that susceptibility
Vegetation is an important component of or resistance of snail to infection is a hereditary
the habitat since this provides not only a food character. 
source, but also substrates for oviposition and 
 

316   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Cross et al. proposed that the snail- consumed by the parasites. There is an overall
trematode compatibility is a highly specific reduction in proteins and free amino acids,
relationship often atthe population or strain level especially the methionine and heme-containing
for both participants. In the course of millions moiety of hemoglobin, which is eaten up by the
of years of selection and adaptation, the authors  parasites. Furthermore, there is an increase in
 proposedd that the vector-parasite
 propose vector-par asite compatibility
compatibil ity the activities of acid and alkaline phosphatases
has reached its optimum condition, particularly  resulting in increased intracellular activities, and 
 between the
th e local species
speci es of Oncomelania and in exchange of polysaccharides between host
the local strain of S. japonicum. and parasite. Significant reduction in glycogen
After the miracidium settles in a compatible reserve weakens the host tolerance to anaerobic
anaerobic 
snail host and starts the intramolluscan conditions.
development, the pressure effects manifest as The presence of parasites affects growth,
g rowth,
congestion of the blood sinuses due to migration fecundity, life span, heart rate, respiration, and
and maturation of the sporocysts. Other general thermal tolerance of the snail host. Growth
effects include toxic effects that may lead to rate is reduced among infected snails, especially
destructive changes in organs, particularly the among younger snails. Reduction in size and
digestive glands, starvation as nutrients are degeneration of the albumen gland result 
drained by the parasites, and tissue reaction in lowered egg production. Ohmae et al. in
 particularly noted as marked generalized 2003 reported that oogenesis was abnormal
 proliferative tissue reaction around dead and in infected snails, as shown by fewer eggs laid
trapped cercariae.  and poor hatching ability. Declining heart 
thoesht e p
glandThoer  m teadnocregasn, , shthoewds ir 
aff aetco p gaedstiicvael r matet  banodlicoxr yagte.nOu pthtear k p
e hyasvieolaongiecf af le cthaongtehs e
 ph
histopathological modifications such as include lowered maximum thermal tolerance
displacement of tubules and loss of branched limit and hemolymph osmolarity. Snails with
nature, erosion of the tubules’ epithelium, heavy infection have been shown to have higher
rise in the number of cytoplasmic vacuoles, mortality. In general, infected snails are less
overall destruction of gland epithelium and mobile and migrate more slowly.  
neighboring tissues, and significant reduction
Snail Control 
in the size of the glands.  
At the cellular level, marked changes Snail control is an integral component
are noted, such as: cristolysis and reduction in the control and prevention of digenean
in size and number of mitochondria; slight  parasites, especially
especially schistosomes. Elimination
Elimination
atrophy of the Golgi apparatus in the secretory of schistosomiasis through chemotherapy
cells of the epithelium and digestive glands; alone is difficult. Japan is credited with having
irregular outline of secretion granules; myelin   eliminated schistosomiasis in the absence of a  
figures and
figures  and electron dense material filling
filling  up well-accepted drug of choice (i.e., praziquante
praziquantel),
l),
vacuoles; and connective
more electron dense andtissue
filled,matrix becoming
accumulating mainly relying on measures
snail intermediate that targeted the
host with considerable
collagen-like fibers.  success. 
Marked alterations in the biochemistry Physical control by handpicking may
of the parasitized snails are shown by the  be suitable for large terrestrial snails, but in
decreased level of host glycogen and blood the early phase of schistosomiasis control,  
 proteins, including fluctuations in lipid the Japanese government resorted to massive
content suggesting that food reserves are being   collection of O. nosophora by residents in
 

CHAPTER 6: Arthropods and Mollusks of Medical Importance  317 

endemic areas, providing various incentives to Ecological control focuses on the alteration
 promote this campaign. This method may be of snail habitats to reduce survival of the snails
hard to implement in the Philippines because of and to slow down or prevent their breeding.
the extreme difficulty in locating and collecting This includes radical modification of the
the local species of snail intermediate host, environment to destroy snail habitats and their
which are usually found underneath leaf litter residents. It may be as extreme as removal
and mud. of water by drainage, and proper water  
Chemical control using molluscicides management in irrigation systems that may
can wipe out huge populations of snails and involve stream channelization,
channelization, seepagecontrol,
should be done using appropriate strategies.  and construction of diversion and intercepting
i ntercepting 
Chemical molluscicides include potassium channels. This can be very expensive and will
aluminum sulfate, calcium arsenate, NaPCP require participation of the local irrigation
(sodium pentachlorophenate), Yuramin   agency. 
(3,5-dibromo-4-hydroxy-4-nitroazobenzene), B- Removal of shade or shelter from the sun
2 (sodium 2,5-dicholoro-4-brompophenol),  by clearing of vegetation exposes the snails
and niclosamide (2’,5-dichloro-4-
(2’,5 -dichloro-4- with deleterious effects. Although this method
nitrosalicylanilide). Niclosamide has been  produces favorable
f avorable results,
r esults, sustainabil
sus tainability
ity is 
 proven to be the most versatile and most a major problem since this has to be done
effective of these synthetic molluscicides, and regularly and is labor-intensive. Cementing
has become the molluscicide of choice. In recent linings of irrigation canals or making them
years, however, the use of niclosamide has been   more perpendicular prevents snails from 
r eeff setr citctoend tf hoelloewnvinir gonclmaiemnts aonf  ditsnodne-letater gr ieotus  banr ededir ir nigaotinonthcea b s  hoir s m
nalns.kT war sgoi nse  of  sJta p
r eam
’ns
organisms. Plant derivatives have been shown ways of controlling O. nosophora, and to date,
to have molluscicidal properties. Endod fruits this is seen also as evidence of better agricultural
( Phytolacca dodecandra
dode candra ) are used in Africa management.  
to kill snail intermediate hosts of S. mansoni Velocity of water can be accelerated to
and S. haematobium . In the Philippines, dislodge snails by proper grading and cleaning
Croton tiglium ,  Jatropha curcas , and Entada of the stream bed and removal of debris. If the
 phaseoloides have been proven to have promising area cannot be drained, the depth of the water
molluscicidal efficacies.  may be increased rendering it uninhabitable
When resources are limited and snail to snails. Snail habitats may be simply covered
colonies are confined to limited areas,   with landfill. 
focal mollusciciding is effective. Area-wide  success in eliminating snails in
Japan’s success
Japan’s
mollusciciding is recommended in endemic Kurume can be attributed to conversion of the
areas where transmission is spread over a   marshy lands into extensive golf courses and 
watershed or an irrigation system. Repeated orchards. Constant monitoring and surveillance
applications
must of molluscicides
be accompanied are needed
by vegetation and
clearing of the
to once
yield O.endemic area
nosophora .  has consistently failed
to make sure that repopulation of snails is   Ecological control methods can be
 prevented. The
The use of chemical
chemical molluscicide
molluscicide has incorporated
incorporated into agricultural programs. Results
 been banned in the Philippines in compliance can be permanent if adequately maintained, as
with a widespread campaign because of its shown by the experience in Kurume, Japan.
harmful effects on non-target organisms and Increased agricultural productivity is assured.
accumulation in the environment.   The activities can be locally initiated and do  
 

318   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

not require foreign exchange, unlike the use of The successful elimination of schistosomiasis in
chemical molluscicides.  Japann emphasizes the fact that there can be snails
Japa
Corollary to ecological control is proper rice even without the disease, and that the snails
cultivation, which brings about environmental can be eliminated by radical transformation
changes and increased productivity. With   of the environment resulting in widespread
rice fields serving as important snail habitats, destruction of the snail habitats. Molluscicides,
measures such as deep plowing that turns over   may result in large scale mortality of snails but 
the soil and buries the snails, harrowing that may not be enough to kill them all. Altering
removes the weeds which provide cover, spacing the environment to make it uninhabitable to
that exposes them to sunlight, and weeding   snails is effective, but the cost and effect on the 
that removes vegetation, are surefire ways of environment are still uncertain.  
destroying the snails. Pesticides used by farmers
References 
may even be molluscicidal. The stoppage of
flow of
flow  of irrigation water between harvesting Bao-Zhen Q, Thomas K, Bogh HE. Allozyme
and planting can certainly interrupt breeding. variation among six populations of the
Drainage makes sure that waterlogged areas are freshwater snail Oncomelania hupensis in
 prevented from
f rom becoming
beco ming transmissio
tr ansmissionn sites. Zhejiang, China. Southeast Asian J Trop
There have been efforts in some endemic areas Med Public Health . 1996;27(2):400-5. 
in the Philippines to coordinate snail control Cross JH, Lo CT. Susceptibility of new
with the local agriculture agency, especially Taiwan foci of Oncomelania hupensis to
where farming methods and irrigation are   geogr a phic str ai ains of S 
 s  s
 poonicum. 
S chi t o oma  jja p
involIvnedev.aluating the effectiveness of the snail S1o9u8t0h;1ea1s:t3A74si-a7n. J Tr o p
 p  Med Pu blic Health.
control program, certain parameters should Dewitt WB. Susceptibility of snail vectors to  
 be measured, such as reduction in size of area geographic strains of Schistosoma
Schistosoma japonicum. 
japonicum. 
inhabited by snail population, reduction in snail J Parasitol. 1954;40:453-6. 
density, change in population structure, and Hsu SYL, Hsu HF
HF.. Infectivity
Infectivity of the Philippine
mortality or percentage of dead snails as a result strain of Schistosoma japonicum in
of mollusciciding. Monitoring should include Oncomelania hupensis, O. formosana and 
regular checks of snail density and population O. nosophora. J Parasitol. 1960;46:793-6.
structure.  Ishi A. Successful parasite controls in Japan: 
The Future of Snail Control  
eradication of schistosomiasis. Asian
Parasitol. 2005;5:184-276. 
Experience in many endemic countries Iwanaga Y, Santos MJ, Blas BL. The
shows that snail control is an integral part in determination of the Oncomelania hupensis
any program to eliminate snail-borne parasitic quadrasi population density using the
diseases, foremost of which is schistosomiasis.  banana leaf method in four municipalities
municipali ties
Since the discovery
 programs of praziquantel,
have focused control
mainly on control of of Eastern
Med Leyte, Philippines.
Sci. 1977;26:19-27.   Hiroshima J
morbidity by chemotherapy. Japan eliminated Leonardo L, de Lara A, Regadio A, Estores M,
schistosomiasis even before the advent of Vicente IM, Victoria MV. Molluscicidal
 praziquant el primarily through
 praziquantel throug h snail control. To
To activities of four botanical extracts against
date, O. nosophora still thrives in rice fields and Oncomelania hupensis quadrasi , snail
other habitats in the Kofu Basin but has been intermediate host of Schistosoma
Schistosoma japonicum.
eradicated in Kurume
K urume along the Chikugo
Chikugo River.   Acta Med Philipp. 2007;41(2):37-44.  
 

CHAPTER 6: Arthropods and Mollusks of Medical Importance  319 

Malek EA. Snail-transmitted parasitic diseases. Sturrock RF. Current concepts

con cepts of snail control.
 New Orleans: University Book Publishing Mem Int Oswaldo Cruz. Rio de Janeiro.
Company; 1980.  1995;90(2):241 – 8 8..
Minai M, Hosaka Y, Ohta N. Historical view Takahiro T, Hirai H, Upatham S, Agatsuma  
of schistosomiasis japonica in Japan: T. Sex chromosome differences among
implementation and evaluation of disease the three races (alpha, beta, gamma) of
control strategies in Yamanashi prefecture.  the snail intermediate host of Schistosoma 
Parasitol Int. 2003;52:321 – 6.
6. mekongi, Neotricula aperta. Parasitol Int.
 Nihei N, Kanazawa T, Blas BL,
B L, Saitoh Y,   2000;49:267 – 72.
72.
Itagaki H, Pangilinan R, et al. Soil factors Tanaka H, Santos MJ, Matsuda H, Yasuraoka
influencing the distribution of Oncomelania
Oncomelania K, Santos AT Jr. A quantitative sampling
quadrasi , the intermediate host of method for Oncomelania quadrasi by
 by filter
fil ter
Schistosoma japonicum, on Bohol Island,  paper.
 paper. Jpn J Exp Med. 1975;45:255 – 6
62.
2. 
Philippines. AnnTropMed Parasitol
Parasitol. 1998;  Woodruff DS, Staub KC, Upatham S,
92(6):699 – 710.
710. Viyanani V, Yuan HC. Genetic variation
Ohmae H, Iwanaga Y, Nara T, Matsuda H, in Oncomelania hupensis: Schistosoma
Yasuraoka K. Biological characteristics  japonicum transmitting snails in China
and control of intermediate snail host and the Philippines are distinct species.
of Schistosoma japonicum. Parasitol Int. Malacologia. 1988;29(2):347 – 61. 61.
2003;52:409 – 17.
17. Woodruff DS, Carpenter MP, Upatham S,
Sobhon P, Upatham S. Snail hosts, life cycle  Viyanant V. Molecular phylogeography  
al NstDr uPc/tW
ur eosr lodf BO Oncomel ania l ind oen i (G str o poda:
ascnhdisteogsoumesn.tU anr ike/nW
taH
l  O; oPf om  s  s
atio psidae),  the inter mediate host of
1990. Schistosoma japonicum in Sulawesi. J Mol
Studies. 1999;65:21 – 31.
31.
 

320   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

CHAPTER 7 

Diagnostic Parasitology 

ExaminatioWnino f  dSatoUo. lda
r e
if r  e n
Ledo nBo dy Fluids 

Laboratory Diagnosis  cysts, oocysts, trophozoites, and antigen) or

 by the detection of host immune response
ost parasitic diseases cannot be established
M   based on clinical
clinical signs and symptoms  
alone. Confirmation of a suspected parasitic
to the parasites (e.g., antibodies). It must be
emphasized that demonstration of the parasite 
and/or the parasitic antigen provides a definitive
condition generally depends on the result
diagnosis, while detection of the humoral
of proper laboratory examination. Correct  
immune response provides only presumptive
diagnosis can likewise provide prompt treatment evidence of infection. 
thus preventing possible complications that may
arise. Correct diagnosis of parasitic infections   during the patent stage
Demonstration
Demonstratio of the infection.
n of parasites There
is possible only 
cinancidaelsnoce ptr hoavtidar ee aicc
m puor ar tean ptr ienvathlenscuer vaenidllance are cases where the parasite is not demonstrable
even in active infection, as in schistosomiasis. 
and monitoring of diseases. A parasitology
In light infections and when parasites are still
laboratory should be able to: 
immature, recovery of parasites from infected
•  con rm a clinical
clinical impre
impression
ssion that the individuals may not beb e possible. In such cases,
condition has a parasitic nature;   immunoassays may become useful.  
•  rule out differential diagnoses; Among the specimens available for parasitic
•  aid a clinician in the choice
choi ce of proper
proper   examinations, the stool is most commonly
medication; and utilized. Other specimens like urine, blood,
•  help in monitoring the effect
effect of a sputum, cerebrospinal fluid, tissue aspirate,
treatment regimen. tissue biopsies, and orifice swabs are also used
for diagnosis. Fresh specimens in sufficient
The ability of a parasitology laboratory to amounts are valuable in most instances.  
generate reliable results is dependent on the The proper procedure can be determined if  
 proper collection, handling, and processing of
specimens prior to examination, the skill of the  bthioeldoia iaanr ahsaitsea.  b
gygonf otshtiec p Thaseiclif kencoywcle dwgiell ohf el p
thein
laboratory analyst
of equipment used(examiner), and the quality
in the examination.   deciding which specimen to be collected, as well
as the frequency and timing of collection. The
Diagnosis of parasitic infections is done  parasite species and stage of development
develop ment in the
either by the demonstration of parasite or life cycle are also important factors to consider.  
 parasite components
compone nts (e.g., adults, eggs, larvae,  

320 
 

CHAPTER 7: Diagnostic Parasitology   321 

Examination of Stool or Fecal Sample  C.  Amount of stool to be collect ed is

dictated by the techniques that will
The most common method of diagnosis of  be used. A routine
routin e stool examination
intestinal parasites
of eggs, larvae, is through
adults, the demonstration
trophozoites, cysts, or
usually requires a thumb-sized
specimen of formed stool or about 5
oocysts in the stool. Techniques are available to 6 tablespoons of watery stool.  
where recovery of both helminthic and
D.  Contaminationwith toiletwater, urine,
 pr otoTzhoeanf  p
ecar las p
siteecsim  enosissi b
is p   b
bles. t  collected  in or soil must be prevented since these
clean, wide-mouthed containers made of waxed can destroy protozoan trophozoites. In
addition, soil and water may contain  
cardboard or plastic with a tight-fitting
tight-fitting lid
 lid to
free-living organisms that would
ensure retention of moisture and to prevent
complicate diagnosis of infections.
i nfections. 
accidental spillage. 
E.  Age of the stool sample is very
The stool specimen should be submitted important for diarrheic specimens
with the following information:  
since the trophozoites it may contain
1.   patient’s name  
 patient’s are likely to die within 30 minutes to
2.  age  1 hour after passage. Therefore, stools
3.  sex  must be examined within that period
4.  date/time of collection  of time.
5.  requesting physician  F.  Delay in examination of specimens
6.  requested procedure  may require preservation to ensure that  
7 
8. es in pf etcivtieodnisagnosis 
 pr iour  m star gaes.ites ar e  p
 p pr esent in the identifia ble 
9.  travel history  G.  Temporary storage of fecal samples in
a refrigerator (3-5°C) is acceptable,
For stool materials to be useful in parasitic  but prolonged refrigeration can bring
diagnosis, there are important factors to about desiccation. Trophozoites are
consider:  killed by refrigeration, although
A.  Intake of drugs/medicinal substances   helminth eggs and protozoan cysts are
usually not damaged. 
1.  antacids   NEVER FREEZE STOOL
2.  anti-diarrheals  SAMPLES. NEVER KEEP THEM
3.   barium IN INCUBATORS.
4.   bismuth
Stool Preservatives 
5.  laxatives 
Appropriate fixation of parasites in the
t he stool
cr ystAalllinoef   tr heesside uder sutghs ahtacvaen beinentef r of eur nedwtiothleathve will preserve protozoan morphological
morphological features
identification of parasites. Stool samples should and
eggsprevent possible
and larvae. destruction
Several of helminth
stool preservatives are
 be collected a week after the last intake of any
of these drugs.  available, but only the more common ones will
 be discussed here. When
When selecting a fixative, the
B.  Intake of antibiotics usually decreases  possibility
 possibil ity of preparing
preparin g a permanently
permanen tly stained
the number of protozoans for several slide should be considered. Stool samples
weeks.  must be adequately mixed with the selected  
 

322   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 preservative in a proportion of one part stool stools can be examined through the
to three parts preservative. Any of the following wet mount, but difficulty in the
stool preservatives can be used:   specific identification of protozoans
may be encountered. The Lugol’s
1.  Formalin is an all purpose fixative. A iodine component should always be
5% concentration is recommended freshly prepared since it is unstable.
for protozoan cysts, while a 10%  Staining of preserved stools in MIF  
concentr ation  is r eco lar evnadee. dThe
f or  helminth eggs andmm
yields unsatisfactory results.  
5.  Sodium acetate-acetic acid formalin
solution may be buffered with
(SAF) has the advantage of not
sodium phosphate to preserve the
containing mercuric chloride. Images
morphological characteristics of the of organisms fixed in SAF,however, are
organisms. Preserved stool can be
not as sharp after staining compared
comp ared
concentrated using formalin-ether/ with those fixed in PVA or Schaudinn’s
ethyl acetate concentration technique solution. It is a liquid fixative
fixative with
 with a
(FECT).  long shelf-life. 
2.  Schaudinn’s solution is used to
 preserve fresh stool in preparation
preparati on for Methods of Examination 
staining the stool smears. It contains
contains Stool samples are submitted to the
mercuric chloride which is highly
laboratory in the fresh state or as preserved
toxic to humans.
disposal Problemsarise.
may therefore of mercury
  samples. If stools are fresh, the laboratory can 
3.  Polyvinyl alcohol (PVA) is a plastic staotoelr sya. sTf ohr emed,
heedco, nssoif st,enlocyosoef , tohr e w
cselamssii-f f yor tm
resin which serves to adhere a stool
stoo l consistency can give an indication of the stage of
sample onto a slide. It is normally the organism that may be present in the sample.
incorporated into the Schaudinn’s Protozoan trophozoites are generally observed
solution, therefore the actual fixation in soft or liquid stool, while the cysts are often
is done by the Schaudinn’s.
Schaudinn’s.  The main found in formed or semi-formed samples. 
advantage of using PVA is related to On the other hand, helminth eggs and
the preservation of protozoan cysts and larvae can be found inany type of consistency. In
trophozoites for permanent staining. watery samples, there may be a reduction in the
Stools preserved in PVA can be
number of eggs and larvae due to the dilution
concentrated using FECT and can be
factor. Some authorities recommend the use
shipped to any laboratory for further
of purged stools to increase the chances of
examination. One major drawback of recovering the protozoan trophozoites. Purged
PVA is the use of mercuric chloride.  
samples should be examined immediately after
Ssuogmgestlea bdor r ea ptolar cyintgechthnios locgoimts ohuanvde
s p collection.
with cupric sulfate.  The color of the stool can be indicative of  
4.  Merthiolate -iodine-formalin (MIF)
the presence of the parasite. Presence of blood
contains merthiolate (also called
should always be reported. Dark-colored blood
thimerosal) and iodine which act as
suggests bleeding high up in the gastrointestinal
tract, while bright red blood means bleeding
staining components, while formalin from a more distal location. Blood and mucus
acts as the preservative. It is useful for in soft or watery stools may possibly yield the
the fixation of intestinal protozoans,
 presence of trophozoites. Ingestion of some  
helminth eggs, and larvae. Preserved  
 

CHAPTER 7: Diagnostic Parasitology   323 

compounds may impart a characteristic color 8.  Elements o f plant srcin which
to the stool (e.g., black color with iron intake).  resemble some parasites include:  
By gross examination of the stools,
tapeworm proglottids or adult nematodes a.    plant cells/fibers 
like Ascaris or Enterobius may be found on or  b.  pollen grains 
 beneath the surface of the sample.  c.  starch granules 
d.  vegetable spirals 
 A. Microscopic Examination 
Examination  9.  Plant and animal hairs may look like
Microscopic examination can reveal many helminth larvae. 
elements present in the intestinal tract aside
Techniques 
from parasites and normal fecal constituents.
It is therefore highly recommended that a  A. Direct Fecal Smear (DFS)  
 parasitology
 parasitol ogy diagnostici
diag nostician
an be able to
t o identify
 parasites apart from artifacts.  About 2 mg of stool (amount forming a
The following are elements that may low cone at the tip of an applicator stick) is
 be found in stool specimens in addition to comminuted thoroughly with a drop of 0.85%
 parasites:  sodium chloride solution (NSS) and then
covered with a cover slip.  
1.  White blood cells:  This is a routine method of stool
examination primarily useful in the
th e detection
a.  Polymorphonuclears (PMNs),
which may indicate inflammation
inflammation   of motileon,protozoan
 preparati
 preparation, trophozoites.
the trophozoites
tropho zoites In this
appear very pale
 b.  Eosinophils, which may indicate  and transparent. Trophozoites can be stained
an immune response to a parasitic to demonstrate the nuclear morphology using
infection 
r’ss buffered methy
 Nair’
 Nai methylene
lene blue (BMB) solution.
solution.
2.  Red blood cells, which may indicate  Entamoeba
 Entam oeba cytoplasm will stain pale blue and
ulcerations or bleeding   the nucleus, darker blue.
3.  Macrophages are usually present in Protozoan cysts can also be seen in a DFS.
 both bacterial
bacterial and parasitic infections.
infections. A weak iodine solution (Lugol’s
(Lugol’s solution
 solution or
In actual practice, one can mistake D’Antoni)  can be used as a temporary stain
D’Antoni) can
the active macrophages for amebic to demonstrate nuclei. Alternatively, a new
trophozoites.  mount can be prepared with iodine alone. The
4.  Charcot-Leyden crystals are released cytoplasm will stain golden yellow, the nucleus
with the disintegration of eosinophils. will be pale and refractile, and the glycogen will
They may indicate presence of  be deep brown. Helminth eggs and larvae can
hypersensitivity or parasitic infections, 
hypersensitivity also be detected using this preparation. Because 
especially amebiasis.   the amount of stool used in DFS is very small,
light infections may not be detected. 
5.  can
Epithelial
also becells from the intestinal
recovered.   tract   Micrometry, as a tool to measure cysts
6.  Eggs of arthropods, plant nematodes, and ova, will be useful in specific species
and other spurious parasites may be identification. 
mistaken for human parasites. B. Kato Thick Smear  
7.  Fungal spores coming from Candida
spp., yeast, and yeast-like fungi may About 50 to 60 mg of stool (approximately
also be mistaken for parasites.  the size of two mung beans)is placed over a glass  
 

324   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

slide and covered with cut cellophane paper of Trichuris , Capillaria, and trematode eggs,
soaked in a mixture of glycerine and malachite especially Schistosoma. This is also the choice if
green solution. Glycerine is a clearing solution stool material comes from animals like cats and
and malachite green is used to give color to dogs. Drawbacks in the use of this technique
the cellophane in order to give a pale green include: loss of parasite to the plug of debris and
 background to the eggs aandnd to minimize the  possible destruction of protozoan cysts. 
 brightness of the microscopic
microscopic field. If malachite 
green is not available, green cellophane soaked b. For malin-Ether /Ethyl  A
Technique (FECT)
Ac etate Conc ent r ation
ntr 
in glycerine
glycerin e may be used. The
T he preparation
preparat ion is bets
bets
examined within 10 to 20 minutes. This procedure makes use of 10% formalin
The technique is simple and economical, which is an all purpose fixative, and ether, which
and is therefore useful in mass stool examinations. can dissolve neutral fats in the stool. This is
It is very good in detecting eggs with thick shells useful in the recovery of both helminth eggs and
(e.g.,  Ascaris and Trichuris) but not eggs with  protozoan cysts. FECT can also be done with
thin shells (e.g., hookworm). In many instances, formalin-preserved and PVA-preserved stools.
if the preparation is kept too long before More parasites can be recovered from formalin-
examination, hookworm eggs become too  preserved samples. Parasite morphology is also
transparent or distorted, makingidentification
making identification  better preserved in formalin than in PVA.
very difficult. Usefulness is limited if stools are Sediments from FECT can be stored for a long
diarrheic or watery. Likewise, it is not able to  period of time. 
detect protozoan cysts and trophozoites.  The use of ether has been a cause for  
C. Concentration Techniques
Techniques   corr  on bce
 p cle    sininthsteor la bgeor antodr yhasnecdtloinr g boeecf fc atuhsies  of
leerr m
n
Concentration techniques can separate explosive and flammable compound. In
 protozoan cysts and helminth eggs from a  place of ether, ethyl acetate may be used in in
larger amount of stool (usually 1 g in amount) sedimentation procedures. Those who have
 based on differences in specific gravity. In tried ethyl acetate claim that it is more efficient
cases of light infections, or if there is a need than ether in the recovery of cestode eggs and
to recover more parasites, stool concentration Giardia cysts. However, ethyl acetate is not
 proceduress are recommended.
 procedure recommended. These procedures
procedures as efficient  as ether in the extraction of fat or
efficient as
are based either on sedimentation or flotation. mucoidal material from the stool.  
In sedimentation techniques, a parasite that 2. Fo
l a
t to
i 
i nProcedures
has a higher specific  gravity than the reagent
specific gravity  
a. Zinc Sulfate (ZnSO4 ) Flotation
will sink to the bottom of the preparation,
while a parasite with a lower specific  gravity
specific gravity The main reagent is a 33% zinc sulfate  
will float to the surface. Mounts prepared from 
flotation techniques are cleaner than those from enck. eBde.f oTr he eusied,etahlesspeciific gravity  sr hanouggeleds
 bsoelucthioec
sedimentation. from 1.18 to 1.20. If parasites are exposed to
1. Sed m
i ena
t tii 
o nProcedures high specific gravity, distortion and shrinkage
  of protozoan cysts and thin-walled
thin -walled nematode
a.  Ac id Ether  Concentr 
ntr ation Tec hnique (  A
AECT)  eggs may
m ay occur. 
The main reagents are 40% HCl, which b. Brine Flotation
can dissolve albuminous material, and ether,
which can dissolve neutral fats in the stool. This This makes use of a saturated table salt
technique is recommended for the recovery  solution. Stools are directly mixed with the brine 
 

CHAPTER 7: Diagnostic Parasitology   325 

solution. There is no need for centrifugation environmental conditions in nature. Larvae

since helminth eggs rise to the surface of are harvested using the Baermann procedure.  
the solution. This technique is low-cost and
simple but helminth eggs like hookworm and 2. Harada-Mori
Method 
or the Test Tube Cutl ure
Schistosoma become badly shrunken. This is
not useful for operculated eggs like Clonorchis, This technique makes use of test tubes
Opistorchis, and heterophyids because these do  and filter  paper strips. Positive stool is applied 
not float in brine solution. 
solution.   to the filter  paper
 paper and placed into a test tube
with about 7 mL of boiled or distilled water. 
c. Sheather’s Sugar  Flotation
 Flotation
Filariform larvae will generallymove
generallymove downwards
Boiled sugar solution preserved with against the upward capillary movement of water
 phenol is used in this method. This technique
techniq ue is and can therefore be recovered from the water
considered the best for the recovery of coccidian at the bottom of the tube. On the other hand,
oocysts, mainlyCryptosporidium, Cyclospora, and Strongyloides larvae may instead move upwards
Cystoisospora. Withthis procedure, visualization and accumulate at the upper end of the filter
of oocysts can be better appreciated through the  paper strip.
use of a phase microscope. Filariform larvae are infective and caution
must be observed in handling stool cultures.
D. Stool Culture Methods 
Methods 
Stools for culture should not be refrigerated
Ova of all hookworm species are similar,  because some specie
speciess fail to develop when
and speciation is therefore impossible to make   exposed to cold temperature. 
on.anLdar vS at lr odni g f  yf el r oeind teiataiot nthe
ciees nidheonotikfiwcaotr im
 bs peetw  s cultiC thediinateasr teinalls p
vautilotunr oe f m o r aovtaoizlao banle; hf  or wtehver
rhabditiform stage is possible but difficult. very few laboratories offer this service. Intestinal
At the filariform stage, however, sp ecies  protozoanss have been successfully
 protozoan successfully cultivated cultivated in
be  done. 
identification can be done. the laboratory but these culture methods are
Stools positive for hookworm ova and/or not recommended as substitutes for routine
Strongyloidesrhabditiform larvae can be cultured microscopic examination. 
until filariform larvae develop. This technique E. Egg Counting Procedures  
can also be used for Trichostrongylus sp. 
Egg counting procedures may help correlate
1. CoproCu lture
  the severity of clinical disease with the intensity
Positive stools are mixed with moistened of infection or worm burden (Table 7.1). It is
soil or granulated charcoal. This simulates   also done to assess the efficacy of anthelminthics  

Table 7.1. WHO classification

classification ofand
intensity
Schistosomaspp.
Schistosoma
of infections
spp. with soil-transmitted helminths

Organism  Lightintensity Moderateintensity  Heavyintensity

 Ascaris lumbricoides
lumbricoides  1 – 4,999 epg  5,000 – 49,999 epg  ≥ 50,000 epg 
epg 

Tr ichur iis
str ichiur a  1 –999epg
999epg   1,000 –9,999epg
9,999epg   ≥ 10,000 epg 
epg 
Hookworm   1 –1,999epg
1,999epg   2,000 –3,999epg
3,999epg   ≥ 4,000 epg 
epg 

Schistosomamansoni
 

326   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

and the reduction of worm burden following constant, there may be a need for a correction
treatment. factor in computing for the egg count taking
into consideration stool consistency. 
1. Kao
t -KatzMeh
t odor theCelophaneCoveredThci kSmear 
F. Staining of Stool Specimen 
Specimen  
This procedure uses a measured amount of
stool which has b
 been sieved thr ough a wir e mehs  Staining of stoolspecimen can also be done
and pressed under cellophane paper soaked in specifically in the examination of the  nuclear  
glycerine-malachite
glycerine-m alachite green solution. A uniform  characteristics of amebae. These are also useful
useful
amount of stool is examined through the
th e use in the identification of the other intestinal
of a template with a uniform-sized hole in the  protozoans like  Balantidium and Giardia . 
middle. All eggs seen in the whole preparation Techniques available include:  
are counted. The total egg count is multiplied
with a factor depending on the amount of 1.  Iron-Hematoxylin
stool used.  2.  Trichome
The procedure is useful for
f or assessing the 3.  Periodic Acid Schiff (PAS)  
intensity of infection with Schistosoma and 4.  Chlorazol Black E 
common soil-transmitted helminths like Ascariss,
 Ascari The abovementioned techniques are not
Trichuris, and hookworm.   very useful for the identification of coccidian
Consistency of the stool is the main oocysts like Cryptosporidium, Cyclospora, and
determinant for the sensitivity of this technique,  Cystoisospora . For these parasites, Kinyoun’s
method of acid-fast staining is
i s recommended. 
meolli-sf toor 
stihnacne  w r m eicehldnihqiugehecr aenggocnolyu  b
nesd.  sTtohoelstyec nbtes
done on fresh formed stools and not on liquid Acid-fast staining of stool specimen
requires spreading a thin layer of stool on a  
and preserved samples.   glass slide. The oocysts of the three coccidian
For the identification of Schistosoma ova,  parasites stain pink to red with a blue or green
1% eosin solution can be layered over the  backgrou nd. The background
 background. backgroun d actually depends
cellophane paper. This
This method can help in the on the counter stain used. For Cryptosporidium
visualization of the miracidium.   and Cyclospora, oocysts are spherical, although
2. Stoll 
E
  ggCount  Cryptosporidium has a diameter of 4 to 6 µm,
  while Cyclospora are 8 to 10 µm in diameter. On
This technique makes use of 0.1 N NaOH the other hand, Cystoisospora oocysts are more
and a stool displacement flask  calibrated at 56 ovoid than spherical.
mL and 60 mL. The sodium hydroxide
h ydroxide acts as a Generally, these organisms are recovered
stool diluent. It saponifies fat and frees eggs from  better from diarrheic and watery samples. 
fecal debris. The amount of diluted stool used 
Perianal Swab 
for egg counting is measured by Stoll pipettes
calibrated at 0.075 mL and 0.15 mL. The   The perianal swab can be used to recover
constant used
depends on thetoamount
multiply
ofthe total
stool egg count
examined.   eggs of Enterobius vermicularis and Taeniaspp.
The Enterobius gravid female migrates out
Like the Kato-Katz method, sensitivity   through the anus at night time, and deposits
is determined by the consistency of the stool eggs on the perianal skin. Taenia spp. gravid
since formed stool can displace more sodium segments can crawl out of the anus
anu s and in the
hydroxide than liquid stool. Aside from the    process, ova are squeezed out of the segment and
are deposited on the perianal skin.
 

CHAPTER 7: Diagnostic Parasitology   327 

 A. C ellulo se T ape or S cotc h Ta pe Meth od   an area which is about 2 cm in diameter.
Films are then thoroughly dried and then
This is done by sampling the perianal skin dehemoglobinized prior to staining. 
using a strip of cellulose tape attached onto b. i smearsare prepared in such a way that
Thn
a glass slide. The sticky side is applied to the
they are thick at one end, and thin and
skin. The specimen can be collected early in feathery at the other end. Streaks and
the morning before the patient has taken a bath  holes should be avoided in the film. Clean  

oPr o bsietf ivoer er tehsue p thteai pner dinf er uom.
ltsathieanvte  haalsow basehenedo b
slides and spreaders are used. After air-
drying, slides are fixed with m ethanol before
swabs collected late at night when patients have staining.
already slept for several hours.   Thick smears are used in the demonstration
Collected specimens are then examined of microfilariae and rapid diagnosis of malarial
under the microscope for the presence of eggs infection. Thin smears are mostusefulin species
or the adult Enterobius. In some laboratories, a
 Enterobius identification of malarial 
malarial  parasites. 
drop of toluene or xylene solution helps in the Stains that are usually used for blood
visualization of eggs.    parasites include:
includ e: Giemsa stain, Wright’s stain,
Repeat examinations are recommended if and Delafield hematoxylin 
hematoxylin  stain. 
results are negative.   •  Giemsa stain may be prepared from
Examination of Blood   powder or may be commercially
 purchased as concentrated stock
Several species of helminthic parasites solution. With this stain, red cells
(e.g., filariae) and protozoan parasites (e.g.,
(e.g.,   stain pale red, white cell nuclei stain
 Plasmodium , trypanosomes, and  Babesia) are   purple, eosinophils
eosinop hils stain bright purple  
in the blood at some stage of their life cycle. red, and neutrophils stain deep pink
There are several techniques utilized for blood  purple.
 preparation
 preparati on and examination.
examination . Glass slides for •   Wrig ht’s stain already contains
 blood examination
exa mination must be absolutely
ab solutely clean alcohol, so fixation is not needed
and grease-free.   before staining. Stained smears
Methods  show light red erythrocytes, bright
 blue nuclei of leukocytes, bright
 A.  Finger-prick blood sample must be free- red eosinophilic granules, and pink
flowing to prevent dilution of blood with
neutrophilic granules. 
tissue fluid, which decreases the number
of parasites. 
•  Delafield hematoxylin stain is
mainly useful in demonstrating the
 
1. Wet/fres
eshPrepara
at 
i 
o
t n detailed structures of microfilariae.
microfilariae.  

and  M icr ofilar ia and tr y pomastigotes ar e lar ge

motile in f r esh  blood  pr e par ations. Their
Inehtehm
d gloe bthinodiz,edthinck 2f %
isom r ealin
ilmf sor am
 presence in the sample can therefore be easily with 1% acetic acid. The main stain
detected. Species identification, however, is not is a mixture of hematoxylin and
 possible with the wet mount.  ammonium alum which enhances
nuclear detail and morphological
2. Sta inedSmears features. Another advantage of this
 
a. Thickfilmsareprepa
prepared
red from two to three small
sma ll method is that stained smears could
drops of blood which are mixed and  be permanently
permanen tly mounted
moun ted with Canada
spread with continuous
continuous movement over    balsam or permount.  
 

328   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

3. Capa
l 
i ryTubeMethod  2. MembraneFtl 
i ra to
in
   
Finger-prick blood sample is collected Like Knott’s concentration, this method is
using
sealedaat
heparinized capillary
one end and tube. The tube
then centrifuged. is
After also veryThis
is low. useful when themakes
technique densityuse microfilariae
of of a syringe
centrifugation, there will be three layers. At attached to a Swinney filter  holder.
 holder. One mL
the bottom is the red cell layer, followed by the  of fresh or anticoagulated blood is drawn up  
w ayae.r M
is htihte  pcellalslm cailcler dofithlaer  b , aand  osonmto p
iauef af yndcotar ty p es inagter a. nTdhleyzleydze bdy balododinigs 1th0enmL
ionf todistthiellesdyr w
can be readily visualized at the buffy coat area  passed through
thr ough the Swinney membrane filter
fi lter
when the capillary tube is examined under a where microfilariae will be recovered. The
microscope.  membrane filter  can
 can be examined like a wet
a. Buffy Coat Films
smear preparation or may be dried, fixed, and
then stained. 
The capillary tube can be broken at the
Examination of Sputum 
area of the white cell layer after centrifugation
of the capillary tube. The white cell layer can There are several parasites that may be
 be spread and stained either
either with Giemsa or recovered from the sputum. These include: 
Wright’s stain. Trypanosomes and Leishm
 Leishmania
ania
are concentrated at the buffy coat portion.   A.  Mi gr a t i ng l a r v a e o f  A s c a r i s
lumbricoides, Strongyloides stercoralis,
b. Quantitative Buffy Coat (QBC) and hookworms
This method makes use of a capillary tube B.   Paragonimus ova 
which is precoated with acridine orange and C.   Echinococcus granulosus
gr anulosus hooklets from 
 potassium oxalate. A cylindrical
cylindrical float is inserted  pulmonary hydatid cysts 
to enlarge the layers. After centrifugation, the  D.  Protozoa such as: 
tube is read using an ultraviolet microscope. 1.   Entamoebah
 Entamoebahistolyticatrophozoites
istolytica
The DNA of the parasites takes up the acridine from pulmonary amebic abscess 
orange stain causing fluorescence  among the
fluorescence among 2.  Cryptosporidium parvum oocysts,
non-fluorescing red blood cells. This method is although very rare
useful in the demonstration of malaria parasites, 3.   Non-pathogenic
 Non-pat hogenic  Entamoeba
microfilariae, trypanosomes,
microfilariae,  trypanosomes, and Babesia .   gingivalis
 gingivalis and Trichomonastenax 
B. Venous blood may be concentrated in
For most sputum examinations, the first
order to detect microfilariae. Aseptic
technique must be observed in the
morning specimen is considered the best
collection of the sample. 
sample.   specimen to examine. If the patient cannot  
1. Knot s
’Concentra to
in ecxh ploer citdoer aotr eh,  yinddrr  ougcetna  p
nptesr olixkiede1m
0%ay siondcr iueamse  the
In cases of low microfilaremia,
microfilaremia, 1
 1 mL of amount of sputum collection. The specimen
 blood can be mixed with 10 mL of 2% formalin must be collected in disposable, impermeable,
and then centrifuged. The supernate is discarded tightly covered containers and must be sent to
and the sediment is studied. Part of the sediment the laboratory immediately. 
can be spread like a thin blood film  and stained. 
 

CHAPTER 7: Diagnostic Parasitology   329 

Methods  Aside from Trichomonas vaginalis ,

 A. Gross or Macroscopic Examination 
Examination 
some laboratories have reported recovery of
Wuchereriabancrofti microfilariae from chyluric
1.  Consistency of the sample as to samples. With massive labor exportation to the
serous, mucoid, purulent, bloody or Middle East, it is worth mentioning that the
combination, should be reported; and  Filipino overseas contract workers may acquire
acquire
Schistosoma haematobium. Eggs of this parasite 
2.  C or may  be indicative  of   cellular  
cooml position such as: are passed out with urine.
Examination of Tissue Aspirates  
Yellow color may indicate pus;
greenish tint may indicate Pseudomonas Samples aspirated from the following
infection; while bright red color   organs have been found to yield some
som e parasites. 
may indicate a recent bleeding rust
color may indicate breakdown of
1.  Liver  
hemoglobin.  
2.  Duodenum
3.  Bronchial 
B. Microscopic Examination 
Examination  4.  Lymph node
1.   Wet mount using saline or iodine is
5.  Skin 
useful when searching for protozoan In the Philippines, the most common
trophozoites; and  aspirate submitted for parasite diagnosis comes
from the liver. It is usually requested to rule  
2.  Sputum Concentration
out hepatic amebic abscess. Demonstration of  
If the sputum is thick or viscous,  Entamoeba
 Entam oeba hhistolytica trophozoites is not easy  
istolytica
an equal amount of 3% NaOH   especially in cases when the submitted material
is added, thoroughly mixed, and is aspirated from the center of the abscess where
then centrifuged. The supernate is there is necrosis. The best material for this
discarded, and the sediment is studied  purpose is aspirate coming from the margin or
as a wet mount.   the wall of the abscess. 
In endemic countries, liver aspirate can
Examination of Urine 
 be used in the recovery of hydatid sand,
Parasites have been reported from urine. composed of intact and degenerating scolices
Considered best for parasite recovery is urine of Echin
 Echinococcus
ococcus granulosus. While the parasite
granulosus
collected first thing in the morning, since there is generally believed to be absent in the
could have been concentration of parasites Philippines, there are a few reported cases of
overnight. infection in Filipino overseas contract workers
assigned to endemic countries. 
her indeia
f or   tU iaigsnaosviser oyf  gtor oicdhos pmeocnim
iaesnis  tvoagsitnuadlyis.  A. Duodenal Aspirate 
Aspirate 
The sample is centrifuged and the sediment is
studied under the microscope. The organisms There are occasions when duodenal
appear as rounded, globular, and transparent aspirates are better specimens to use in the
structures exhibiting jerky tumbling motion. diagnosis of the following:  
Vaginal and urethral discharges are also used
1.  Giardia lamblia
in the diagnosis of trichomoniasis.  
2.  Strongyloides stercoralis 
stercoralis 
 

330   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Duodenal aspiration may be done through 20 minutes, while the morphology and motility
intestinal intubation but there is a simple and of  Naegleria trophozoites are also affected
convenient procedure now available in the within the same time period. The CSF must
m ust
collection of duodenal contents. This is done  be centrifuged at 7,000 g for 10 minutes, the
through the “Entero
“Entero  Test,”
Test,” also
 also known as the supernatant fluid discarded, and the  parasites
String test, where a capsulated yarn is swallowed visualized from the sediment.
 by the patient. The yarn is expected to reach 
the duodenum. After about 4 hours, the yarn Examination of Tissue Biopsy Material  
is retrieved and the mucoidal material clinging  A.Muscle Biopsy  
to the yarn is examined for the
th e presence of the  This specimen is very useful in the diagnosis
above mentioned parasites.  
of Trichinella spiralis infection, where small
B. Cutaneous or Skin Aspirates 
Aspirates    pieces of muscles are pressed between two glass
slides and the preparation is examined under
In very rare occasions, there may be
the microscope. Encapsulated larvae may be
requests to examine aspirates taken from
appreciated. While Trichinella spiralis is not
cutaneous ulcerations,
ulcerations, like in cases of cutaneous  present in the Philippines, larval infection with
leishmaniasis. Like some of the parasites
Taenia solium can result in cysticercosis, or a
mentioned in other sections of this chapter,
larval infection with Spirometra spp. can result
leishmaniasis is not supposedly endemic in the in sparganosis. In both cases, muscle biopsy
Philippines but due to exposure in endemic
countries, there are reported leishmaniasis cases  will be useful in the diagnosis of the conditions.  
ly.ne  clinical  f or m  of   leishmaniasis  is
localO B. Rectal Biopsy  
A more common biopsy material
cutaneous, otherwise known as an Oriental sore. submitted for parasitic diagnosis is rectal
The recommended specimen is an aspirate taken  biopsy. Examination
Examinati on of the rectal
r ectal tissues
ti ssues can
from below the ulcer bed using a sterile needle. reveal the presence of deposited Schistosoma
Smears are prepared and stained with Giemsa  japonicum eggs. 
when dried. Positive samples will show the
 presence of amastigotes.
amastigot es. In endemic countries, References 
 part of the needle aspirate can be inoculated
Ash L, Orihel TC. Parasites: a guid e to
into a culture medium.  
laboratory procedures and identification.
Examination of Cerebrospinal Fluid (CSF)   Chicago: SCP Press; 1987.
Garcia LS, Buckner DA. Diagnostic medical
Trypomastigotes of Trypanosoma cruzi ,
 parasitology.
 parasitolo gy. New York: Elsevier; 1989.  
Trypan osomabrucei
Trypanosomabru hodesiensee, and Trypanosoma
cei rrhodesiens
Goldsmith R, Heyneman D. Tropical medicine
brucei gambiense may be demonstrated in
the CSF. Likewise, trophozoites of Naegleria Lanr agsei;to1l9o8gy9..  Connecticut:  A ppleton
and   p
may also be found in the CSF. In cases of Heinz M. Parasitology in focus: facts and trends.  
 parastrongyliasis, CSF eosinophilia is a common
 parastrongyliasis, Germany: Springer-Verlag; 1988. 
finding, although there were reports that among
Manson-Bahr PE, Bell DR. Manson’s tropical
infected children,  Paras
 Parastrongylus larvae have
trongylus
diseases. 19th ed.London: Bailliere Tindall;
 been recovered.
recovered.   1987. 
Immediate examination of the CSF is
Parzy D,Raphenon
D, RaphenonB,
B, MartetG,
Mart etG, NicolasP, Touze
Touze
required since trypomastigotes perish within   JE, Baudon D, et al. Quantitative buffy  
 

CHAPTER 7: Diagnostic Parasitology   331 

coat test kit for falciparum comparative Schmidt GD. How to know the tapeworms.
value in the rapid diagnosis of malaria. Med Iowa: Wm.C. Brown Company
Comp any Publishers;
Publis hers;
Tropicale. 1990;50(1):98 – 101.
101.  1987.
Rickman L, Oberst R, Sangalang R, Chulay Valencia CI, Abear RF. A modification of
J, Long G, Cabanban A, et al. Rapid the quantitative thick smear method for
diagnosis of malaria by acridine orange Schistosoma japonicum. Southeast Asian J
staining of centrifuged parasites. Lancet.
Lancet.  Trop Med Public Health. 1981;12:280 – 33.. 
1989;8629(1):3 – 9. 9. World Health Organization. Basic laboratory
methods in medical parasitology. Geneva:
World Health Organization; 1991.  
 

332   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Examination of Tissues
Elia G. Paulino-Cabrera

arasites may be an unexpected finding

finding  in with some other pathology. Schistosoma ova
tissues. A 60-year old male with headache  were incidentally found in the ovary and  
thought to have a primary brain tumor was fallopian tube of a patient operated on for
found to have cysticercosis (Plate 7.1). A 2-week uterine leiomyoma (Plates 7.2 and 7.3). A
old female with respiratory difficulty attributed  hemicolectomy specimen with adenocarcinoma
to herpes turned out to have Trichomonas also had Schistosoma ova (Plate 7.4). 
vaginalis of the nasopharynx. There are instances, however, when tissues
In other cases, parasites may not be the are deliberately biopsied for the diagnosis  
cause of the symptoms but are seen together   of parasitic diseases. Because of the ease of  

Plate 7.1. Cysticercus in brain Plate 7.2. Ovary with incidental finding of  
(Courtesy of Dr. Elia Paulino-Cabrera) Schs
itosomaa
j pon icumova (Courtesy
of Dr. Elia Paulino-Cabrera)

Plate 7.3. Fallopian tube with incidental finding of   Plate 7.4. Colon with adenocarcinoma and  
Schs
itosomaa
j ponc mova
iumo (Courtesy Schistosomao
aova
of Dr. Elia Paulino-Cabrera) (Courtesy of Dr. Elia Paulino-Cabrera)
 

CHAPTER 7: Diagnostic Parasitology   333 

obtaining other specimens like blood or stool for factor. It is more practical to biopsy a skin mass
detection of parasites, tissues are usually not the than a visceral mass to
t o document cysticercosis.
initial specimens sent for diagnostic purposes. A fourth factor is the possible complications
Biopsies are done when other specimens yield of the procedure. A hepatic puncture is more
repeatedly negative results or when other tests likely to have complications than a lymph node
are equivocal. For example, clinically suspected
s uspected  biopsy in the diagnosis of visceral leishmaniasis. 
ameba cases with negative stool examinations   Examples of commonly biopsied organs 
may be definitely diagnosed by a direct smear and parasites which may be found therein are
or biopsy of the intestine. A biopsy may also be shown in Table 7.2. 
needed in the case of chronic schistosomiasis 
when the patient no longer excretes ova. Some Table 7.2. Organs and parasites isolated
 parasites are found only in tissues, and biopsy
is the best means of diagnosis. The presence of Parasite
Trichinella spiralislarva in muscle, for instance,  Ancylostoma
diagnosis of  trichinellosis. 
 provides a definitive diagnosis brazil 
 Ancyl 
oso
l e nse
t ma
se(l(la rva)

Virtually any organ of the body can be can inum (a l l rva)

examined. Ova, larvae, adult forms, cysts, and  

trophozoites may all be seen. Before doing a Dracunculus
 biopsy, several
s everal factors
facto rs should be considered. consid ered.
First is the nationality and travel history of the
 patient. Leishmaniasi
Lei shmaniasis, s, which is not endemic  Filaria
Leishmania
Trypanosoma

ipapinateise,nsthwoiutlhdh be p 
idniatghneosPishinl  p  p if lf enr eonmtiegaal ly,
e   atods p
 p Brain Schistosoma

lymphadenopathy, and a history of travel to

the Middle East. The second factor is the life
cycle and tissue trophism of the parasite. An
adult nematode in a lymph node, for instance,
is almost certainly a filarial worm (Plate 7.5).
The accessibility of the biopsy site is a third  Sch s
itosoma

  Trichinella

Eye Toxocara
Toxoplasma

Trypanosoma
Toxoplasma

Definitive diagnosis depends on the

identification of the parasites. The morphology
of the ova, cysts, and trophozoites in tissues
Plate 7.5. Adult filaria with microfilaria in an
are similar to those in other specimens, such
inguinal lymph node as stool. Diagnosis of metazoans in tissues is
(Courtesy of Dr. Elia Paulino-Cabrera)  based on the demonstration of the following  
 

334   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Plate 7.6. Adult Trichuris

Trichurisid
iden
entiffiied
ed by ova
ov a in Plate 7.7. C ysticercus with calcareous corpuscles
genital tract (Courtesy of Dr. Elia Paulino-Cabrera) (Courtesy of Dr. Elia Paulino-Cabrera)

characteristics:
characte ristics: (a) integument, (b) musculature,  to them. Grossly, organs may appear normal,
(c)  body cavity, (d) digestive system, (e) enlarged, necrotic, or inflamed. Lesions may
reproductive organs and ova present (Plate 7.6),  present as tumorous masses such as in an
and (f) special glands or structures.  ameboma of the colon or echinococcosis of the
The integument may be chitinized liver or kidney. Fibrosis may cause hardening
hardening of
(arthropods), striated (acanthocephala), spiny   the parenchyma, such as pipestem fibrosis  in 
(M ar ientdhess)c, r  b
pluastcylheeslm
  p  iobr edsmeoitohtehr  (ansem aitaotdedes)o. r
str  weiiaalllls.iIs.n M
svcahr iestdoasos m cr eoisncso  p
soim hoalyo b
tpainccefisn, dnion pgsatm  gbiec
smooth, and circular or longitudinal. Points of changes are evident. Intestines of patients with
muscle attachment to the body and the number giardiasis and uncomplicated hookworm disease
of cells per circumference are also noted.  typically show normal-looking mucosa. 
Meromyarian pertains to few cells (four or Acute reactions are present when there is
less), while polymyarian pertains to numerous tissue necrosis. These are exemplified by early
cells per circumference. The body cavity is amebiasis, ulcerated cutaneous leishmaniasis,
described according to content, which may be trichomoniasis, and strongyloidiasis. Chronic
 parenchymatous
 parenchym atous matrix, mesenchyme cells, or inflammation is seen in any long-standing
fluid. Of
fluid.  Of interest in the digestive tract are the infection. A specific type of chronic infection
 pharynx and intestines.
intesti nes. The number of branches is characterized by granuloma formation. Dead
of the pharynx and the number of intestinal cells or degenerating parasites form the center of
should be noted. For the reproductive system, the lesion and are surrounded by
b y lymphocytes,
it should be determined whether the sexes are   plasma cells, macrophages,
macrophages, multinucleated
multinucleated giant 
separate
tubular orand whether
sac-like. the gonads
Special are paired
copulatory and  
structures
cells, and fibroblasts. Hyaline or eosinophilic
material may be present. Several parasitic  
may be present. Examples of special structures diseases show this reaction. Schistosomiasis
which serve as diagnostic aids are the calcareous and ascariasis lesions exhibit the characteristic
characteristic
corpuscles (Plate 7.7) seen in cestodes, and Splendore-Hoeppli phenomenon. In filar iasis,
iasis,
reduplication of esophageal glands as seen in granulomas are known as Meyers-Kouvenaar
the group Trichinellina.   bodies. 
Tissue specimens may show not only the Thereare findings that are pathognomonic
 parasites themselves
themselves but also the body’s reaction 
 body’s for some parasitic diseases. Lymph nodes in  
 

CHAPTER 7: Diagnostic Parasitology   335 

toxoplasmosis are characterized by the presence

toxoplasmosis Trichrome stain
Trichrome stain has been found to be useful in
of epithelioid histiocytes in the perifollicular differentiating the trophozoites of ameba and
zone. Malaria is characterized by the presence Giardia from host tissue. It also emphasizes
of hemozoin pigment in parasitized red blood structures such as flagella. Giemsa is used for
cells. In the brain, the characteristic finding different protozoa. Table 7.3 summarizes the
is Durck’s granuloma, which consists of glial  parasites and special stains used for them. 
 proliferations around capillaries. 
Fine needle aspiration biopsy (FNAB) may Table 7.3. Special stains and corresponding
 be done prior to or in lieu of a formal biopsy. parasites 
Parasite identification and host tissue response 
evaluation may be achieved with this method. Stain Parasite

Aspiration may be done on palpable lesions or Crypo

t spor d
iu
i mIsosporaCyco lspora

under the guidance of ultrasound or computed

  Toxocara
tomography. Toxoplasma
Biopsy specimens are placed in 10%
Trichomonas
 buffered formalin for fixation. Many laboratories
have automated tissue processors which allow Toxoplasma
slides to be completed the next day.
day. Processing
can also be done manually. Tissues are usually
cut 3 µm thick. Examination of serial sections
may be needed before a diagnosis is made.  
Sstoe p
m esteicmtieosntshaer  p
 p  o dleymtonos btr iagtethat
e areaqsiutier eids stimp
different levels of organ systems.  
Aspirates are smeared like peripheral blood Di 
rof 
i 
l 
arii 
a  Ga
i rd ia

smears. In aspirates which yield abundant

fluid, a
fluid,  a few smears should be made first.
first. The
 The Immunohistochemistry can be used as
rest of the specimen is preserved in an equal an adjunct in difficult cases. Immunologic
volume of 95% ethyl alcohol for cell block techniques and principles are applied. Parasite
 preparation. Touch imprints may be made on  protein is identified using anti-parasite
some specimens before fixation. Excess blood or monoclonal or polyclonal antibody.  
fluid is
fluid  is blotted off from the surface before the An ordinary light microscope is used to
specimen is pressed against a clean slide. Smears examine tissue slides. Sometimes, polarizing,
and imprints are fixed by placing slides in 95%  phase contrast, immunofluorescent and
alcohol for at least 15 to 20 minutes. Examples electron microscopy are used as well.
w ell. Ova of
of parasites which may be demonstrated on    Paragonimus , spores of Microsporidia, and  
touch imprints are Toxoplasma in placental hooklets of  Echinococcus are birefringent and
 Echinococcus
tissues and  Leishmania in lymph nodes. are demonstrable under polarizing light.  
Histopathologic
Histopathologic slides are routinely stained Polarization microscopy also increases detection
with hematoxylin and eosin (H & E). Special
Sp ecial of hemozoin pigment in placentas.  
stains may be needed to provide contrast Trichomonads and microscoporidians
 between parasite and the background, or to are enhanced by phase microscopy.  
highlight special structures. Periodic Acid Immunofluorescent microscopy is used in
Schiff (PAS) will demonstrate the cyst wall Trichomonasinfection. With acridine orange as
of Toxoplasma and the larva of Toxocara .  the stain, fluorescent microscopy is more reliable  
 

336   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

than wet mount or culture. It has also been used References 

as an adjunct in the diagnosis of Chagas disease.
Ultrastructure of human parasites, especially
especially Carter JE, Whithaus KC. Neonatal respiratory
of protozoa, has been described. Electron tract involvement by trichomoniasis
microscopy is employed for the definitive
vaginalis: a case report and review of the
literature. Am J Trop Med Hyg. 2008;
diagnosis and speciation of microsporidiosis. 
78(1):17 – 9.
9 . 
The first case of cyclosporiasis was demonstrated  
 by light microscopy. However, sporozoite, Chanandlaedr   jFuW
nc, tW hi.sItom
toattthseJC atuhnoolfloguiocr desiacgencoesaiss
 pm
trophozoite,
trophozoit e, schizont, and merozoite stages were of Chagas’ disease. J Clin Microbiol.  
identified by electron microscopy. Specimens 
Specimens  
1988;26(3):567 – 9 9..
forelectronmicroscopicstudiesare fixed in 3%
Chitwood M, Lichtenfels JR. Parasitology
glutaraldehyde in phosphate buffer. 
A tissue sample with parasites may also be review-identification of parasitic metazoa
in tissue sections. Exp Pathology.
sent for frozen section diagnosis, usually with an
1972;32:407-519. 
initial or a working impression of malignancy.
Preliminary diagnosis of the presence of a
Eapenn M, Matthew CF,
Eape CF,Aravind
Arav indan
an KP.
KP.Evidenc
Evi dencee
 based criteria for the histopathological
 parasite is usually satisfactory for surgeons. 
Definitive diagnosis can be made after routine
diagnosis of toxoplasmic
t oxoplasmic lymphad
lymphadenopa
enopathy.
thy.
J Clin Pathol. 2005;58(11):1143 – 6
6..
 processing. 
Gupta E, Bhalla P, Khurana N, Singh T.
Tissues from autopsy cases are treated in the
same way as biopsy specimens. Representative Representative   Histopathology for the diagnosis of
infectious diseases. Indian JMed Microbiol.
saencdtiostnasinf r 
reo dmaos  r igna b
nsioa pr esytask peenc,ifimxends, p
.Wr ocheoslse  d, 2009;27(2):100 – 6
6..
organs may be kept in jars for future references Kenner JR, Aronson NE, Bratthauer GL,
or as museum materials.   Turnicky RP, Jackson JE, Tang DB. etal.
There are limitations to tissue diagnosis of Immunochemistry to identify  Leishm
 Leishmania
ania
 parasites. Parasites
Par asites may ddegenerate,
egenerate, fib
fibrose
rose or i n fixed tissues. J Cutan  Pathol.
 parasites in
1999;26(3):130 – 6
6..
calcify. Severe inflammation or necrosis may
mask them. Artifacts may render identification  Ndao M. Diagnosis
Diagnosi s of parasitic
parasit ic diseases: old
difficult. For instance, formalin pigment may be andnew approaches[Internet].Interdiscip
difficult to differenti
d ifferentiate
ate from
fro m hemozoin
hemozoin.. Tissues Perspect Infect Dis. 2009 [cited 2010
may also be contaminated by bacteria or fungi Dec 30];2009:278246. Available from
which may show up in the slides. In such cases, http://www.hindawi.com/journals/
ipid/2009/278246.html.
otherdiagnosticmodalitieslike immunoassays,
molecular-based techniques and proteonomics Romagosa C, Menendez C, Ismail MR, Quintó
using mass spectrometry may be useful.   L, Ferrer B, Alonso PL, et al. Polarisation 
Criteria for the histopathologic diagnosis of cr ozsocoi p
heim
m n yanin cr l ea sasmesod tihuemsednetseitcitviiotyn  ionf   the
d P 
 parasitic diseases
 proposed like toxoplasmosis
toxoplas
in the absence mosis haveThese
of parasites. been histological assessment of placental malaria.
need further evaluation and correlation with   Act Trop. 2004;90(3):277 – 8 84.
4. 
Sahai K, Kapila K, Verma K. Parasites in
serologic findings. 
fine needle breast aspirates-assesment 
of host tissue response. Postgrad Med J.
2002;78:165 – 7 7.. 
 

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Song SM, Park JH, Kim J, Kim SI, Hong B. Fine needle aspiration of toxoplasmic
YC, Kong HH, et al. Identification
Identification and
 and (Piringer-Kuchinka) lymphadenitis:
characterization
characterization of Par
 Parago
agonimus. Parasitol
nimus acytohistologic correlation study. Acta
Int. 2008;57(3):334 – 41.
41. Cytol. 2005;49(2):139 – 4
43.
3. 
Sun T, Ilardi CF, Asnis D, Bresciani AR, Wong MT, Goh L, Chia KH. Inte stinal
Goldenberg S, Roberts B, et al. Light and schistosomiasis manifesting as colonic
electron microscopic identification of   intussuception arising from a mucocele of  
Cyclospora species in the small intestines. the appendix: report of a case. Surg Today.
Am J Clin Path. 1996;105(2):216 – 20.
20.  2008;38(7): 664 – 7
7.. 
Vega-Lopez F. Diagnosis of cutaneous Warton A. Diagnostic ultrasound of human
leishmaniasis. Curr Opin Infect Dis.  parasites. In: Papadimitriou
Papadimit riou JM, Henderson
2003;16(2):97 – 101.
101. DW, Sagnalo DV.Diagnostic ultrasound
Viguer JM, Jimenez-Heffernan JA, Lopez- of non-neoplastic diseases. Edinburgh:
Ferrer P, Gonzalez-Peramato P, Vicandi
Vi candi  Churchill Livingston; 1992. p. 203 – 1
11.
1. 
 

338   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 Advances in Diagnostic Parasitology  

Maria Cielo J. Pasay

iagnosis of parasitic diseases relies on the sensitivity of microscopic diagnosis of

laboratory diagnosis to complement    parasitic diseases, an
an experienced microscopist
microscopist 
clinical symptoms, clinical history, and travel is required. The sensitivity of microscopic
D 
history of the patient. While microscopic
demonstration of parasites remains the only
diagnosis is highly dependent on the level
of training and experience of a microscopist
tool available in resource poor settings, recent  for accurate identification of the parasitic  
developments in the diagnosis of parasitic agent. Specimen preparation for microscopic
infections provide promising alternatives. This examination can also be laborious and tedious
chapter will highlight new developments in when a lot of samples need to be examined
diagnostic parasitology.   during epidemiologic investigations. Therefore,
Therefore,
in parasite endemic regions with limited
Microscopy 
resources, misdiagnosis using the microscope
Microscopy as a tool to diagnose parasitic may compromise patient care. 
diseases remains as the gold standard in most Immunodiagnosis 
laboratories especially in the diagnosis of
common helminth and protozoan infections.  To overcome problems related  

, laendas initf oar llmowatsivdeir aesctmdoer  p
Itar ias ssitiems p
 p
tehctoiloongicoaf lly muicnr oodsciao p
o m
tim teicnhantiioqnueos f  p pr oar 
gnicosetixcam asites,
vide usef ul
distinct parasites are readily differentiated. alternatives. A number of immunodiagnostic
i mmunodiagnostic
However,
However, to achieve a good level of sensitivity, tests for parasitic infections are available that
microscopy requires high parasite density in detect either antigen or antibodies in clinical
the clinicalspecimen being examined. Parasites specimens. These include immunofluorescent
can be low in numbers during pre-patent and assay (IFA), enzyme-linked immunosorbent
chronic periods of infection, hence, microscopic assay (ELISA), hemagglutination test (HA),
examination may yield false negative results.   and immunoblotting (dot blot). These methods
Parasite concentration techniques such as are also useful in monitoring response to
the FLOTAC method can be used prior to chemotherapy.  
microscopic examination, but these require  A. Detection of Antibodies 
Antibodies 
additional equipment, supplies, and reagents.
 In vitroculture methods may enhance recovery Tests to detect antibodies against the
of parasites; however, a biosafety cabinet    parasite in question are used when biologic
and special culture media are required, and specimens do not permit microscopic diagnosis
results are not readily available. The use of an during chronic or asymptomatic infections.
ultraviolet (UV) fluorescent microscope can  also They are also recommended in parasitic
improve detection of parasites in wet mount infections where direct identification of parasites
 preparations.
 preparati ons. With fluorescence microscopy
microscopy,, in host deep tissues is not generally possible such
Cyclospora oocyts exhibit intense blue color as in toxoplasmosis or toxocariasis. Detection
in contrast to refractile spheres with distinct of antibodies is also a useful alternative in the
oocyst wall in bright fieldmicroscopy. While the diagnosis of cysticercosis
cysticercosis or echinococcosis
application of fluorescent techniques increases  where invasive techniques to obtain specimen 
 

CHAPTER 7: Diagnostic Parasitology   339 

for diagnosis can pose some risk to the patient. A antigens as they provide a larger repertoire of
 positiv e antibody
 positive antibod y test can be a useful indicator
indicato r of antigens recognized by the immune
i mmune system.
However, different types of antigen preparation
a recent infection
exposure if the patient
to the parasite priorhas
to no previous
travel in an (such as native protein, purified peptides,
endemic area. In contrast, positive antibodies and recombinant proteins) may also produce
in a resident of an endemic area may reflect variable antibody results. The use of a mixture
either past or current infection with a specific  of antigens can increase antibody detection but 
 parasite under consideration. Therefore, cross reactivity between parasite species cannot
 parasite diagnosis
diagnosis based on positive
positive antibodies
antibodies  be ruled out leading to false positive results. 
can only be indicative of infection at some   Given these limitations, the results of
indeterminate time and not necessarily current antibody tests in the diagnosis of parasitic
or acute infection. In addition, antibody tests infections must be interpreted with caution.
are useful when significant levels of antibodies The greatest utility of antibody tests is in
are produced with parasitic infections. In some investigating etiology of disease outbreaks and
 people, parasitic
parasit ic infections
infection s may not stimulate
stimulat e in epidemiologic investigations to map foci of
antibody response or seroconversion may be disease transmission essential to institute control
delayed with onset of clinical symptoms.  measures.  
Antibody detection assays use whole There are a number of antibody tests
 parasites from animal models or in vitro cultures available for the diagnosis of parasitic diseases at
or soluble crude extracts as antigens. Better the Centers for Disease Control and Prevention
sensitivity is achieved with the use of these  (CDC), USA (Table 7.4). There are only a few 

Table 7.4. Antibody detection tests offered at CDC  

Disease Test
Entamoebahistolytica Enzyme immunoassay (EIA)

Babesiosis Babesiamicroti

Trypanosomacruzi

Echinococcosis Echnococcusgranuosusi  l EIA, Blot

Leishmaniasis Leishmaniabraziliensis  
L.donovaniL.tropci a

Paragonimiasis Paragonmusweserman iti   Blot

Schistosomiasis Schistosomaspp.

Strongyloidiasis Srongyodessercorai sl 
tilt   EIA

Toxoplasmosis Toxop lasmagond ii   IFA-IgG, EIA-IgM

(Source: Division of Parasitic Diseases, Centers for Disease Control, Atlanta, Georgia, USA)
 

340   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

commercially available antibody detection tests

commercially available kits range from 93 to 100% when
to diagnose blood-borne parasitic infections used in clinical settings. Some EIA tests come
diseases
such such asand
as malaria giardiasis,
filariasis,cryptosporidiosis,
 intestinal parasitic in microplate
to format and are
detect Cryptosporidium robusteither
antigens enough
schistosomiasis, and cysticercosis.  from fresh, frozen or preserved stool samples
in either formalin or sodium acetate-acetic
B. Detection of Antigen 
Antigen 
acid-formalin (SAF). However, concentrated 
A mo r e s en s i t i v e a n d s p e c i f i c or polyvinyl alcohol (PVA)-treated samples are
immunodiagnostic test to determine the not suitable for EIA testing. Combined
Co mbined antigen
disease status of patients is the detection of   detection of either Cryptosporidiumand Giardia
specific parasite
specific  parasite antigens. Antigen detection or Cryptosporidium , Giardia and E. histolytica 
histolytica 
in serum or whole blood (for blood parasites)
p arasites) are also commercially available as rapid
and in feces, urine, duodenal fluid fluid or
 or biopsy immunochromatographic assays in fresh or
specimens from the small intestine or urine  preserved stool specimens. As the name implies,
(for intestinal parasites) is commonly achieved rapid tests have the advantage of quickest
 by immunocapture utilizing two antibodies. turnaround time and the least requirement
The first antibody (either monoclonal or for an experienced laboratory personnel. They
 polyclo nal) is immobilized
 polyclonal) immob ilized in a solid phase such also offer the convenience of multiple
multip le results
as a microtiter plate or nitrocellulose membrane.  in one reaction device without the need for
This will capture the parasite antigen which special equipment. Both EIA and rapid test
is detected by the second antibody, usually
usu ally a  kits show good correlation with DFA, which is 
A oconlocr leodnr aelaacntitoi b
m ioen.
 bnoisdoy blas ber evled awf tietr htahne aedndzyitm r te pstoir ntetdhetdoia bgentohseis m
of ocsr ty psetnos pitiovr eidainodsiss p
. Iet cuisfiecs a
of an enzyme substrate. Antigen detection fluorescein isothiocyanate (FITC)-labeled
tests have quicker turnaround times than monoclonal antibody which detects antigens on
microscopy and do not require experienced the surface of Cryptosporidium oocysts in either
microscopists. To date, much research work concentrated or unconcentrated fecal samples. 
has been achieved towards development and Pathogenic E. histolytica histolyticaand commensal E.
optimization of parasite antigen tests that dispar are morphologically identical. Antigen Antigen
resulted in commercially available reagents/kits detection tests thatdifferentiate the two species
for intestinal parasites such as Cryptosporidium eliminate unnecessary treatment of patients.
spp.,  E. histolytica , Giardia intestinalis , and Commercially available diagnostic kits are
Trichomonas vaginalis(Table 7.5).  mostly enzyme-based assays using monoclonal
monoclonal
Several commercially available kits for antibodies that detect galactose adhesins of
the detection of Cryptosporidium antigens the pathogenic E. histolytica. The Techlab E.
come in different formats such as enzyme   histolytica II specific for  E. histolytica was found 
immunoassay (EIA), directimmunofluorescence to be highly sensitive and specific
specific by  by several
(DFA), or IFA. These kits detect either studies conducted in at least five five countries
 countries in
Cryptosporidium alone, or combinations the world. A major drawback in using this kit
involving Cryptosporidium and Giardia or   in the diagnosis of intestinal amebiasis is the
Cryptosporidium, Giardia, and  E. histol
histolytica. The
ytica requirement for fresh, unpreserved fecal sample.
requirement
choice of test will depend on particular need for Extraintestinal manifestations
manifestations of amebiasis such 
single tests in clinical settings or batch testing as amebic liver abscess (ALA) on the other hand
in epidemiological investigations or research.
research. can be diagnosed by serology. Detection of Gal/
Sensitivities and specificities of commercially  GalNac lectin antigen in serum provides early  
 

342   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

diagnosis of ALA and can be used as a test of fluorescence  resonance energy transfer (FRET),
treatment efficacy. Additionally, the presence of and Scorpion primers.  

lectin in saliva
for invasive can also
disease be used
with as a predictor
the advantage of The principle
fluorescence of real-time
 chemistries PCR using
is illustrated two 
below:
noninvasive sample collection.  The principle of SYBR Green detection
Commercially available immunodiagnostic in real-time PCR is outlined in Figure 7.1.
tests for diagnosis of giardiasis are in the  The fluorescent dye SYBR Green is added to  
same format as the diagnostic test kits for the the PCR mixture (1). SYBR Green is a DNA
diagnosis of cryptosporidiosis and amebiasis.  binding dye that fluoresces strongly when
The same requirement for unpreserved
unpreserved stool   bound to double-stranded
double- stranded DNA. At the start of  
specimen applies for enzyme-based assays for the reaction, very little double-stranded DNA is
the diagnosis of giardiasis. Detection of Giardia  present, and so the fluorescent signal detected
cysts by DFA assay employs FITC-labeled  by the thermocycler
thermocycl er is low (3). As the reaction
monoclonal antibody which is highly sensitive  proceeds and PCR product accumulate, the
and specific
specific compared
 compared to microscopy.  amount of double-stranded DNA increases
and with it the fluorescence
fluorescence signal
 signal (4-5). The
Molecular Diagnosis 
signal is only detectable during annealing and
 Nucleic acid-based assays offer greater extension, since the denaturation step contains
sensitivity and specificity than the above  predominantly single-stranded DNA (6). 
mentioned tests. They allow for direct detection
of parasites in samples including those with
w ith 
vear tyienlotw
 p Tahr easiutseelooaf dgf er noemam
s.  p as pym f ictaotm
li p ioantic
technology by polymerase chain reaction (PCR)
detects nucleic acid sequences specific
specific to
 to the
 parasite in question. This technique uses two
oligonucleotide primers which flank the parasite
target sequence andTaq polymeras
 polymerase.
e. The process
involves successive cycles of DNA denaturation,
denaturation,
annealing of primers, and extension to generate
an exponential number of copies of the target
sequence using a thermocycler. The amplified
target is then analyzed by gel electrophoresis
or alternatively, by ELISA methods. Several
variations of the traditional PCR have been
developed to increase sensitivity such as nested
PCR where a second round of amplification
is introduced using a set of primers
prim ers internal
to the target sequence; multiplex PCR using
 parasite/species-
 parasite/sp ecies- specific primer sets to detect/
differentiate parasite/species
parasite/species simultaneously 
in one reaction tube; and real-time PCR to Figure 7.1. SYBR Green detection in real-time PCR
(From da Silva A, Pieniazek N. Latest advances
quantify srcinal template concentration by and trends
trends in PCR-based diagnostic methods.
using various fluorescence chemistries such as In: Dionisio D, editor. Textbook-Atlas of Intestinal
SYBR Green, sequence-specific TaqMan
aqMan probes,
prob es,   Infections in AIDS. Springer; 2003. p. 397-412.)
 

CHAPTER 7: Diagnostic Parasitology   343 

The principle of TaqMan real-time PCR Real-time PCR assays using SYBR Green
is depicted in Figure 7.2. The TaqMan probe are simpler and less expensive than TaqMan

is designedspanned
sequence to be complementary to a specific
by the PCR primers. The  probe assays. How
Howev
double-stranded er,, all
ever
DNA arefluorescencebound to
detected, including
TaqMan probe has h as a repotrer
repotrer dye at its
i ts 5’ en
 endd and  primer-dimers
 primer- dimers and other PCR artifacts. Caution
a quencher dye at its 3’ end.
nd. As long as the probe should be exercised when analyzing data
is intact and the reporter and the quencher dyes   resulting from this assay.To improve specificity, 
are in close proximity, no fluorescence signal a melt/dissociation curve analysis should be
is emitted due to the quenching effect (black included to distinguish real PCR products
arrow in 1, 2, and 3) (1). After the annealing of   from artifacts. Probe-based assays on the other  
the TaqMan
TaqMan probe (2) and the primers (3), the hand, are highly specific and can detect multiple
 primers are extended by the DNA polymerase. targets in one tube.  
As the polymerase
polymer ase reaches the TaqManprobe, it Other new molecular approaches in the
uses its exonuclease
exonucl ease activity
activity to remove the probe
pro be diagnosis of parasitic diseases such as loop-
one nucleotide at the time (4). This releases the mediated isothermal amplification (LAMP) and
reporter from the proximity of the quencher and Luminex-based technologies are also currently
allows for the release of a fluorescence
fluorescence signal
 signal available. LAMP reactions are easier to set up
from the reporter (5).  as they do not require extraction of parasite
DNA. The specimen of interest is mixed with
diagnostic primers, substrates, and DNA
 polymerase capable of strand displacement  
icr hocs p
ionf   pa ymr o p enhtr aitf eugioentsu bar ee.  p
Lar r ogdeucqeudandtuitr iiens g
the reaction forming white precipitates. The
resulting turbidity is proportional to the
amount of DNA synthesized which can be
measured in real-time or by the naked eye.
Unlike a conventional PCR, LAMP is carried
out at a constant temperature (usually 60-
65°C) therefore eliminating the need for a
thermocycler. LAMP can also be multiplexed
for simultaneous detection and differentiation
of parasite species. Because of its simplicity,
the use of LAMP technology in the diagnosis
of parasitic diseases in peripheral laboratories
shows promise. 
The Luminex xMAP
x MAP Technology
Technology is another
new method that allows for high throughput
diagnosis of parasitic diseases in large scale
studies, but is applicable only in central  
laboratories. It is a bead-based flow cytometry
assay that allows for simultaneous detection of
Figure 7.2. TaqMan real-time PCR
(From da Silva A, Pieniazek N. Latest advances
different targets (parasite species or genotypes)
and trends
trends in PCR-based diagnostic methods. in the same reaction using very low volumes.
In: Dionisio D, editor. Textbook-Atlas of Intestinal The microsphere beads are covalently bound
Infections in AIDS. Springer; 2003. p. 397-412.) to antigens, antibodies or oligonucleotides and  
 

344   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

used as probes in the assay. This assay is very  primers and TaqMan probes for E. histolytica
useful in parasite genetic diversity and drug and Giardia intestinalis were designed on a

resistant allele studies.  small

those ofsubunit ribosomal
Cryptosporidium RNA
spp. weregene, while
designed on
Molecular Diagnosis of Stool Specimens  
Cryptosporidium oocyst wall protein (COWP).
At the CDC, both conventional and real- This assay was found sensitive and specific when
time PCR analysis are currently used to detect validated with clinical specimens.
Cryptosporidium spp., Cyclospora cayetanensis,  Another multiplex real-time PCR assay
 E. histolytica, and E. dispar , while conventional  
histolytica using primers and probes targeting the
PCR is used to detect Giardia duodenalis and cytochrome C oxidase gene of Schistosoma can 
cytochrome
microsporidia. DNA is extracted from fecal detect and quantify two important species ( S.
samples and diagnostic primers are used to mansoni and S. haematobium) in fecal samples.
amplify target gene or sequence. Amplification Real-time PCR cycle threshold (CT) values
 products of conventional PCR are are loaded in representing parasite/species DNA extracted
agarose gels and analysed. Real-time PCR, on from fecal material show good correlation with
the other hand, measures the fluorescence signal egg counts of S. mansoni in stool and egg counts
in the reaction tube per cycle and is proportional of S. haematobium in urine. 
to the amount of accumulated amplified Recently, arapid diagnostic multiplex PCR
 product. The concentr
concentration
ation of amplified DNA (RD-PCR) to distinguish S. haematobium ,
is measured by comparing it to a standard curve.   causing human schistosomiasis from S. bovis,
A TaqMan-based
TaqMan-based real-time PCR has been   causing schistosomiasis in cattle was developed. 
deif vf elr oe pnetidataen
s dC vr  ya p
lit doa s pteodr iad tiutmhe hCom
DiCni swhf rr io chm T
s p ies isina Asyf rr mi c paaatr nicd othcceuyrr heanvce tohf e tah beisleitytwto
 pheecr 
Cryptosporidium parvum. The assay combines infect the same intermediate snail host, Bulinus  Bulinus,
a generic TaqMan assay which targets the 18S thus, there is a need for a reliable method to
rRNA to detect Cryptosporidium species and differentiate the larval stages of the parasite.
two other TaqMan assays to identify
ident ify C. hominis This assay uses a single forward primer and
and C. parvum . The generic TaqMan assay two species-specific reverse primers targeting
can detect one to 10 oocysts in a 300 µL stool the cytochrome oxidase subunit 1 (COX 1)
specimen, and the two species-specific TaqMan mitochondrial DNA (mtDNA) which gives a
assays are ten-fold more sensitive. These are 306 bp PCR product for S. bovis and 543 bp
valuable tools in outbreak investigations of PCR product for S.haematobium. 
cryptosporidiosis. Several molecular methods of detection
A single-tube multiprobe real-time PCR and differentiation of Taenia species in stool
assay can simultaneously detect the pathogenic
pathogenic  samples have been developed. These include
 E. histolytica and the non-pathogenic E. dispar .
histolytica PCR restriction fragment length polymorphism  
The assay uses two species-specific probes (PCR-RFLP), multiplex PCR targeting
encompassing new SSU RNA regions of the mitochondrial DNA, and nested PCR method
ribosomal DNA-containing episome. It is a targeting Tso31 gene encoding the T. solium
highly sensitive assay capable of detecting one oncosphere-specific protein. A simple but highly 
 Entamoeba per mL of feces and is therefore sensitiveand specific LAMP technology, on the
more sensitive than a conventional nested other hand, targets COX 1 and cathepsin L-like
PCR method. A multiplex real-time PCR cysteine peptidase ( clp) genes for differential
assay can simultaneously detect  E.histolytica
histolytica, detection of Taenia
Taeniaspecies. This method utilizes
Giardia intestinalis and Cryptosporidium spp. a Bst DNA polymerase with strand replacement
in one tube using parasite-specific probes. The  activity and four primers that recognize six 
 

CHAPTER 7: Diagnostic Parasitology   345 

sequences on the target DNA under isothermal filarial antigens are detected by either ELISA
conditions. DNA prepared from proglottids, or immunochromatographic test (ICT). Several
cysticerci,
can be usedandfor
fecal
thissamples
assay.of
  taeniasis patients PCR-based assays are available
malaria or Bancroftian to diagnoseIn
filariasis separately.
areas where the two parasitic diseases are co-
Molecular Diagnosis of Blood Specimens  
endemic, a multiplex PCR assay can be used
A highly sensitive multiplex real-time PCR to simultaneously detect P. falciparum and W. 
assay has been shown to detect the five human   bancroftii in humans and
 bancroft an d a real-time multiplex
mult iplex
 Plasmodium species ( P. falciparum, P. vivax
 P. falciparum vivax, P
 P..  quantitative PCR assay to detect P. falciparum
falciparum
malariae ,  P. ovale
ovale, and  P. knowlesi
knowlesi) in a single and W. bancroftior P. vivaxand W. bancroftiin
reaction tube even in samples with very low mosquitoes. Recently, a multiplex, post-PCR  
 parasitemia.
 parasitemi a. This method
meth od has been optimized
optimize d oligonucleotide ligation detection reaction-
for the detection of mixed infections with the fluorescent microsphere assay (LDR-FMA)
increased sensitivity of detecting minor species was developed for simultaneous detection
d etection of
 by using species-
species-specific
specific forward
 forward primers in four  Plasmodium spp. and W. bancrofti in
combination with a conserved reverse primer.  blood samples.
samples. This methodology
methodology is very useful
useful
It also provides great advantage over standard in the conduct of large scale epidemiologic
microscopy as it allows quick turnaround investigations in areas where malaria and
time and reduces cost per assay in large scale co -endemic. 
Bancroftian filariasis are co-endemic.
investigations. Multiplex real-time PCR can also
investigations. PCR-based assays are capable of detecting
 be used in differentiating
differenti ating drug-s dr ug-sensitiv
ensitivee from   very low parasite loads, making them more  

inr uing-sr tietsuisttianngtm
d str  ealatmmeond ti.um, impor tant
aalainr isaotf r  P 
 s ivoeunmdethimodes  of f fe dr iatghneo bsiesn. eTfiht eoif r   eqaur ilcyk
steunr nsiatr 
LAMP technology was recently used in   diagnosis and treatment of patients. Efficacy
the diagnosis of malaria by targeting the 18S of treatment can be monitored as a decrease in
rRNA gene to simultaneously detect the four  parasite DNA
D NA concentrations
concen trations by
b y quantitative
quanti tative
human Plasm odiumspecies
 Plasmodium species.. When compared to real-time PCR; however, results should be
nested PCR in the diagnosis of malaria, LAMP interpreted with caution as they may not
demonstrated a similar level of sensitivity, necessarily mean non-viability of the parasite in
greater specificity, and a faster turnaround time.  question. The chances of false negatives due to
Three LAMP assays based on SAG1 ,  presence of PCR inhibitors that may be present
SAG2, and B1 genes of Toxoplas
Toxoplasmama gondii are in blood and other clinical specimens and false
highly specific and sensitive, and allow  rapid  positives due to carry-over contamination
detection of active toxoplasmosis compared should not be overlooked. In this regard, proper
to conventional nested PCR. The lowest standardization procedures are needed for more
limit of detection of these LAMP assays is 0.1 reliable and reproducible results. Without these,  
tachyzoite, and they do not cross react with PCR-based assays cannot be routinely used and
DNA of other parasites.  may be limited to in-house
in -house research use only. 
Malaria and lymphatic filariasis  are co-
filariasis are
Rapid Diagnostic Tests (RDTs) 
endemic in many tropical and sub-tropical
regions such as Southeast Asia, Western Pacific, While molecular-based assays show
Africa, South and Central America. As such, excellent sensitivity, specificity, and rapidity
other diagnostic tests have been developed than other methods of diagnosis of parasitic
to complement microscopic examination of diseases, their use is still uncommon in daily
stained blood smears to detect  Plasmodium laboratory practice especially in rural endemic
spp. and Wuchereria bancrofti. Circulating   areas where cases of parasitic infections are  
 

346   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

concentrated. Early diagnosis and treatment of stool, urine or other body fluids. These assays
any parasitic disease are essential components employ immunochromatographic
i mmunochromatographic methods in
of control programs,
development hence the
of diagnostic continued
tests that can lateral
within flow  devicesThey
15 minutes. wheredoresults are available
not require skilled
 be performed on site without the need for microscopists but provide accurate diagnosis
electricity, sophisticatedequipment,
sophisticatedequipment, or extensive in a timely manner important for prompt and
training of laboratory personnel. The use of   appropriate treatment.
Rapid Diagnostic Tests (RDTs) therefore has  A. R DTs for m alari a  
great potential in improving
improving diagnostic accuracy
of parasitic infections in field settings that still  A malaria RDT (Figure 7.3) is a lateral flow
rely on the microscope.  immunochromatographic device that detects
RDTs use antibodies (monoclonal or  protein [antigen
[anti gen (Ag)] derived from the blood
 polyclonal)
 polyclo nal) to detect parasite antigens in blood,   stage of malaria parasites. Blood is usually  

Figure 7.3. Mode of action of antigen-detecting malaria rapid diagnostic tests (RDTs)  
(From Bell D, Wongsrichanalai C, Barnwell JW. Ensuring quality and access for malaria diagnosis: how
can it be achieved? Nat Rev Microbiol. 2006 4(9 Suppl):S7-20.)
 

CHAPTER 7: Diagnostic Parasitology   347 

obtained from a finger  prick,

 prick, in a similar way test kits detect pLDH from all four
fo ur species of
to that usually used for malaria microscopy. A  Plasmodium and can differentiate  falciparum

small sample
 placed on theof blood,
RDT usually
strip, or in 5ato 20 µL,
well is
of the from
 P. non-
riaee falcipa
malaria
mala  falciparum
rum
, P. viva species
x, and
vivax  P. but. Newer
 P. ovale not between
RDTs 
cassette or card test device, and lysed to release developed can detect both PfHRP-2 and pLDH
the Ag from within red blood cells and parasites at the same tim
time.
e.
from within these cells (a variable amount of   To date, over 50 brands of malaria RDTs  
Ag is also present in the serum). After several are manufactured, and over 150 products are
minutes, the test produces a series of visible commercially available. RDTs for malaria are
lines to signal the presence or absence of Ag in   easier to perform than the standard microscopy 
the blood sample by the mechanism outlined and have great potential to accurately diagnose
 below.
 below. (a) Dye-labelled antibody (Ab), specific malaria in endemic areas. Several malaria
for the target Ag, is present on the lower end RDTs have been tested in the field,
field, and
 and good
of the nitrocellulose strip, or in a well provided levels of sensitivity have been achieved with
 by a casing covering the strip. Ab, specific for  parasitemi a levels of >100 parasites/µL
 parasitemia parasites/ µL blood.
another epitope on the target Ag, is bound to However, sensitivity drops when parasitemia is  
the strip in a thin (test) line, and Ab specific for <100 parasites/µL. Failure to detect cases with
the labelled Ab is bound at the control line; (b) very high parasitemias have been reported.
Blood and buffer, which have been placed on Variability in performance of commercially
the strip or in the well, are mixed with labelled available RDTs in the field
field have
 have been found
Ab and are drawn up the strip across the lines   to be influenced by several factors such as kit  
owf i b  be;d(co)nIf thAegteist plr inese.nOt,tlha b
ll  bouentdr a pA p  bdelAle bd
er elale ter xatnr es p
moer team satotur ar geeancdonhduim
n pder  tioidnisty()s,en
qusiatliivtey tof
Ab is trapped on the control line. If sufficient manufacture, and variability in interpretation
labelled Ab accumulates, the dye labels will of results by laboratory personnel. Generally,
 become visible to the naked eye as a narrow line.  HRP-2 based assays demonstrate comparable
RDTss for malaria detect either 
RDT ei ther  P. falciparu
falciparum
m sensitivity to good quality microscopy, and
histidine-rich protein 2 (  Pf HRP-2),
HRP-2), a water other factors affecting their performance have
soluble protein specific to  P. falciparum ,  been recently
recentl y investigated.
invest igated. Genetic
Gen etic diversity
div ersity
or parasite lactate dehydrogenase (pLDH) of Pf HRP-2
HRP-2 gene was determined and it was
 produced by all four  Plasmodium species. found that the deduced amino acid sequences 
 Pf HRP-2
HRP-2 is synthesized throughout the asexual are highly polymorphic in different isolates.
i solates. The
life cycle of the parasite and identified as a number and sequence of specific repeats present
surface-exposed protein in infected red blood in Pf HRP-2
HRP-2 vary widely; therefore, the epitopes
cells. It is also found circulating in the peripheral recognized by the monoclonal antibodies
 blood of infected individuals, hence a good  specific to
specific  to HRP also vary between isolates.  
target for the diagnosis of P. falci
falcipa
parum. HRP-2
rum Additionally, it was found that monoclonal
 based kits however, cannot be used to monitor antibodies raised against  Pf HRP-2
HRP-2 can also
treatment efficacy as HRP-2 stays in circulation  bind to  Pf HRP-3
HRP-3 which raises its potential
for as long as two weeks after parasite clearance.  role in the performance of HRP-based RDTs. 
While pLDH (an intracellular metabolic Despite extensive global sequence variation in
enzyme produced by both asexual and sexual  Pf HRP-2,
HRP-2, no statistically robust correlation
stages of malaria parasites) does not persist in  between gene structure
structur e and RDT detection rate
the blood, it may provide a good indication of for P. falciparum parasites at 200 parasites/µL
 parasite clearance
clearance following treatment.
treatment. Current   blood was identified. However, a more recent  
 

348   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

investigation in the Amazon region of Peru disease is endemic. Evaluation of ES33-MICT

found that a large proportion of P. falciparum showed 94.5% sensitivity and 96% specificity in
in
isolates implies
finding lack  Pf HRP-2
finding implies H RP-2
that and  Pf 
HRP-2 HRP-3.
HRP-3.
based RDTs This
will detecting taeniasis, and
93.9% sensitivity while98.9%
ES38-MICT showed
specificity in
fail to detect a significant proportion of  P. detecting cysticercosis. 
 falciparum in malaria endemic areas in Peru Diagnosis of schistosomiasis relies heavily
and should therefore not be used. Instead,   on stool Kato-Katz technique which can  
 pLDH-bas ed RDTs and quality
 pLDH-based qualit y microscopy
microsco py  be cumbersome
cumbers ome when performin
p erformingg disease
are recommended for the diagnosis of malaria surveillance and mapping for large scale
s cale
in the area.   control programs. The use of RDT as an  
In malaria endemic areas, mixed infections alternative method to estimate prevalence
with P. falciparum and P. vivax are not and intensity of infection is now undergoing
uncommon; therefore a combination RDT field evaluation. One commercially available
kit is a more appropriate diagnostic method. RDT to diagnose schistosomiasis detects the
The Care StartTM Malaria-HRP-2/pLDH  presence of circulating
circulating cathodic
cathodic antigen (CCA)
(CCA)
(Pf/Pan) Combo Test is a three-band RDT in urine. This method eliminates the need for
that can detect both Pf HRP-2
HRP-2 and pan-pLDH a fecal sample which is more difficult to collect
from infected blood. It is a lateral flow antigen from patients. A positive association between
detection test in a cassette format. The presence increasing intensity of CCA urine-dipstick test
of an HRP-2 line indicates infection with P.
 P.  band and fecal eggcount was observed;however, observed;however,
 falciparum , and the presence of a pan-pLDH  difficulty in assigning trace reactions as putative 

ltihne nionnd- P 
ica.t f easl cii p pewcitehs. oTnhe  p
nf aer cutimons  p seonr 
o rem ce of enegcoatuivneter oer d p. uOtavteir vaell pdoisaigtinvoestiincf escetniosintivwitays of
n
 both HRP-2 and pan-pLDH lines indicates this CCA urine-dipstick is 87.7% and specificity
mixed infection with P. falciparum
falciparum and one is 68.1%, a useful supplement to Kato-Katz
or more of the non- P. falciparum
falciparumspecies. A examination for the rapid detection of intestinal
recent evaluation of this improved RDT against schistosomiasis.  
microscopy and PCR-diagnosed blood samples Visceral leishmaniasis is commonly
showed good
goo d levels of detection
detecti on for 
for  P
 P..falcipa
falciparum
rum diagnosed by microscopic identification of
and P. vivaxand poor levels of detection for P. the parasite in bone marrow, spleen, or lymph
malariae and  P. ovale
ovale. node aspirates. In field  settings, this method
field settings,
is unsuitable. The development of a rapid
B. RDTs for other parasites  
diagnostic test using rK39 antigen to detect
A magnetic immunochromatographic  Leishmania antibodies revolutionized the
test (MICT) to detect taeniasis caused by the
th e diagnosis of visceral leishmaniasis in the Indian
adult worm of the cestode Taenia solium and  subcontinent. However,
However, the same high level of  
neurocysticercosis
neurocysticercosis caused by the larval forms sensitivity and specificity of the rK39 -based
has been developed based on two specific
specific  T. RDT cannot be achieved when the test was
 solium excretory-secretory proteins, ES33, used in the African
Af rican subcontinent
subco ntinent.. To
Toaddress this
thi s
and ES38. This test detects antibodies against   issue, another rK38 polyprotein-based RDT  
human T.solium
soliu m and can be used as a point-of- was developed which when tested in Sudan and
care case detection or confirmation. This assay Bangladesh demonstrated a much improved
is also a useful tool in identifying tapeworm  performance than the rK39-based RDT.
carriers that must be treated to ensure success This new RDT was found to be an excellent
of control programs in communities where the   serodiagnostic tool and has great potential in  
 

CHAPTER 7: Diagnostic Parasitology   349 

simplifying diagnosis of visceral leishmaniasis technologyy in the diagnosis of several parasites

technolog
at the point-of-care.  such as  Entamoeba , Trypanosoma , Taenia,
Towards New and Im proved Technologi
Technologies
es   Plasmodium
 Plasmodium
C.
studies , and
show Cryptosporidium
very , and current
promising results.
Previous experiences
experiences in the
t he use of RDTs Development of new and improved
for malaria diagnosis have documented diagnostics is a fast evolving field; therefore, it is
thermostability as one critical factor affecting   expected that in the very near future, diagnosis  
variability of their performance in the field. of parasitic diseases can be done with ease
Majority of commercially available RDTs were and confidence at the point -of-care requiring
developed for storage and use at 25-30°C,   minimal training.  
 but are used in malaria endemic areas where
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14.
 

352   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Quality Assurance in a Parasitology Laboratory  

Vicente Y. Belizario, Jr., Winifreda U. de Leon,
Serafin O. Malecosio, Jr., June Rose A. Naig  

uality assurance (QA) refers to a system in testing, and the results are compared
which there is a continuous improvement  to the standard. It gives an objective  
in reliability, efficiency, and utilization of measure of the laboratory performance
Q 
laboratory services. It encompasses all factors
that affect laboratory performance such as
and it is cost-effective.  
2.  Rechecking or retesting, in which
 procedure manuals; quality control for tests  the slides that have been read are
reagents, and equipment; workload; work rechecked or samples that have been
rechecked
 place conditions;
condi tions; training and laboratory
labor atory staff analyzed are retested by the reference
support. It is an important part of the operations laboratory. It is useful when it is
in clinical laboratory practice, which could be difficult to prepare samples to test all
attained through:  of the testing process. It is expensive
and uses considerable staff time. 
A.  Internal Quality Control (IQC), in 3.  On-site evaluation is done when it
which a set of procedures is utilized by is difficult to conduct traditional
laboratory personnel
personnel in the assessment  proficiency testing or to use the
of their laboratory work. Internal rechecking/retesting method. It is 
quality control allows the laboratory
laboratory
to look at its own processes, ensures
aveenl stiivme,e.and r equir es staff  time and
etr x p
that the staff performed the test to the
 best of their ability with utmost care.
car e. QA in a diagnostic parasitology laboratory 
It can be done frequently as needed, is a guarantee of reliability of the results obtained
and it is more economical compared
compared in the diagnosis of parasitic infections. Its main
to external quality control.  objective is to make sure that the laboratory
B.  External Quality Assessment (EQA),  produces reliable,
r eliable, relevant,
r elevant, and reproducible
reprodu cible
in which there is an objective and results based on generally agreed principles
 periodic assessment of the laboratory andusing acceptedcriteria.Accuratelaboratory
 performance by an outside party  diagnosis of parasitic infections provides a sound
or agency. External quality control  basis for the provision
provisi on of appropriate
appropr iate treatment,
 provides early warning for systematic
systemat ic as well as a basis for formulation of health policy
 problems in laboratory processes, (Figure 7.4). 
indicates areas thatneed improvement,   The components of quality assurance,  
identif ies  tr aining needs,  pr ovides which ar e im por tant in  pr oducing r eli  ble
o b jecallows
and t v v d n
i e e comparison
  f  t s t ng q ali y,
i e ce o eof iperformance
u t r esults, incluand
 personnel de tthe
he  puse cienstandardized
r ofiof cy of  la bor ator y
and results among different test sites.   techniques. The standard techniques start from
the choice of procedure and reagents, collection
The three types of external quality of parasitologic samples (stool, urine, blood,
assessment are:   orifice swabs, aspirates, etc.) to the proper
1.  Proficiencytesting,
Proficiencytesting, in which unknown  processingg of the specimen, accurate reading,
 processin
samples are sent to the laboratory for   and correct reporting of results.  
 

CHAPTER 7: Diagnostic Parasitology   353 

of the hierarchical status, should strive and

 be responsible
responsi ble in achieving
achi eving quality.
qu ality. Current
Cu rrent
laboratory
identified,status should be made,
and appropriate stepsdeficiencies
initiated.  
On the other hand, in the External QAP, a
clinical laboratory is required to participate
in the National External Quality Assessment 
Scheme (NEQAS) administered by designated
 National Reference Laboratories (NRLs). The
 NEQAS is a schematic quality assessment 
of laboratory processes using materials of
known but undisclosed results through an
Figure 7.4. A flowchart showing the importance
of ensuring quality of laboratory diagnosis of external agency. It is conducted to ensure that
parasitic infections  laboratory procedures are done in accordance
accordance
with standards, and that laboratory results are
accurate and within the standard range for
Quality Assurance Program for Parasitology  
quality health care. The Research Institute of
A number of quality assurance programs Tropical Medicine (RITM) is the reference
for parasitology have been established in laboratory designated to conduct NEQAS in
different countries, and one good example    parasitology laboratories. 
is the United Kingdom National External  
Three Stages of Quality Assurance in a

Paur alsityoloAgsys.uIr tahnacse r aSicsheedmthee (lU

Q el NoEf  aQwAaSr e)nf eossr
evK  Parasitology Laboratory 

on parasitic infections in UK laboratory practice The QA in a clinical laboratory encompasses

encompasses
 by highlighting problem areas and providing the entirety of the testing process beginning with
focused teaching/training. The UKNEQAS
UKNEQAS was a clinician ordering a test and ending with the
designed to improve the diagnosis of parasitic clinician interpreting the results. All activities
disease by examination of samples from patients necessary to produce accurate results are part
with parasitic infections, to provide teaching of quality assurance. It is divided into three
material illustrating unusual or uncommon stages, namely, pre-analytical, analytical, and
 parasites, and to target areas where a particularly
particular ly  post-analytical
 post-an alytical stage.
st age. The pre-analyti
pre -analytical
cal stage
 poor performance was noted. At prese
present,
nt, the includes activities performed before the actual
UKNEQAS has the following sub-schemes:   laboratory procedure that influence the quality
(a) fecal parasitology, including extra-intestinal of laboratory results. These activities include:
 parasites; (b) blood
bloo d parasitology,
parasito logy, including
in cluding the training of personnel conducting the 
tissue parasites; (c) Toxoplasma serology; and   test; preparation of a patient before specimen 
(d)  the teaching sub-scheme. collection; specimen collection; specimen
In the Philippines, every clinical laboratory  quality and volume; and specimen handling and
is required to have a quality
qu ality assurance program labeling.Theanalyticalstageincludestechnical
t echnical 
(QAP) as a requirement for procurement of or laboratory procedures performed to produce
license. The QAP shall include an Internal accurate test results. It covers routine work
w ork
and External Quality Assessment Program. In organization, the type of test and reagents, the
the Internal QAP, implementation of internal state of the equipment, and standard operating
quality control measures should be ensured in  procedures.
 procedure s. It also includes all aspects of quality
each laboratory. Laboratory staff, regardless
regardless  controlincluding corrective measures to be done  
 

354   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

when inaccuracies in the results are identified.

identified.   Procedure Manual 
The post-analytical stage includes proper  
A procedure
procedure manual must be made available
availab le
and accurate reporting
organization of results.
of recording, It includes
reporting, and to the laboratory personnel for reference. This
should contain the following information: 
interpretation of results, and speed of reporting.  
Personnel 
1.  Instructions for proper collection and
handling of samples  
The laboratory supervisor has overall 2.  Inform ation on when to reject
responsibility for QA in a diagnostic parasitology  parasitologic
 parasitologic sample (e.g., inadequate
inadequate
laboratory. The qualifications of the supervisor amount of specimen, specimen not
must be consistent with the existing policies labeled with full name or ID number,
on the operation of a clinical laboratory. The improperly preserved specimen, etc.) 
supervisor should ensure that:  3.  Preparation of reagents and solutions  
1.  A procedure manual is available  4.  Detailed description of techniques  
2.  Records are properly kept  5.  Criteria for identification of  parasites
 parasites 
3.  Controls are available for diagnostic 6.  Quality control procedures
 procedures 
7.  Reporting and interpretation of results  
4.  Equipment and instruments (e.g., 8.  General safety precautions (e.g.,
use of gloves, laboratory gown,
microscopes,, incubators, centrifuges,
microscopes
etc.) are properly functioning and  proper disposal
 proper handling
han of inflammable
dling of specimens,
inflammab and  
le  and
calibrated 
5.  Clerical and analytical errors (if hazardous reagents, etc.)  
committed) are corrected   In a study that assessed the quality assurance
6.  Unusual laboratory results (e.g., of a number of clinical laboratories in Iloilo,
uncommon parasites, unusual Philippines, 65.5% of laboratories visited were
antibody titers, etc.) are checked   shown not to have any manual of procedures
7.  Standardized procedures are being available as reference. 
followed in the laboratory 
Instruments and Equipment 
All laboratory personnel should be trained
on the different aspects
aspect s of running aparasitology A diagnostic parasitology laboratory must
laboratory. The person in charge of providing  be adequately
adequatel y equipped
equippe d in order
ord er to guarantee
instructions to the patient must be familiar with efficiency. As in any laboratory, preventive
maintenance of instruments and equipment
all aspects of specimen collection including
must be routinely done. This will ensure that
 preparati on of the patient, specimen collection
 preparation collectio n
all instruments and equipment are in good 
times, sample quality and volume, condition
of specimen container, use of preservatives, condition and are properly functioning.
and proper labeling. Laboratory staff must The most important instrument used
 be familiar with the appropriate diagnostic in a diagnostic parasitology laboratory is the
microscope. It needs constant care to keep it
 proceduress to be used for each type of specimen
 procedure
in good working condition. The alignment
and parasite, and must be competent in
of the condenser must be regularly checked.
ch ecked.
morphologic recognition and differentiation
of parasites.  The microscope must be protected from dust, 
 

CHAPTER 7: Diagnostic Parasitology   355 

vibration, and moisture. Heat and humidity can Reagents 

lead to fungal growth, which can damage the
In practice, not all reagents in a parasitology
lenses. Thetissue
using lens lensesand
should be cleaned
not other regularly
types of tissues laboratory require periodic review; however,
that may scratch the lenses. Desiccants should antigens,stains,and fixatives should be checked
 prior to use. Reagents for concentration
 be placed in the microscope
microscop e cabinets to prevent
accumulation of moisture. 
techniques like zinc sulfate solution may require 
In the identification of protozoan cysts  bchueff cekr inr geaogef  ns ptsecmifiacy gar lsaovithya,vw
e htoile btehceh pecHkeodf .
in particular, size is taken into consideration. All reagents must be properly labeled, and
It is recommended that microscopes should  
must have preparation and expiration dates. It
 be calibrated using an ocular and
and a stage
is also wise to remember which reagents must
micrometer.  
 be kept in sealed containers or dark bottles
A stereoscopic microscope should also be to prevent degradation. Special precautions
available in a diagnostic parasitology laboratory must be observed in handling and storing of
for easier examination of large specimens such explosive chemicals like phenol crystals, as
as adult worms and worm segments, as well as well as flammable solvents like xylene, ether,
arthropods. 
and acetone. 
In most concentration techniques,
centrifugation is necessary. Centrifuges must If reagents are purchased commercially, lot
also be calibrated for appropriate speed.  
and/or batch numbers must be properly noted.
Properly calibrated balancing tubes at opposite   Overstockin
Overstocking
solutions forg blood
of commercially prepared
parasites must staining 
be avoided.
 bduam
ckaegtes  ator etshter ocnegnltyr ir f eucgoemanmde b
ndr eadktaoge por ef vtenst The quality of the stain can be checked by using
tubes. The inner walls of the centrifuge must be a positive slide as control at least once with
every new batch of stain. The use of control
wiped with antiseptic after each use.  
Temperature of refrigerators,
refrigerators, incubators, reagents is strongly recommended particularly
in seroimmunodiagnosis. 
water baths, and freezers must be regularly
checked using a standard thermometer. A good Appropriate Parasitologic Techniques 
diagnostic parasitology laboratory should also
The use of appropriate parasitologic
have a fume hood where the use of volatile or
toxic chemicals for diagnostic procedures such techniques in the laboratory will help ensure
as ether and formalin should be done. 
accuracy of results from diagnostic procedures.
The choice of laboratory technique may
Additional items that may be needed in
depend on what is being considered as part
a parasitology laboratory include pH meter,
differential counter, and glassware (e.g.,
of differential diagnosis and what particular
microscope slides, volumetric flasks, beakers,   purpose the
t he laboratory
laborat ory examination
exami nation is being  
funnels, drop bottles, pipettes, test tubes). r equested f or . For  instance, diarr heic stools that
Chipped glassware must be properly discarded. m ight contamay
duodenalis in  Entam
 Entamoeba
oeba
be best h
histol
istolytica
examined ytica or Giardia
using direct 
With the increasing problem on parenterally-
parenterally- fecal smear. A number of intestinal helminths
transmitted organisms (e.g., Hepatitis B virus,  are better demonstrated using modified Kato
HIV,, malaria), the
HIV th e use of disposables like gloves,
syringes, and needles is also recommended.  
thick smear method than by direct fecal smear.
Routine parasitologic screening and diagnosis  
 

356   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

in health centers and hospitals may make use Reporting 

of combined direct fecal smear and modified
Results of an examination done in the
Kato thick
chances of smear method
catching to increase
true intestinal the
parasitic laboratory must be regarded as confidential
infections. Food handlers are best screened using information between the laboratory and the
formalin-ether/ethyl acetate concentration
requesting physician. All laboratory requests
together with the results must be properly 
technique (FECT) than by direct fecal smear or  
modified  Kato thick smear method. Modified
modified koen plyt  bine  aaccloesg b
seodo bkyoar utahowr oizr ekdsh
 peeer tsownhnieclh.  Tcahne
Kinyoun stain may better demonstrate intestinal date of examination and reporting of results
coccidian infections. A clinical trial using  
new anthelminthics against soil-transmitted
should also be properly recorded. Qualifying
helminth or schistosome infections benefits
statements regarding the quality of specimen
such as “inadequately preserved when received
most from the use of Kato-Katz method that
allows quantitative diagnosis in terms of egg
in the laboratory” or “contaminated with water
and urine”
urine” should
 should also be noted.  
counts. Control programs for soil-transmitted
In the reporting of results, the complete
helminth and schistosome infections may utilize
name (i.e., genus and species) of the
th e parasite
Kato-Katz method to demonstrate baseline and
must be mentioned and specific stage/s (e.g.,
follow-up
follow- up parasitologic parameters
parameter s (Table
(Table 7.6).  
All the health center laboratories in Iloilo, ova, larvae, adults, cysts, trophozoites, etc.)
must also be indicated. The presence of
Philippines utilize direct fecal smear (DFS)
technique for parasitological diagnosis, while  Charcot-Leyden crystals (CLCs) and budding
yeast cells must be noted. CLCs indicate an 
ounselyo3f  .K 
7% er eltah bodr ,atK 
at of t hicekaltshmceeanr  tm or aiteos-K 
matdz e eosinophil response and are usually associated
method or FECT. with allergic or parasitic disease. There is no
common convention for the reporting units
Table 7.6. Recommended stool examination of CLCs. It is reasonable to report them on
techniques for specific situations    presence/absence
 presence/ab sence basis only.
o nly. Likewise,
Lik ewise, the
 presence of macrophages, eosinophils, and
 polymo rphonuclears
 polymorphonucl ears is important
import ant information
infor mation
for a clinician. Quantitative reporting of fecal 
leukocytes per high power field is  recommended
(WBC/HPF). However, caution must be taken
 because fecal leukocytes
leukocyt es could be mistaken for
amebae. 
Pitfalls in the Diagnosis of Parasitic Infections  
Overseas Filipino
Workers
L  bor ator y diagnosis of  par asitic inf ections
ys an im p
ofladisease.
 p Inothe t r ole in thethe
r tanPhilippines, ly detectionof
ear diagnosis
 parasitic infections
infectio ns is still much dependent on
the ova and parasite (O and P) examinations.
In some instances, artifacts such as fungal
spore, mite egg, plant cell, and pollen grain are
mistaken as parasite ova. Other artifacts like
 plant hair can be confused as helminth larvae.
Howell-Jolly bodies and nucleated red blood 
 

CHAPTER 7: Diagnostic Parasitology   357 

cells are sometimes misidentified as malaria  – 7.15).

7.8 – 7.15). These practices lead to inaccurate
 parasites. Fungal spores of  Helicosporium diagnosis of parasitic infections (false positives)
may also be mistaken as microfilariae  (Plates  and inappropriate treatment of patients.  

Plate 7.8. A fungal spore in a wet mount stool   Plate 7.9. A mite egg in a formalin-concentrated  
may look like a cyst of Entamoeba spp.  stool specimen may look like a hookworm egg.
(Accessed from 
from  www.dpd.cdc.gov/dpdx)  (Accessed from www.dpd.cdc.gov/dpdx)
from www.dpd.cdc.gov/dpdx) 

Plate 7.10. A plant cell in a concentrated wet Plate 7.11. A pollen grain in a concentrated wet
mount of stool may look like a helminth egg. mount of stool may look like a fertilized egg of
(Accessed from 
from  www.dpd.cdc.gov/dpdx)   Ascarislumbricoides . 
(Accessed from www.dpd.cdc.gov/dpdx)
from www.dpd.cdc.gov/dpdx) 
 

358   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Plate 7.12. Plant hair in a concentrated wet Plate 7.13. Howell-Jolly bodies in a thin blood
mount of stool may look like a hookworm or smear stained with Giemsa  
Strongyloides stercoralis larva.  may look like malaria parasites.
(Accessed from www.dpd.cdc.gov/dpdx)
from www.dpd.cdc.gov/dpdx)  (Accessed from www.dpd.cdc.gov/dpdx)
from www.dpd.cdc.gov/dpdx) 

Plate 7.14. A nucleated red blood cell Plate  7.15.  Fungal spor e s oH 
f ec  os or 
l i  p ma y be
i ummay
may look like a schizont of Plasmodiumspp.  mistaken as microfilariae in stained blood smears.
(Accessed from www.dpd.cdc.gov/dpdx)
from www.dpd.cdc.gov/dpdx)  (Accessed from www.dpd.cdc.gov/dpdx)
from www.dpd.cdc.gov/dpdx) 

Quality Assurance in Parasite Microscopy  differ in terms of basic training and skills.  
A physician, health manager, or a scientific
For many parasitic conditions as in
investigator should be assured of the quality
helminth infections and malaria, microscopic of the microscopic examination. On some
examination is still considered to be the “gold occasions, the requesting party may also be
 occasions, the requesting party may also be
standard” procedure. Microscopists, however, 
interested to know the burden of infection 

CHAPTER 7: Diagnostic Parasitology   359 

of the patient. This can be determined by •  Poorqualityof microscopy,particul

microscopy,particularly
arly
counting the number of parasite or parasite
p arasite at the peripheral level  
•

ova in a predetermined
reporting the intensity amount of sample,
as number and
of parasite/   Dif  cultiesin maintainingmicroscopy
facilities in good order  
ova per volume or weight of sample. In practice, •  Logistic problems and high costs of
quantification of
quantification  of malarial parasites in blood   maintaining adequate supplies and
is more commonly requested. The result is  equipment
reported as the number of malaria parasites per •  Lack of adequate
adequate training and
microliter of blood. Quantifying the parasites retraining of laboratory staff  
also helps in the assessment of the efficacy  •  Delays in providing results to clinical 
clinical  
of interventions (e.g., chemotherapy) in the staff  
control of specific parasitic infections.   •  Lack of qualit y assurance and
The reliability of results depends on the supervision of laboratory services 
ability of the microscopists to identify and count •  Inability to cope with the workload of
stages of the parasites. This can be assured by traditional systems for cross-checking
cross-checking of the same samples, whereby the
cross-checking of routinely taken malaria slides
reading of the initial microscopist is compared
to the reading of a reference microscopist.
microscopist. The These limitations can only be overcome
reference microscopist must be “blinded”
“blinded”  or  by new health policies that acknowledge  
must have no prior knowledge of the reading the importance of strengthening laboratory
of the initial microscopist.  services, the need for adequate funding, and the
implementation of a QA system. Such policies
 Foer dm
may b r yyt,hqr ouaglihty“ bcolintdr eodl ”
la bicor r oastco p
onaelair nia  m should ensure the following:  
cross-checking
cross-check ing of a minimum of 10 randomly •   Adequate staff and resources
selected slides (five reported as low-density, five •  Regular training and supervision of
reported as negative). This is done by a trained staff, and quality control of their tasks  
validator/cross-checker at the end of each •   Accurate and timely
timely slide collecti
collection,
on,
month. When the number of tests performed staining, and reading, linked to clinical
in one month is less than the minimum sample diagnosis
size, all slides must be cross-checked.   •  Reliable results quickly provided to
For the soil-transmitted helminth infections clinicians 
andschistosomiasis,allnegativeslidesand 10% •  Provision of logistic support for quality
of the positive
positiv e slides may be reread by areference supplies and equipment
microscopist. The main drawback of this
 procedure is that the technique
techniq ue may belaborious At present, a QA program designed by the
and not be feasible in many settings, such as  World Health Organization is used to assist 
in large-scale examination in surveillance and managers of national malaria control programs
monitoring of the impact of control programs.  aand laboratorymalaria
sustainable servicesmicroscopy
to develop and maintain 
QA program.
It has been difficult to maintain good
quality for malaria microscopy especially in This program outlines a hierarchical structure
 peripheral laboratories.
laborator ies. Current
Curren t challenges
challen ges in  based on re-training, validation, and the
malaria microscopy include:   development
developm ent of competency standards designed
to ensure the quality of diagnosis necessary for
•   Lack of politi cal commi tment a successful malaria program.  
to support the development and When validation of results is not feasible
expansion of laboratory services   through slide cross-checking, a certification 
certification  
 

360   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

scheme for microscopists may be considered. Department of Health. Department

Microscopists will initially undergo training to memorandum no. 2009-0086.

enhance theirtraining
An intensive basic knowledge on the parasites.
on microscopic diagnosis Implementation of external
assessment program quality
as a regulatory
of parasitic infections will provide basic requirement for licensing of clinical
competency, which will be assessed through laboratories. 2009. 
theoretical and practical examinations, the latter   Garcia LS, Bruckner DA. Diagnostic medical
using prepared control slides. Sensitivity and  parasitology.
 parasitolo gy. New York:
Yo rk: Elsevier;
Else vier; 1988.
19 88.  
specificity scores of the microscopists will be Kettelhut MM, Chiodini PL, Edwards H,
determined. A certificate  will then be awarded   Moody A. External quality assessment
to the microscopists who passed the theoretical schemes raise standards: evidence from
and the practical examinations administered by the UKNEQAS parasitology subschemes.
a panel of experts. After certification, possible J Clin Patho
Pathology.
logy. 2003;56:927 – 3 32.
2. 
questions on the veracity of results issued by the MMWR. Epidemiologic notes and reports
microscopist may be minimized. The certified  pseudo-outbreak
 pseudo-ou tbreak of intestinal
intestinal amebiasis — 
 —  
microscopists will also develop a higher level of California. 1985;34(9):125 – 6 6.. 
confidence in performance of their laboratory Montressor A, Crompton DW, Bundy DA,
work.  Hall A, Savioli L. Guidelines for evaluation
of soil-transmitted helminthiases and
References 
schistosomiasis at community level.  
Belizario VY. Quality assurance in laboratory   Geneva: World Health Organization;1998.
 plair caH
Cioagllnegoesios f oPf u b
d siteiacltihn,f eUcntiiovnesr silteyctouf r teh. e Par isdiLa.gnMoiscisr osf coi pnitsetstinaclc pur ar caysitionsitshaend  the
’

Philippines Manila; 2000.   current state of diagnostic parasitology

Belizario VY, Barcus M. Quality assurance laboratories of government hospitals and
in malaria microscopy lecture. Training main health centers in the province of
sponsored by US-NAMRU, DOH and Iloilo: Implications for standardization
UP-CPH. 2001. and quality improvement [dissertation].
Butler K, Guy R. Development of standards [Manila]: College of Public Health,
in malaria microscopy. World Health University of the Philippines Manila; 2005. 
Organization; 2002.  Shimizu RY. Parasitology. In: Garcia LS. Clinical
Center for Disease Control and Prevention, microbiology procedures handbook. 2nd
Division of Parasitic Diseases. Laboratory ed. Washington DC: ASM Press; 2007.  
identification of parasites of public health Tetraultt G. Clinical
Tetraul Clini cal laboratory
laboratory quality assurance
assu rance
concern. Image library: Artifacts [Internet]. in clinical laboratory diagnosis and
2011 [cited 2012 Mar 3]. Available from laboratory management. 20th ed. 2001. 
http://www.dpd.cdc.gov/dpdx/HTML/ UK NEQAS. Parasitology EQA scheme
ImageLibrary/AF/Artifacts/body_ [Internet]. 2007 [cited 2010 Jun 5].
Artifacts_il9.htm. Available from http://www.btinternet.
Cli
Cline
ne BL,Habi
BL, Habibb M, Gamil F,
F, Abdel-Aziz F,Litt
Little
le com/~ukneqas.parasitologyscheme  
MD. Quality control for parasitologic data. Vlad JL. Quality assessment and control in
Am J TropMed Hyg. 2000;62(2)S:14-6.
2000;6 2(2)S:14-6.  the research microbiology laboratory. Ann
De Leon WU. Pitfalls in the diagnosis of Fundeni Hosp. 2006;11(3 – 4):98
4):98 – 103.
103. 
 parasitic infections lecture. College of World Health Organization. Manual of basic
Public Health, University of the Philippines techniques for a health laboratory.
laboratory. Geneva:
Manila; 2000.  World Health Organization; 1980.  
 

CHAPTER 7: Diagnostic Parasitology   361 

WorldHealthOrganization Regional Office for

World  New Delhi:
Del hi: World Health Organization;
Organizat ion;
South-East Asia. Guidelines on standard
st andard 2003.

operating procedures
and parasitology. for microbiology
Geneva: World Health World Healthassurance
quality Organization. Malariamicroscopy
manual. Geneva: World
Organization; 2000.  Health Organization; 2008. 
World Health Organization Regional Office World Health Organization.
Organization. Laboratory quality
for South-East Asia. Quality assurance in management system (handbook). Geneva:
health laboratory services: a status report.  World Health Organization; 2011.
 

362   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

CHAPTER 8  

Special Topics in Parasitology 

lcseitdi o LZ. o
Par a
Sa c Edounaor dsoes 

and control measures of the causative agent are

Z   oonoses as defined
defined by
 by the World Health
Organization (WHO) are “those  diseases 
and infections which are naturally transmitted
dependent on the knowledge of its life cycle.
cy cle.
The groupings are presented in more detail with
 between vertebrate animals and humans.” examples and illustrations in succeeding parts
Zoonotic parasites therefore are protozoan, of this section. 
helminth, and arthropod agents transmitted
Parasitic Zoonoses 
 between these mentioned hosts. 
Zoonoses include a wide assemblage   Only zoonotic agents that have been
ofclinical
diseases with varied
features. Thus,epidemiological
attempts have beenand  reported in the Philippines, either in humans
or in animals or both, are considered in this  
made for their groupings. Zoonoses have section. These are arranged according to the
 been classified
classif ied based on
o n reservoir
reservoi r host of   life cycle of the agent. As majority of these are
the causative agent, whether humans or already presented in detail in other sections 
lower vertebrate animals. Those that are of this book, the information given here are
transmitted: to humans from lower vertebrates
vertebrates those of the animal hosts and the mode of
are anthropozoonoses, to lower vertebrates from transmission to humans. The assignment of
humans are zooan
 zooanthrop
thropozoon oses, and in either
ozoonoses some to a particular group (e.g., intestinal
direction and maintained in both humans capillariasis) is temporary until the life cycle in
and lower vertebrates are amphixenoses. This nature is exactly known.
known.  
classification however has caused confusion
 A. Direct Zoonoses  
and sometimes, has been used indiscriminately.
indiscriminately. 
A more acceptable classification  is that
classification is In this group are those infections that
of Schwabe in 1984, which is based on the are transmitted from an infected vertebrate
life cycle of the etiologic agent. The zoonoses  host to another vertebrate host by contact, 
ar e gr ou ped as f ollows:  (a) dir ect zo o oses,  f omite,  or  mechanical vector  with li tl or  no
(zaprozoon oonosThis
  bb)  cyclozoses.
zaprozoonoses. )  m etazoon is
es, (cclassification s,  and (d)
oseconvenient d mental change(Figure
evelo p transmission
during   in the 8.1).
causa tive  age t
for use for teaching purposes since prevention 

362 
 

CHAPTER 8: Special Topics in Parasitology   363 

2. Cryptospor idi 
osi 
s
 
A number of species of the genus
Cryptosporidium has been recorded but only
(definitivehost) Cryptosporidium parvum is known to cause
zoonotic infections. This species has been
recorded in a wide range of domestic and  

diiald
w rr haenaim
inallam o stas.ndItcaislvoesn.eInotf htehPehcilai pu pseisneosf ,
h b
Cryptosporidium has been recorded in cattle,
water buffaloes, pigs, and chickens.  
Human infection results from ingestion of
By Contact or through fomite or infective oocyst through contaminated food and
water from infected persons oranimals. Infection
is usually severe in immunocompromised
 persons. Human cases of cryptosporidiosis
Figure 8.1. Direct zoonoses
have been recorded in the Philippines both
1. Bal 
an tidi 
asi 
s
in urban and rural areas and in diarrheic and
  cancer patients, with a prevalence rate of 1.9%
The causative agent of this disease is in the latter.  
 Balantidium coli (Plate 8.1), which is a 3.  Amebi 
asi 
s
cosmopolitan parasite of pigs. Infection occurs 
cosmopolitan  
when cysts from feces of infected animals are d isease is caused by  Entamoeba
The disease
ingested through contaminated food and water. histolytica and human is its principal host.
Human infection is sporadic but common It is however widespread in non-human
among workers in piggery establishments.    primates. It is cosmopolitan
cosmopol itan in distribution
distri bution but 
more common in the tropics and subtropics,
especially in areas with low economic status
where poor hygienic conditions occur and favor
transmission. Food, especially raw vegetables
and fruits, as well as water contaminated
with cysts from feces are important sources of
infection. Transmission through infected food
handlers also exists. 
4. Gi 
ard a
i si 
s
 

Mor e than 50 s p
 pecies of the genus Giar d di  a
have been deas
recognized i bed but oincluding
scr distinct, rr ently
nly five ar e cuGiardia
duodenalis (also known as Giardia intestinalis
and G. lamblia). G. duodenalis affects human
and a wide host range of animals including
numerous mammalian species. Giardia is
highly prevalent in domesticated animals.  
Plate 8.1. Balantidiumcolfrom
i  pig
Fecal-oral transmission is common especially
(Courtesy of Dr. Salcedo Eduardo)  among inmates in institutions and prisons,  
 

364   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

and in animals in close confinement aggravated (one definitive and the other intermediate

i ntermediate hosts)
 by coprophagy.
coprophagy. Humans become infected  and no invertebrate hosts in the completion of
 by ing esting cysts
ingesting
transmission directly
d irectly through
or contaminated throug
foodhorfecal-oral
water.  the life cycle. Humans may be obligatory or
non-obligatory hosts. There are two subtypes. 
5. Scabi 
es(human)andmange(an imas
l ) Suby
tpe1:Humanasanob
blg
i 
i l atorydefi nit vehost(Fg
i  ure8.2)
 
Aside from Sarcoptes scabiei, Sarcoptes spp., 
and Demod ex spp. from other animals, as well
 Demodex
as  Notoed res cati of cats affect humans. These
 Notoedres These
mites are the cause of mange in animals. Lesions
are usually found on the hands and forearms  Man
of pet owners. Sarcoptes spp. from cattle, water (definitive host)
 buffaloes,, horses, pigs, and S. scabiei of human
 buffaloes
and Notoed res cati of cats have been recorded in
 Notoedres
the Philippines. 
6. Tromb icul 
i 
dos s
i
 
The mite family Trombiculidae
(chigger mites) is an assemblage of several
genera
are freewhose
living adults and nymphal
but whose stages  
larvae normally
Vertebrate
deinr dt s, cinausescintigvodr esr ,mantodsegsr .ouGnidven
adtwtaecllkinr go b
(intermediate
(intermediate host)
the opportunity, they will feed on human,
livestock, and poultry. In the Philippines,
the following trombiculid genera have been
recorded:  Eutrombicula ,  Leptotrombidium ,
stia , Schoengastiella , Trombicula,
 Neoschoengastia
 Neoschoenga Figure 8.2. Cyclozoonoses subtype 1:
human as an obligatory (definitive) host  
Toritrombicula, and Walchiella.
Walchiella.  
 Eutrombicula wichni is the cause of
1. Sarcocystosis
human trombiculidosis.  Leptotrombidium
akamushi is a known vector of scrub typhus Members of the genus, Sarcocystis, which
or tsutsugamushi disease in humans caused by has an obligatory prey-predator two-host cycle,
Orientia tsutsugamushi. Scrub typhus has been cause this condition. Asexual and sexual stages
reported in China, Japan, Southwest Pacific develop in the intermediate and definitive hosts, 
to Siberia, and Pakistan. Cases of human  respectively. Intermediate host becomesinfected
infestation in the Philippines have occurred through ingestion of oocysts in food and water
especially among
amon g soldiers
soldier s during World War
War II contaminated with feces of the definitive host. 
and cases of infestation in the navel and scrotum Definitive host becomes infected through
among children playing on areas where rat nests   ingestion of mature sarcocysts (Plate 8.2) from
abound. tissues of infected intermediate host.  
B. Cyclozoonoses 
Humans serve as definitive hosts for
two species, namely, Sarcocystis hominis and 
To this group belong those infectionswhose S. suihominis . Cattle and swine serve as the
causative agents require only vertebrate hosts  
 

CHAPTER 8: Special Topics in Parasitology   365 

Plate 8.2. Sarcocyst in sectioned esophageal

muscle of water buffalo  
(Courtesy of Dr. Salcedo Eduardo) Plate 8.3. Cysticercus cellulosae freed from
muscle of pig 
intermediate hosts, respectively. Humans can (Courtesy of Dr. Salcedo Eduardo)
also serve as accidental intermediate hosts 
of a number of species occurring in animals. Human cases of cysticercosis have been
Sarcocystis species have been reported from the reported in the Philippines and were diagnosed
muscles of, S.cattle
 fusiformis (S.),cruzi
levinei goats ), (water buffaloes (S. 
s), and
S. capracanis
capracani to be, or highly
animals, suggestive
cysticercosis of common
is more
T. solium. In
in  
swine (S. mieschieria
mieschieriana
na) in the Philippines. swine (1.67%) than
2. Tae niasis/Cystice r c osis 
in cattle (0.02%)
or water buffalo
Taenia solium and T. saginata asiatica are (0.03%).  
the causes of human taeniasis in the Philippines. Another
What was previously referred to in literature species that can
as Taenia saginata or Taenia saginata-like in cause taeniasis in
Taiwan, Korea, China, Thailand, Indonesia, humans is Taenia
and the Philippines is in fact Taenia saginata taeniaeformis , a
asiatica . Taenia solium requires pig as the common intestinal
intermediate host and the cysticerci (Plate tapeworm of
8.3) are found in the host’s
host’s muscles.
 muscles. The cats. Rodents and
true Taenia saginata requires cattle and water rabbits serve as
 buffaloes asintermediate
intermedi ate host and its cysticerci intermediate hosts
are also found in the muscles. Taenia saginata for the larval stage
asiatica, on the other hand, requires pig
p ig as Strobilocercus
the intermediate host and its cysticerci occur called
 fasciolaris (Plate
mainly in the liver. Examination of slaughtered 8.4), which is found
 pigs during
duri ng meat inspection
in spection should therefore in their liver. In the
include the liver and not only the muscles as is  Philippines, the 

currently practiced. Between the two species,T.  prevalence in rats Plate 8.4. Strobilocercus
Strobilocercus  
fasciolarisfreed from
 saginata
 saginata asiaticais more common thanT. solium.
asiatica may range from liver of field rat
The former species is endemic in Leyte with a 21.4% to as high as (Courtesy of  
 prevalence of 10%. 97.0%. Rice
R ice field  Dr. Salcedo Eduardo)
 

366   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

rats ( Rattus
 Rattus tan
tanezumi) examined in Bay, Laguna
ezumi contaminated food and water. Transplacenta
Transplacentall
revealed 37.4% infection with S. fasciolaris infection occurs when previously non-infected
(unpublished). Cats become
ingestion of infected infected
rat liver where thethrough
larva is hosts become
organism infected
multiplies during
in the pregnancy.
placenta The
and spreads
released in the intestine, attaches to the mucosa to the fetal tissues. Cats play an important role
to grow to maturity. Similarly, infection in in the transmission of T. gondii. The disease is
human can result from ingestion of raw or a major public health concern because of the 
improperly cooked liver of infected rodents. risk of transplacental transmission when cats (as
Although human infections with this species the source of infective oocysts) are in the same
have been reported in other parts of the world,   households with pregnant women. Oocysts are 
none has been recorded in the Philippines.   resistant to most disinfectants and can survive
Subtype2:Humanasanon-obii 
g
 l atory(op tiona
 ) lhost(Fi 
gure8.3)
up to two and a half years even in unfavorable
 
environmental conditions. In the Philippines,
serological surveys revealed prevalence rates to
 be as high as 52.7% in cats, and 19.0%, 8.1%,
1.9%, and 2.4%, in pigs, rats, water buffaloes,
Vertebrate  
and humans, respectively.  
Man
2. Echinococcosis/Hydatidosis
(definitive host)

The species
 granulosus involved
. The dog iscanids
and wild  Echinococcus
are the  
hoasm
inetfienstiitnivee.  M
d ts m ccaunr s,insetr hve
wahles,r eintchleudaidnuglths uom
as the intermediate host where the metacestode
( Echinococcu
 Echinococcuss or hydatid cyst) develops.  
Humans become infected by ingestion of the
egg from infected definitive hosts.  
Vertebrate
Man While the disease is common in other
 parts of Asia, there are only very few reports in
the Philippines. There is only one record of E.
 granul osus in a dog, one report of Echinoc
 granulosus  Echinococcus
occus
cyst in water buffalo, and a few cases of human
Figure 8.3. Cyclozoonoses subtype 2: human as hydatidosis. 
a non-obligatory (optional) host  
3.  Anisakiasis

1. Toxoplasmosis This condition is caused by the larval  

This disease, caused by Toxoplasma gondii, stages of anisakine nematodes persisting in
is widespread among warm-blooded animals, the alimentary canal or penetrating the tissues
including humans. Cats and other wild felids of humans after consuming raw or semi-raw
serve as the definitive hosts. Transmission infected fish. A variety of fish species acts  as 
occurs through the placenta and ingestion of intermediate/transport hosts for the larva
the infective forms found encysted in tissues (Plate 8.5), which mature to adult in warm-
(bradyzoites
(bradyzoit es or cystozoites) of infected animals  blooded marine mammals. Human cases of
or in cat feces (sporulated oocysts) by way of   anisakiasis have been reported in the Americas,
Americas,
Europe, and Japan. Each year, 1,000 cases are 
 

CHAPTER 8: Special Topics in Parasitology   367 

sushi, sashimi, etc.) are gaining acceptance

among Filipinos. It is possible that there may
have
in thebeen unreported
Philippines duehuman cases
to lack of anisakiasis
of awareness by
health workers. 
4. Capillariasis

The cycle of C. philippinensis in nature

has not been fully determined.
d etermined. Experimental
Experimental
evidence, however, points to fresh and brackish 
water  fishes as the sour ccees of  inf eecctio H 
n. y
 y p el eot r 
ri   s  s

bipartita has been found to be a natural

n atural source
of infection in Ilocos Sur. Other species of fish,
Plate 8.5. Anisakis
8.5. Anisakislarva
larva from fish
namely, Chonophorus melanocephalus (bukto,
(Courtesy of Dr. Salcedo Eduardo) biyang bato), Amba
 Ambassis
ssis miops (bagsang ),
miops ), Eleotr
 Eleotris
is
melanosoma (birut )),, Sicyopterus sp. (ipon), and
reported in Japan where consumption of raw reticula ta (guppy), found in endemic
 Poecilia reticulata
fish is common. While no human case has areas in Northern Luzon, have been successfully
 been reported so far in the Philippines,
Philippi nes, a wide infected experimentally. With the exception of  
range of fish
anisakine  species
larvae have8.1).
(Table beenThe
found to harbor
potential of    P.
andreticulat
reticulata
gravid , the
a H. restita
bipart areisoften
bipartita eatenrelished
especially uncookedin 
h nf ecitaiollny ninowthtehaPthmila p
r eant eis p
isugm esatnhesr ef oor ed,
 ipn pyiJna p tchoenr 
sauw sttaitoen.  Hou
m p f   m wayfisr hesuinltf ef cr otemd
tioi-nr am
r aawn oinr f secm
 preparations of raw and and semi-raw fish fish (e.g.,
 (e.g.,  with larvae. 

Table 8.1. Philippine fishes found harboring anisakine larvae (from various authors)

(aumahan)l

 Al 
ect s
i sp.(pampanongpu )t i Luj 
anusmaabarcus(maya-maya) il 
t Sardnea
l abea
 l (bagasbasi 
l 
) l

 Ambygasersrm(onsoy)tii l  Lu
 j 
tanusv tia(dayang
 -dayang) Sardine l 
lal 
ongiceps(ta
tamban) Apogonelo (i danga)ti l 
l 

  Mega a
l sps
icordya
l (orl e
i s) Sauridatumb
 l i(k
ka
alaso) Caesolu nars(daagangbukdi 
l 
) i

  Menemacu lat 
e(h iwas) Scatophagusa
 rgus(kaa
 lso)

 
(taningue)

Caranxsp.(talakitok) Nemipterussp.(bisugo)  

Decapt erussp.(ga lunggong) Ooh
i esru ber(aakaak)t 
ltl  Selaroidesleptolepis(salaysalay)

Oxyuricthysmicrolepis(talimusak) Siganussp.(samaral)
(mamali)

Epinephelussp.(lapu-lapu) Pennahiaaenea(alakaak)   Stolephorussp.(dilis)

Euthynnusaffinis(kutsarita) Pinjalopinjalo(sulid) Sypnaturasorsogonensis(dapa)

Gerresfilamentosus(malakapas) Poecilialatipinna(bubuntis) Sphyraenalangsar(tursilyo)

Lactariuslactarius(pagapa) Priacanthustayenus(bisugongtsina) Teraponjarbua(bagaong)  

Leiognathusequulus(lawaya kan) Psettodeserumei(dapa) Trichiuruslepturus(espada)
 

368   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 
Fish-eating birds are believed to be
the natural host and are responsible for  
disseminating
 path. infection
Experimental
Experimental studiesalong
showtheir
showed migratory
ed susceptibility
of some birds to infection with the parasite. In
the Philippines, Ixobrychus
 Ixobrychussp. (bittern) has been
found to harbor a male specimen of the parasite. 
Other species of fish may be more commonly
infected. Autoinfection is a part of the cycle in
mammals as evidenced by embryonated eggs 
and larvae produced by female worms.  
C. Metazoonoses 

This group includes those infections whose

causative agents are transmitted biologically
b iologically
or cyclically by invertebrates, which serve  
as intermediate hosts and where the agent
multiplies. There are three subtypes.  
Subtype1:Onevertebratehost(de fini 
tiv ehost) andonei 
nvertebratehostn
( itermeda
 i tehost)
(Fg
i ure8.4)

Plate  8.6.  F 

asci o l ag 
c  aand F 
i c 
i gant   epac 
.h p i t a 
Vertebrate
Man from water buffalo
(Courtesy of Dr. Salcedo Eduardo)
(definitive host)

Philippines but recent investigations based on

 previou s and current collections
 previous collection s have shown
that the former is the predominant if not the
only species now occurring in the country. The
 prevalence of  Fasciola infection in domestic
 Fasciola
ruminants is estimated at 45%, but in endemic
(Intermediate Host) areas, it may reach as high as 95%. The snail  
 Lymnaea
 Lymna ea
 philippinens
 philip pinensis
is and in this country are
intermediate hosts  L. auricularia rubiginos
rubiginosaa , 
which are likewise distributed throughout the
Figure 8.4. Metazoonoses subtype 1: one islands. Animals become infected through the
vertebrate host (definitive) and one invertebrate
host (intermediate)  
ingestion of metacercariae (Plate 8.7) encysted
on grass and other water plants, or drinking
1. Fascioliasis (also a zaprozoonoses)
contaminated water. 
From literature, cases of human fascioliasis,
Two species, Fasciola
 Fasciola giganticaand
giganticaand F. hepatica
hepatica   recognized as an emerging human infection,
(Plate 8.6), have been reported in animals in the
t he  have been increasing especially in developing  
 

CHAPTER 8: Special Topics in Parasitology   369 

levels of transmission
 between humans and
dogs. Infection is
through penetration of
the skin by the cercaria
(Plate 8.8) when the
host comes in ccontact
ontact 
with infected water.
3. Dipylidiasis

 Di pyl id iu m
caninum (Plate 8.9)
infection is common in
dogs and cats worldwide.
In the Philippines, the
Plate 8.7. Fasciola metacercaria  prevalencerate especially Plate 8.8.
(Courtesy of Dr. Salcedo Eduardo)   among stray dogs may Schistosoma
range from 5 to 81%. cercaria
(Courtesy of
The cat (Ctenocephalides Dr. Salcedo
countries. It has been estimated that 2.4
million people are infected with this trematode  fe l i s ) and dog flea Eduardo) 
and another 180 million are at risk.
r isk. In the
Philippines, only two cases of human
hu man infection
with Fasciola have been recorded. The exact
srcin of the infection could not be traced but
bu t
it probably resulted from the partly cooked
edible water plant, Ipomea (kangkong ) or the
accidental ingestion of other water plants
harboring metacercariae
metacercariae of the fluke. The high
 prevalence in animals in endemic areas puts the
local human population at risk to infection.  
2. Schistosomiasis

Schistosoma japonicumis the only species of

the genus which causes human schistosomiasis
in the Philippines. It is endemic in Sorsogon, 

Mindoro,
The amphibious
serves Leyte,
as its Samar,
snail, Oncomelania
Bohol,
intermediate host and Mindanao.
in the
quadrasi, 
country.
country.
A variety of domestic and wild animals serves
as important reservoir hosts. Recent studies in
an endemic area (Samar) in the Philippines,
revealed infection in dogs, rats, cats, pigs,
and water buffaloes with high prevalence 

and intensities of infection in dogs and rats. Plate 8.9. Dipylidiumcaninumfrom dog
 A study in the same province suggested high  (Courtesy of Dr. Salcedo Eduardo)  

370   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

(Ctenocephalides canis ), and the dog louse In the Philippines, land snails ( Achatina
 Achatina fulica,
fulica
( Heterodoxus
 Heterodoxus llon
ongit
gitarsuss) serve as intermediate
arsu  Hemiplecta
 Hemipl ecta sagittifera,  Helicos
sagittifera  Helicostyla
tyla macrosto ma,
macrostoma
hosts that harbor the cysticercoid stage. Chlorea fibula, and Cyclophorus spp.), garden
Chlorea fibula
Humans, especially children, become infected slugs ( Imerina plebeia, Laevicaulus alte) serve
when fleas and lice containing cysticercoid are as primary intermediate hosts of the parasite.
parasite.
accidentally ingested.  In the rice field,
field,  A.
  fulica and other snails have
 been observed to be important
import ant sources of food  
4. Hymenolepiasis of rodents and especially when grains become
Two s  ppecies with cosmo politan dist b
i brr   ution, scarce. This snail and infected rats contributed
 Hymenolepis nana (previously known as
 Hymenolepis to the spread and its introduction to many
Vampirolepis nanaand also known as the dwarf regions of the world.  
tapeworm) and H. diminuta are involved in Humans are accidental hosts. Infection
this infection. The adult form occurs in rats results from ingestion of infective larvae
and humans. Completion of their life cycle frequently through the paratenic hosts (e.g.,
requires intermediate hosts, but for H. nana, fresh water prawns) which are eaten raw
this is optional. Intermediate hosts include and whose juices are used in the preparation
flour beetles, and other arthropods where of local dishes, or ingestion of vegetables
v egetables 
the metacestode (cysticercoid) is formed.  H. contaminated with larvae from infected obligate
diminuta is widely distributed among rats with intermediate hosts. Parastrongylosis in humans
a prevalence
 prevalence rateHuman
is 1%. of 10.8%. In humans,
infection the  
results from affects the larvae
migrating centralcause
nervous system where
a condition calledthe
 

mceodoikateed hf  oostds cor nthaemir inaactceidewnitahl
inf gecsteiodninotf eur n tinr oc pluicdailnegocsainseo p laer n pinar gaisttisr .oH
s ohf iloicum asheisc, h
loasnis,cw
nguym
ingestion. The infection is prevalent among are all non-fatal and presumably due to larvae of  
children.   P. cantonensis, have been reported locally.
5. Raillietiniasis 7. Dirofilariasis/Human
Dirofilariasis/Human Pulmonary Dirofilariasis
Dirofilariasis

The genus Railli etina is well represented in

 Raillietina immitis (Plate 8.10), the
 Dirofilaria immitis
domestic and wild birds in the Philippines with heartworm of dogs, is common and widely
at least 19 species reported. Only one species,   distributed in dogs in the Philippines and
 R. madag
madagascar iensis, also known as R. garrisoni
ascariensis garrisoni, transmitted by mosquitoes. Latest data showed
sho wed
has been involved in human infection, and its an incidence rate of 20% among client owned
 prevalence rate among rodents may range from dogs from the Greater Metropolitan Manila.
22% to as high as 86%. It has been shown that The dog therefore is an important source for
 beetles and ants serve as intermediate hosts. human infection through the bites of infected
Human infection results from ingestion of the  mosquitoes.
intermediate host infected with cysticercoid.   Human infection with this species usually
6. Parastro ngylo sis or Eosin ophili c
involves the lungs, thus the term pulmonary
Meningoencephalitis dirofilariasis. However, the involvementof other
organs such as the eye, posterior vena cava,  
 Parastrong
 Parastrongylus
ylus ccantonensis is the cause
antonensis abdominalcavity,spermatic
spermaticcord, andpossibly
of the condition and the only species of the the meninges has been reported. Although no
genus reported in the Philippines. This species human case so far has been reported in the
occurs as adults in the lungs of rats (  Rattus Philippines, several cases have been recorded in
spp.) with prevalence ranging from 3 to 10%.
1 0%.  Australia, Japan, Spain, and the United States.
States. 
 

CHAPTER 8: Special Topics in Parasitology   371 

of the infective larva by the insect vector feeding

on eye secretions.  
9.  Acanthocephalosis(Macracanthorhyncho
 Acanthocephalosis(Macracanthorhynchosis
sis
and Moniliformosis) 

Two species of acanthocephala of animals

can cause this condition in humans. These  
are Macracanthorhync hus hirudinaceus (Plate
 Macracanthorhynchus
8.11) of pigs and Moniliformis moniliformis
of rats, which are common in the tropics and
subtropics. In the Philippines, both species are
 present. The former is more common among
among
free-roaming backyard-raised pigs than those
raised in commercial farms. The latter species is
common in both field and laboratory rats. May
 beetles,  Phyllo
 Phyllophaga
phaga rugosa , and cockroaches
rugosa
serve as the intermediate host for the former
and the latter, respectively. Cases of human
infection have been reported in other countries
resulting from accidental ingestion of infected
intermediate host, but no case has been recorded 
Plate 8.10. Dirofilariaimmitisfrom dog
(Courtesy of Dr. Salcedo Eduardo) so far in the Philippines.  

8. Cutaneous Parafilariasis in Animals/Ocular

Parafilariasis in Humans

 Parafilaria bovicola , a nematode, is the

causative agent of this condition. First reported
in cattle in the Philippines causing hemorrhagic
cutaneous lesions, it occurs now in other parts
of Asia, Africa, and parts of Europe affecting
cattle and water buffaloes ( Bubalus bubalis).
In the Philippines, 3% of water buffaloes have
 been found infected with this species. Flies of
the genus Muscaspp. have been incriminated as
vectors. Flies become infected by feeding on the
 bleeding sores and
eggs or larvae, of infected ani mals
animals
eventually containin
containing
develop into theg
infective larvae. Flies introduce infective larvae
to the same or another animal by feeding on
wounds or ocular secretions.  
The first human infection with this species
has recently been reported in Thailand, the
worm infecting the eye of a 72-year old man. Plate 8.11. Macracanthorhynchushirudinaceus
Macracanthorhynchushirudinaceus  
Infection probably resulted from introduction   from pig (Courtesy of Dr. Salcedo Eduardo)
 

372   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Sub
 py e 2: M 
t  or e t 
han one n er 
e ae
t  hostt   i f 
t br 
i v  st 
r 
(   nd sec 
ta ond n er 
med 
ii  t  eho )st 
i t 
a t and one conica. Filipinos eat the
vertebratehost(Fg iure8.5) latter species, which is
  considered the primary
source of infection. The
Ilocanos of Northern
Luzon are known to
consume partly cooked 
(definitive host)  Pila conica(locally called
bisukol ),
), hence human
infection is highest in
this region. 
 Ech ino sto ma
lindoense (Plate 8.12)
is another cause of
(1st Intermediate
Intermediate
Host)
human intestinal
echinostomiasis. It has
 been first described
Figure 8.5. Metazoonoses subtype 2: more and reported as a
than one invertebrate host (first and second
intermediate hosts) and one vertebrate host  
human infection in

Indonesia and later

other Southeast Asianin 
1. Echinostomiasis Plate 8.12. Ech inostoma
onheasiila,nd)
cMoualnatyr siieas, (aIndT lindoensefromfiel
fi eld
d rat
Human echinostomiasis in the Philippines (Courtesy of Dr. 
is caused by Echinostoma ilocanum. The adult and Brazil in both Salcedo Eduardo) 
fluke is found in the small intestines, thus animals and humans.
the disease condition
condition is also called intestinal  It has recently been
recorded in rice field rats 

echinostomiasis. It is widespread with a in the Philippines, although no human case has 

 prevalence of 3%, but it is more commonly  been reported lo
loca
calllly.
y. The life cycle of this species
found in Northern Luzon where prevalence follows the same pattern as that of Echino
 Echinostom
stomaa
reached as high as 44%.   ilocanum and  Artyfechinostomu
 Artyfechinostomumm malayanum ,
 Rattus spp. are important animal hosts  but in addition,
additio n, daughter sporocyst is produced.
produced .
 but dogs and cats may equally be important. The first intermediate hosts are freshwater snails:
However,r, no data are availableon the
Howeve t he prevalence
prevale nce Gyraulus convexiusculus and G. sarasinorum .
of natural infection especially on the last two The second intermediate hosts are snails
hosts. A variety of laboratory animals
animals especially (Gyraulus convexiusculus, Lymnaea rubiginosa, 
rats, mice, and hamsters are the most susceptible exustus, and Biomp
 L. exustus  Biomphalar
halaria
ia glabrata), mussels 
glabrata mussels 
experimental hosts.  (Corbicula lindoensis , C. subplanata ), and
 E. ilocanum requires fresh water snails as tadpoles ( Rhacop
 Rhacophorus leucomystax ). The
horus leucomystax
intermediate host to complete its life cycle. intermediate hosts in the Philippines are not
Locally,the
Locally,t he freshwater planorbidsnail, Gyraulus yet known but Gyraulus and Lymnaea abound
 phrasadii serves as the first intermediate host. The
 phrasad in the country. Human infection results from  
second intermediate hosts include a variety of ingestion of viable metacercaria contained in
freshwater snails including G. phrasadi and Pila  the second intermediate hosts. 
 

CHAPTER 8: Special Topics in Parasitology   373 

2.  Artyfechinostomosi
 Artyfechinostomosis
s

 Artyfechinos
 Artyfechinostomum
tomum m
malayanum is
alayanum the cause
of this condition and it is found in the intestines
of the infected host. This species is distributed
in many East Asian countries, as well as in the
Philippines. Pigs, rice field rats, and a monkey  
inaf vec btieoens  f woiutnhdthniastus  ppr aeclliyesinhf aevcete bde, ean  dr e p
h r taend
huom
from Isabela
Isabel a and Tarlac
Tarlacprovinces in Luzon, and
recently in Siargao Island, Surigao del Norte in
Mindanao. 
This species requires freshwater snails as
intermediate hosts to complete its development.
The snails,  Bu ra cumin g iana,  R
Bulla t ra  s  Rad i  x  ra i,
x quad ra  s

and Physastra hungerfordiana
hunge rfordiana are naturally
infected in the Philippines and therefore serve
as the second intermediate host. The source of
human infection, however, is  B. cumingiana ,
which is eaten by some Filipinos. All human
cases in Isabela had a history of eating  B.
cumingiana , which is locally known as birabid .  Plate  8.13.  E ema
ur 
r 
t 
y  panc 
ap r  i t um f r r om c attle
eac 
(Courtesy of Dr. Salcedo Eduardo)  
3. Carneophallosis

Carneophallus brevicaeca is the etiologic  buffaloe s, sheep). The prevalence of

 buffaloes, o f the first
agent for this condition. In the Philippines, it has three species in cattle and water buffaloes
 been reported in birds (Sterna albifrons sinensis), locally is 11.4%, 2.6%, 4%, and 5.3%, 0.66%,
fish (Glossog
Glossogobius giuriss), and in humans where it
obiusgiuri 1.33%, respectively. The first three species
is particularly associated with lesions in the heart occur in the pancreas, while the last species in
and spinal cord. Snails serve as first intermediate the perirectal fat in sheep. This group requires
hosts, while shrimps ( Macro
 Macrobrach ium sp.) have
brachium two intermediate hosts: land snails (first),
 been found to harbor metacercariae thus serving and grasshoppers and crickets (second). The
as second intermediate hosts for the parasite. second intermediate hosts contain the infective
Infection occurs through ingestion of raw or metacercarial stage. 
 partly cooked shrimps. Other invertebrate Grasshoppers and crickets are among
intermediateandvertebrate definitive hosts still  the many insects eaten in many parts of the 

wohr  aallllr yedtr uine iHuman
hesise ias r esper ce p
elrr de  . tThsources an vAaf riectayinfection
aonf dwAasyiiaas
ofiprotein.
remain
4. to be known.
Eurytremiasis
as good
Members of the genus Eurytrema are the results from ingestion of grasshoppers and
etiologic agents of this condition which are crickets containing live metacercariae of the
 parasites of ruminants.
ruminant s. Four species
s pecies namely    Eurytrema. T
 Eurytrema Two
wo cases of human infection
infectio n with  
 E. pancreaticum (Plate 8.13), E. coelomaticu m , 
coelomaticum  E. pancreaticum have been recorded in Japan.
 E. escuderoi , and  E. ovis have been recorded  No human infection
inf ection with
wit h Eurytrema so far has
 Eurytrema
in Philippine ruminants (cattle, goats, water    been reported in the Philippines. 
 

374   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

5. Paragonimiasis

Members of the genus  Paragonimus

are responsible for this condition. In the
Philippines, it is  Paragonimus westermani
wester mani
 filipinus . Paragonimus infection is endemic in
certain areas in the Philippines and most human  
f ceaw ther r e p
sesow vinScoer s oingoM
 f  rom n,iSnadm
anaar o, .LePyr tev,aalendcea
in endemic areas may reach 4.6 to 12.5%.
Rats, dogs, and cats serve as reservoir hosts but
the foremost may play an important role in
maintaining the cycle in nature.
n ature. The prevalence
in rats may reach 9.4 to 11.1%.  
This species requires freshwater snails and
crabs as first
first and
 and second intermediate hosts,
respectively, to complete its cycle. Wild boars
may serve as paratenic host. In the Philippines, Plate 8.14. Philophthalmusgraflir om du
duck
ck
the snails, Antem
 Antemelania
elania asperata and A. dactylus
asperata dactylus, (Courtesy of Dr. Salcedo Eduardo)  
and the mountain crab, Sundathelphusa
 philip
 philippina, serve as first and second intermediate
pina cercaria in water released by infected snail
hosts, respectively.  intermediate hostduring bathing in areas where  
Human infection results from consumption these snails abound, or when washing the face
of infected crabs, raw or partly cooked. In with contaminated water.
endemic areas, inhabitants are known to
7. Plagiorchiosis
consume crabs raw. A preparation with fresh  
crab juice known as kinagang is considered a rchis species
 Plagiorchis
 Plagio are the causes of this
local delicacy in the Bicol Region.  condition especially those occurring in rats,
6. Philophthalmosis
which serve as definitive hosts in nature.  
The species involved are  Plagi
 Plagiorchis
orchis muris,  P
muris  P.. 
Members of the genus  Philophthalmus  philippinen
 philip sis (Plate 8.15), and  P. potamo
pinensis potamoni
nide .s 
de  s
are responsible for this condition. Birds and All three species have been recorded in rats in 
mammals are hosts to a number of species of the Philippines with prevalence rates of 0.42 to 
 Philophthal
 Philop musinhabiting the eyes (conjunctiva
hthalmus 6.86%, 1.27%, and
an d 6.86 to 14.5%,
14.5%, respectivel
respectively.
y. 
under the nictitating membrane) of their Human infection occurs from accidental
host. Three species namely: Philophthalmus
 Philophthalmus   ingestion of the second intermediate host  
 pal  pebr ar um,  P .  g r al l i, and  P . l u z onen si s have
 beenHuman
r ecor dedinfections i  pines. 
 in avian hosts in the Phil p
with  Philophthalmus (ireported nsetcatcsear ncd
naqf f eucattiviceim
as infective
s.t pcheial in
ar ciiaar ru .  P 
P 
toahumans
  p sp)icnoentai inwiansgfitr 
p  p
 s  s

before it was
hset
have been reported in various parts of the reported in rice field
field rats
 rats locally. For P. muris
muris,
world and the species involved were those cases of human infection have beenb een reported
found in birds as follows: P. gralli(Plate 8.14)  ,,  in Japan and Korea, but no human case so far
lucipetu s, and  P. lacrymosus
 P. lucipetus lacrym osus . One case of for this species and P. potamonides have been
human infection (with P. gra llii) so far has been
grall reported in the Philippines. The potential risk of
recorded in the Philippines. Humans become human infection with the latter species remains
accidentally infected through the eyes with   high because its metacercariae have been found  
 

CHAPTER 8: Special Topics in Parasitology   375 

1. Heterophyidiasis

Members of the trematode family

Heterophyidae are the causes of this condition.
In the Philippines, infection by several species of
the family has been recorded in carnivores and
 birds. Many of these species are known to be 
tr aa p
 H  or icshsii b
nsl m leaitcohhuiu,m
 s t 
a.n ys .ok 
 H  Foo g uar ws paie,c P 
ier so, cnear m y,
oveulm
calderoni , and Stellanthchasmus falcatus , also
known as S. pseudocirrata, have actually been
recorded in human infections locally, and
these were associated with lesions in the heart,
 brain, and spinal cord. Unspecified heterophyid
infections of humans detected through fecal
examination have also been reported.
There are no data available yet on the
Plate 8.15. Pa
l go
i rchsi ph
 p
 ii 
l 
l pi 
nenssi from ra
ratt  prevalence of infection in animals. In humans,
(Courtesy of Dr. Salcedo Eduardo) less than 1% of 3,000 stool samples examined
from various places in the country were found
in the same crab which serve as intermediate  positive for heterophyid ova. In Mindanao,
however, ahigh prevalence rate of 36% has been 
host for Parag
 Paragonimus
onimus westermanii in the country. 
westerman reported for  H. taichui.
Subtype 3: One invertebrate host (2nd   Heterophyids require freshwater snails and
n
i termeda i tehost)andtwovertebratehosts(one
ne defn
i ti v
vehos
ehost and the other as
fishes as
fishes  as first
first and
 and second intermediate hosts,
1stin termeda  i tehost)(Fg
 i ure8.6)
respectively, to complete their cycle. A variety of
  freshwater and marine fishes, have been found
infected with the metacercariae of heterophyid
species. Philippine fishes found infected with
Vertebrate
heterophyid metacercariae are enumerated in
Man Table 8.2. Infection therefore occurs when
(definitive host) raw or partly cooked fish containing the
metacercaria are consumed. The life cycle of
only two species, H. taichui and P.
 P.calderoni are
known in the Philippines. The snail hosts are
 Melaniajuncea and Thiar
Thiara riquettii, respectively. 
a riquett
Vertebrate 2. Opisthorchiasis

Opisthorchis (Clonorchis )  sinensis , the

etiologic agent of this condition, has been
reported in humans in the Philippines during
routine stool examination. In a survey of 30,000
Figure 8.6. Metazoonoses subtype 3: one
Filipinos, ova similar to that of Opisthorchis
invertebrate host (intermediate) and two
invertebrate hosts (one definitive and one  sinensis were detected in 135 stool samples.
intermediate)   This parasite requires snails and a variety of
freshwater fishes as intermediate hosts, but for  
 

376   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Table 8.2. Philippine fishes found harboring metacercariae of heterophyid species  

species* species*
 Acentrogobiusjanthinopterus PC Lizasubviridis (banak ) HT, HY, PC, SF
(biyangsapa ) Mugildussumieri (talilong )
 Ambasslsburuensis (lañgaray ) PYC
H ,  Mugil sp.
sp. (banak )  SC
PHFY,,  

estud 
 Anabast  i neus (mar i o) 
i n
t k  CF,  
PS eoc 
Or  omi snl i oi t 
hr  c  us(l i a
t pi a)  HT 

i usmane
 Ar  i l nsi i  (M 
ana
i l  k 
and 
ul i )  HY 
HY  el ae
P  neat 
t squad 
i l r  us(agaak 
)  Y,CS,F 
HP

 Athei r  ensii  (g 
nabal abac  uno)  PC l at 
P   ephal usi nd 
c 
y  p us(sunog 
i c  )  PC

Butisamboinensis (biyangsunog ) PC Poecilialatipinna (bubuntis) PC

Channastriata ( dalag )   ,C
TY
HP ,  P usbi not 
uni t  at 
us p
( ai 
t 
)  HT 

Chanoschanos (bangus ) PC Rhynchorhamphusgeorgii (buging ) HPY,C  

Clarias batrachus(hito) HY 

HY  Scatophagus argus(kitang ) PC

Eleutheronematetradactylum (mamali )  PC Siganuscanaliculatus(barangan ) HPYC

, 

Epinepheluscorallicola (lapu-lapu ) T,C  

HP Siganusgutatus (barangan ) HHYT,

Gere ament 
r  sl i f  osus (mal ak 
apas)  PC Siganusjavus(barangan ) CY,  
PH

Gere
r  s k 
appas(mal ak 
apas)  HY 
HY  Spratellicypispalata ( manobud )   HT 

Glossogobiusgiuris (biya) PC Teraponjarbua (bagaong )  HHTS,YF,

species involved in the Philippines, intermediate  persons examined

examined
hosts are not yet known. Data on animal
anim al host in various places
infection, especially in carnivores, are still in the Philippines.  
needed. Human infection results from ingestion Prior to
of live metacercariae from infected fish.  1963, only four
human cases of
3. Spirometrosis/Sparganosis
sparganosis have
Spirometra species and their spargana have  been reported
 been reported in animals in the Philippines. locally and since
Sparganum (Plate 8.16) is widespread in then, no other case
tadpoles and frogs and has been found in a has been reported.
 bird ( Ixobrychus
 Ixobrychus cinnamomeus), a lizard (Gecko
cinnamomeus As all cases gave no
 gecko), and several species of snake ( Lapem
 Lapemis
is history of having
hardwickii ,  Boiga dendrophila , Ah ae
aetul
tul la
la   eaten fresh meat 
ahaetulla, A. caud
caudoli
olineata, and Natrix chr
neata chrysa
ysarga). 
rga
Adult  Diphyllobothrium latu
latumm has been  and birds,reptiles,
of frogs, or used 
reported locally from a boy who died of anemia. them as poultices,
Since D. latum is only found in temperate the mode of
countries of the Northern Hemisphere, this transmission was
identification is doubtful. It is possible that attributed to the
the species in question is Spirometra erinacei Plate 8.16. Sparganum of drinking water
Spirometrafrom muscle
musc le of frog
fro g
or S. mansonoides . Stool survey showed (Courtesy of Dr. Salcedo
with infected
diphyllobothrid ova in less than 1% of 30,000  Eduardo)  copepods. 
 

CHAPTER 8: Special Topics in Parasitology   377 

4. Gnathostomiasis human gnathostomiasis have been reported

in China, Japan, and Thailand due
d ue to these
Members of the genus Gnathostoma cause
this condition. The genus is represented in two species. Gnathostoma doloresi is currently
recognized as an important cause of clinical
the Philippines by three species namely, G.
human gnathostomiasis
gnathostom iasis in Japan. 
 spini
 spinigerum, G. hispidum, and G. doloresi. All three
gerum
Cases of human gnathostomiasis due to  
species have been recorded in humans in other  
G. hispidum in Japan have been attributed
r Ae psiaonr tceoduintr hiuesm
 bauntsolnolcyaGlly. .  ppGnathostoma
 s ini ger u
umm has b
  s pe pen
., to the consumption of the fish,  Misgurnus
anguillicaudatus . It is interesting to note that
in order to complete their development, require this fish
fish now
 now abounds in the rice terraces of  
aquatic copepods and fishes
fishes as
 as intermediate
hosts, and a wide range of paratenic hosts may Ifugao. The Ifugao call it jojo, which probably
is derived from the Japanese name dojo for
intervene as “extension
“extension  host”
host” in
 in the cycle. 
the fish.
fish. How
 How the fish
fish found
 found its way to the
G. spinigerum has been reported locally
Cordillera is not exactly known. It is postulated
in dogs, cats, flying
flying lemurs,
 lemurs, and palm civets.
however that Japanese soldiers during World
Copepods ( Cyclops serrulatus , C. bicolor )
War II brought it as a protein supplement for
and freshwater fishes ( Glossogobius giuru s,
their diet. This is a case of the introduction of
Ophicephalus striatus , Therapon argenteus )
serve as first
first and
 and second intermediate hosts,
a new suitable intermediate host for a parasite
respectively. Water snakes ( Hurria rynchop
rynchopss )
already existing in a country. The introduction
and frogs ( Rana limnocharis ) may serve as the increased thelocally
host available range of
andsuitable intermediate
hence ensured further  
 paratenic hosts locall
locally.
y.
Both G. hispidum and G. doloresi (Plate  p iteincaotniocner aned. continued  sur vival  of   the
diasr saesm
8.17) have been recorded in pigs in the In Japan, wild boars, salamanders, frogs, 
Philippines, but no case of human infection and snakes have been reported to harbor larvae
has been reported locally. However, cases of   of G. doloresi. In the Philippines, the larvae
(Plate 8.18) of G. doloresi have been found in 

Plate 8.17. Gnathostomadol oresi from pig Plate 8.18. Gnathostoma larva from frog muscle
(Courtesy of Dr. Salcedo Eduardo)   (Courtesy of Dr. Salcedo Eduardo)  
 

378   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

frogs and Ophicephalus striatus (dalag ) from A number of animal hookworms ( Ancylo
 Ancylostoma
stoma
Laguna Lake, suggesting that this fish serves as braziliense , A. canin um , and  Bunostomum
the intermediate host. spp.) and threadworms ( Strongyloides spp.)
Human infection may result from are involved in cutaneous larva migrans. The
consumption of improperly cooked infected first two species occur in dogs and cats, while
fish or paratenic host, or through drinking water the third occurs in ruminants. Threadworms
contaminated with infected copepods. The larva   are common intestinal parasites of mammals 
migrates to the subcutaneous tissues, central including humans, and many of the nonhuman
nervous system, and other tissues.   species can cause larva migrans in humans. A.
D. Zaprozoonoses 
braziliense is the cause of creeping eruption.
Human acquires the infection through contact  
In this group, the causative agent of the with soil containing infective larvae. Normally
infection develops from a non-infective to an larvae are restricted to and die in the skin but
infective stage in an environment containing may also migrate to the lungs. 
organic matter including food, soil, or plant, or Toxocara canis(Plate 8.19), a common dog
a reservoir before transmission to the vertebrate  Ascaris is the main causative agent of visceral,
 Ascaris
host (Figure 8.7).  ocular, and even
e ven cover
covertt larva migrans in
i n human.
Other ascarids like T. cati of cats and other
felids, and T. vitulorum of cattle and water

 buffaloes
 buffaloe s may
is limited alsothebeinfrequency
due to involved, butoftheir
thei r role 
human
Vertebrate
Man
ct.  wcaitnhi  tahseier ar elgygsa.s  Pthu pp
cwointhtaT   s e f ietsalasr teaginef eocr teadt
(definitive host)  birth due to transplacental
transplac ental and transmammary
transmission from the infected bitch, and

Figure 8.7. Zaprozoonos

Zaprozoonoses
es

1. Larva migrans

This condition is caused by a wide range of

nematode parasites of animals, the larva of which
may invade skin (cutaneous larva migrans),
viscera, and other organs (visceral larva migrans) Plate 8.19. Toxacaracanis from dog
of human, where they do not normally
norm ally mature.  (Courtesy of Dr. Salcedo Eduardo)  
 

CHAPTER 8: Special Topics in Parasitology   379 

are therefore the important source of eggs.

Female T. canis are highly fecund and infected
 puppies may shed 100,000 eggs per gram of
feces. Human becomes infected by ingestion
of embryonated eggs (Plate 8.20) through
contaminated food and water. Larvae migrate
to all parts of the body including the eyes and  
 brain. Other mammals and birds may serve as
 paratenic hosts. All the above species are present
in the Philippines.  Plate 8.21. Mammomonogamus a
l ryngeus in copula
from water buffalo  
(Courtesy of Dr. Salcedo Eduardo)

of human infections have been recorded from

the Caribbean Islands, Brazil, Korea, Thailand,
and the Philippines. 
The Role of Eating Habits and Practices in
the Transmission of Parasitic Zoonoses 

The important role played by food habits

and practices in the epidemiology of a number
of these zoonoses is evident from the above 
summary.  
Food dishes prepared as raw or partly  
cooked are relished in some areas in the
Philippines.  Kilawen is a term given to any
 preparation
 preparati on of raw meat, fish, snail, shrimp, or
crab, usually with salt, vinegar, and spices. This
Plate 8.20. Toxocaracanisembryonated egg
(infective) (Courtesy of Dr. Salcedo Eduardo) 
kind of preparation is considered a delicacy in
some parts of the country. Thus, human cases
2. Mammomonogamosis 
of echinostomiasis, artyfechinostomosis, and
intestinal capillariasis have been described in
 Mammomon
 Mamm ogamuss laryngeus (Plate
omonogamu 8.21) such areas. In Isabela, where human cases of
is the causative agent of this condition and is artyfechinostomosis have been reported, the
a common parasite of ruminants (e.g., cattle, snail second intermediate host is eaten raw or
water buffaloes) in some parts of the world. In   partly fermented. It is prepared by shaking the 
e ili i es   of  sla g e e ca le i
tChagaPyhan pd pe O 23i y wer e f ouunhdt ir nf dectedtttt withn
n r o, C t%  alati,l gwinitgher s,alot ntoior ne,mvoinvegm
sn ar u,  p
cue p secr,etainodn,otthenr
s  p
this parasite.  M. laryngeus
laryngeus has been recovered spices are added and eaten or left overnight
from the trachea of water buffaloes slaughtered to ferment before being consumed. This is in
in Bayog, Los Baños, Laguna (unpublished).  contrast with another place, San Pablo, Laguna
Human infection results from ingestion of in Southern Luzon, where the same snail has
embryonated ova or infective larvae through  been found to have even higher percentage of
contaminated food and water, or accidental infection than in Isabela, but no case of human
ingestion of transport hosts such as earthworms, infection has occurred since this snail is not
snails, or arthropods. To date, about 100 cases  eaten by the local population. Instead, it is  
 

380   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

detested due to its slimy texture. Even the local Some maintain that cooking not only
o nly destroys
term, suson
 susong
g linta, meaning “leech -like” snail,
linta the flavor they relish, but also the nutritive
sounds unpleasant to the ear. value of the food. Nevertheless, with a more
 Kilawen is also popular among folks in aggressivehealtheducationcampaign,together
Leyte. Pig liver is cut into thin slices, soaked with programs directed to the improvement of
in vinegar with salt and condiments and eaten the living condition of the inhabitants in these
raw. Pig meat, partly cooked and prepared as  areas, preventive measures against many of these
t hese 
above, is also eaten. Cysticercus (larva) of Taenia
Taenia zoonotic diseases can be achieved successfully.  
 solium and T . saginata asiatica are found in the
Zoonotic Parasites as Indicators of Fecal
muscle and liver respectively of pigs, which serve Pollution of the Environment 
as intermediate hosts. Human infection occurs 
through consumption of raw or partly cooked Many of the protozoa and helminth
infected organs.  agents causing zoonoses described in this
 Pila conica(kuhol , bisukol ) andSundathelpusa
conica section are associated with fecal pollution of
 philippina (talangka), the second intermediate
 philippina the environment, whether land or aquatic.
hosts of E ilocanum and P.westermani filipinus
westermani filipinus , Many protozoan and helminth parasites shed
respectively, are eaten practically all over   cysts ( Balantidium coli , Cryptosporidium spp.,
the country. However, echinostomiasis and histolytica , Giardia duodenalis ,
 Entamoeba histolytica
 paragonimiasis are prevalent or endemic Toxoplasma gondii, Sarcocystis spp.) and eggs/

only in certain areas.

echinostomiasis has theInhighest
Northern Luzon,as 
prevalence larvae ( Toxocara
Strongyloides
canis , Ancylostoma spp.,
spp.), respectively, that are

tchoeoksnedaiilnhtohsits  iasr eat. eSnimsoilm

ar elyti, p sar gaowniomr   p
maer  iasair stliys o otr he, emnvanir yonhmelemnitnthr  p
f deicssees.mFinuar tehder tm ouagr hasithees
endemic in areas where inhabitants are known require intermediate hosts to complete their
to consume the crab host raw. A preparation cycle (cyclozoonoses and metazoonoses). The
with fresh crab juice locally known askinagang iiss eggs/larvae of the parasites are passed out
considered a local delicacy. Males in these areas with the feces of the definitive host to the
were observed to eat raw crabs during drinking environment before they develop and gain
sessions with the local wine ( basi), especially access to the intermediate host.  
during festivities. The same is true for intestinal  Echinostoma spp.,  Arty
 Ar tyfe
fech
chininos
osto
tomu
mu m
capillariasis in Northern Luzon. The fish host, malayanum , Fasciola spp., heterophyids,
 Hypseleotris bipartite , is especially desired when Carneophallus brevicaeca ,  Plagiorchis
gravid (filled with eggs), and the entire fish is spp., Schistosoma japonicum , Paragonimus
eaten raw. Another fish host, Ambas sis miops, in
 Ambassis westermani , and Capillaria philippinens
philippinensisis
the raw form, is bitten at the belly by some to reach their intermediate hosts through fecal
suck out the juice. Residents of endemic areas   contamination of the water environment. 

in Northeastern
consume Mindanao were also noted to
fish raw.
fish raw. Sarcocystis
 Macra
 Macracantho spp. Eurytrema
 Euryt
canthorhynch usrema
rhynchus spp.,
hirudin
hirudinaceou
aceouss reach
Taenia spp.,their
and
Simply giving up the habit of eating raw intermediate hosts through fecal contamination
contamination 
food of animal srcin may prevent human of the pasture or direct access of the intermediate
infection with a number of these zoonoses. host (pig and cattle) to fecal matter of infected
However, as the saying goes, old habits may not
However, definitive host (humans) in case of human
easily be given up. Furthermore, some people taeniasis. Proper disposal of fecal material,
in these areas, though properly informed about whether of humans or animals, therefore, is
this transmission, still value their food habits.   everyone’s concern.
everyone’s  concern. 
 

CHAPTER 8: Special Topics in Parasitology   381 

The presence of reservoir hosts in depends on agriculture, fishery, and forestry for

combination with the presence of suitable livelihood. One-third of all goods and services
invertebrate
the infectionintermediate
in a particularhosts
area.also maintains
Field rats are  produced by the economy
econo my is accounted
accoun ted for by
the agricultural/rural sector,which also employs
maintaining the cycle of zoonotic parasites such half of the country’s
country’s workers,
 workers, and earns 36%
as Echin ostomaspp., A. malaya
 Echinostoma num, Schistosoma
malayanum of the country’s export income. An unhealthy
icum, Plagio
 japonicum
 japon rchis spp., and Parago
 Plagiorchis nimus 
 Paragonimus working population can only mean low or  
westermani. Because of the intermediate hosts, reduced productivity, while infected animals
the potential risk of human infection is ever mean unwholesome meat such as in cases of
 present. The snail,  Bullastra cummingiana
cumming iana ,  fascioliasis and cysticercosis. This, in turn, can  
had high prevalence of infection with  A. only lead to further reduction of supplies due
malayanum in Sampaloc Lake in San Pablo to carcass condemnation of what is already an
City. It should be noted that piggeries are insufficient meat
insufficient  meat supply. In a country like the
concentrated around Sampaloc Lake, and their Philippines where poverty is widespread in rural
excreta pollute the lake. Pigs, apart from rats, are areas, these diseases can only worsen what is
known as a definitive
definitive host
 host of the parasite and already a bad situation. 
are maintaining the cycle in that area. While
Medical-Veterinary Cooperation in the
there are no human cases of infection as yet, the Control of Parasitic Zoonoses 
 presence of the parasite in the area still poses a
threat to human health. Animals, both
domesticated andinvertebrates andtovertebrates,
wild, are hosts a number  
Economic Losses Resulting from Parasitic
Zoonoses 
ovaer adsitsicuszsoionso.seTs haesir alroealedyasshdoew
oa bf   p f initiinvet,he
The Philippines has a fast growing human intermediate, and reservoir hosts make them
 populat ion and currently
 population cu rrently has
h as already
alread y reached essential in maintaining the zoonotic agents
94 million. It is even projected that at a growth in nature. As paratenic or transport hosts, they
rate of 2% annually, the population may reach  prolon g the availability
 prolong availabil ity of the agent as potential
113 million by the year 2020. However, food sources of human infection, as well as increase
animal production has not increased to keep the potential of disease dissemination.  
 pace with the demand of the increasing human Studies to better understand the processes
 population.
 populat ion. Recent statistics
statisti cs revealed a slow
sl ow involved in the maintenance, transmission,
growth for food animal production. A large and epidemiology of these diseases should
 proportion of the human population live in involve the participation of those concerned,
the rural areas, and a much larger proportion especially physicians, veterinarians, and public
of the food animal population are raised in the health workers. In most countries including
 backyard. This
This food animal
animal populationremains  the Philippines, parasitic zoonoses are the  

large compared
commercial to the
farms. number
This raised
ecological in large
profile of most
humanunderdiagnose
underdiagnosed
d diseases
infections with theseindiseases
human. Some
may
human and animal population distribution  have passed unnoticed or may have been  
makes a large proportion of both populations misdiagnosed, as some are difficult to detect or
at risk of infection. many simply are not aware of them.  
Although it is difficult
difficult to
 to assess exactly The control of zoonoses involves:
economic losses from zoonoses, it is evident control in animals, the veterinarian’s concern;
in the Philippine setting that these diseases are  prevention and treatment in humans, the
 prevalent in rural areas
ar eas where the
th e population
populat ion    physician’s responsibility;
 physician’s  responsibility; and the control 
 

382   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

of vehicles of transmission, the concern of Claveria FG, Cruz-Flores MJ, de la Peña  

 both. For the management and control of C. Sarcosystis miescheriana infection in
zoonoses to be
medical and effectiveefforts
veterinary and successful, joint
are necessary.
domestic pigs (Susscrofa) in the Philippines.
J Parasitol. 2001;87. 
Medical-veterinary
Medical-veterina ry cooperation has been more Claveria FG, San Pedro-Lim MR, Cruz MJ,
 prominentt in parasitology
 prominen parasitol ogy than in any other area  Nagasawa H, Susuki N, de la Peoa C.
of medicine. It should continue toflourish
to flourish  and
and  Ultrastructural studies of Sarcocystis cruzi 
should be fully supported.   (Hasselmann, 1926) Wenyon, 1926
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Cryptosporidium from Palawan, Republic 2000;37:109 – 10.
10.
of the Philippines. Phil J Microbiol Infect  Rivera WL, Yason JA, Rivera PT. Serological  

Dis. 1988;17:1
Miyazaki  – 3.
3. studies on the lung
I. Taxonomical detection of cryptosporidiosis
Filipino cancer among
patients. Parasitol Res.
fluke occurring in the Philippines. Med 2005;98:75-6. 
Bull Fukuoka Univ. 1931;8:153 – 8. 8. Rivera WL, Yason JA. Molecular detection
Molina EC, Ridley-Cash LS. Toxoplasmosis of Cryptosporidium from animal hosts in
in cats at Kabacan, Cotabato, Philippines. the Philippines. Philipp Agric Scientists.
 Philippines.
Univ Southern Mindanao Res Dev J. 2008;91:473 – 77..
2008;16:53 – 5.
5. Rudge JW, Carabin H, Balolong E, Tallo V,
Shrivastava J, Lu DB, et al. Population  
 

384   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

genetics of Schistosoma japonicum within the Greater Metropolitan Manila area of

the Philippines suggest high levels of Luzon Island Philippines. Open Vet
Vet Sci J.
transmission between humans and dogs. 2008;2:50 – 4.
4.  
PLoS Negl Trop Dis. 2008;2(11):e340.   Van Aken D, Lagapa JT, Dargantes AP,
Samuel WM, Pybus MJ, Kocan AA. Parasitic Vercruysse J.  Mamm
 Mammonoga
onogamus
mus llaryng
aryngeus
eus
diseases of wild mammals. 2nd ed. USA: (Railliet, 1899) infections in cattle in
Iowa State University Press; 2001.  Mindanao, Philippines. Vet Parasitol.  
Schwabe CW. Veterinary
Veterinary medicine and human 1996;64: 329 – 32.
32.
health. 3rd ed. Maryland, USA: Williams Velasquez CC, Eduardo SL. Index catalogue of  
& Wilkins; 1984.   parasites of Philippine
Philipp ine vertebrates. Manila
Tangtrongchir A, Monzon RB. Eating habits (Philippines):National
(Philippines):National Academy of Science
associated with  Echinostoma malayanum
malay anum & Technology; 1994.  
infections in the Philippines. Southeast World Bank. World development indicators
Asian J Trop Med Pu blic Health. (WDI). Washington, D.C.: The World
1991;22(Supplement):216 – 21. 21. Bank; 2009.
Theis JH, Gilson A, Simon GE, Bradshaw B, World Health Organization. Parasitic Zoonoses.  
Clark D. Case Report: Unusual location Technical Report Series 637. Geneva:
of Dirofilaria  immitis in a 28-year-old man
 Dirofilaria immitis World Health Organization; 1979.  
necessitates
necessitates orchiectomy. Am J Trop Med World Health
Health Organiza tion. Control of
Hyg. 2001;64:317 – 22.
22. food-borne trematode infections. WHO
Theis JH, Tran ST, Carlos MP, Carlos ET, Technical Series No. 849. Geneva: World 
C r loit si sS(M
imam LeEid. yI)nicnidcelinecnet ow
f  ne D ir o f ilar ia
d dogs f rr o  m  Health Organization; 1999.
 

CHAPTER 8: Special Topics in Parasitology   385 

lmmunocompromised
lmmunocompromised Hosts and Parasitic Infections
Edsel Maurice T. Salvaña, Evalyn A. Roxas, Mary Ann D. Peñamora

arasites are uniquely adapted to survive than normal levels, producing more severe
and thrive in the human host despite the   disease. This opportunism can be exemplified as
as  
 presence of a hostile
hostil e immune system.In
system.In order to infection by parasitic organisms which are rarely
defeat this protection, parasites deploy a number  pathogeni c (e.g., Aca
 pathogenic  Acanth
nthamo eba, microsporidia)
amoeba
of strategies to either evade or overwhelm or those which cause increased disease severity
natural host defenses. Immunocompromised or duration (e.g., Cryptosporidium, Cyclospora,
individuals are at a distinct disadvantage  Cystoisospora , Toxoplasma, Strongyloides ). 
in seeking to detect and control parasitic Multiple processes can predispose to
infections. Moreover, they become susceptible infection by compromising the anatomical
to otherwise non-pathogenic organisms which and physical barriers of the host. Defects
D efects in
then cause opportunistic infections. In this the inflammatory pathways and immune
chapter, we review some of the more common functions may allow infections by opportunistic
opportunistic parasitic infections and describe  pathogens. Some of these defects may be
strategies to prevent and treat these diseases.  related to a congenital disorder or abnormal
Etiology and Pathogenesis  development, underlying acquired disease,
drug therapy, malignancy or irradiation.  
f  a par asite is t r e pr oduce
and  ppTehr  pe eetnudatgeotahleos p ecies. Ther ef or e, sur vival Ss p ifitci b
usecce p  pim
 bdielif teycttsoins p ifiucnseu bcosm
ecm enattshloegadentso,
s onf   p
et p
strategies dictate that the host survives long such that the pattern of opportunistic infections
enough for the parasite to propagate and is a clue to the underlying defect. In addition,
spread. There is evidence that the most once established, some pathogens such as
parasites cause little or no disease as a  protozoans
successful parasites  protozo ans can further
furt her exacerbate
exacerbat e or produce
prod uce
consequence
consequen ce of millions of years of co-evolution other abnormalities in immunologic function
with its host. For instance, we know that the least such as in the case of T. gondii, Leishmania ,
 pathogenicc of the malaria
 pathogeni mal aria species,  Plasm
 Plasmodium
odium or  Plasmodium spp. The consequences of
malariae , is the oldest human parasite among
amon g  protozoan
 protozo an or helminthic
helmi nthic diseases
d iseases which
whi ch cause
the group, and that the most pathogenic,
p athogenic,  P
 P.. malnutrition may alter immune function. 
 falciparum , is the most recent to cross over These alterations are not necessarily associated
to humans. Hosts, specifically human hosts, with clinical susceptibility to opportunistic
should be thought of as not just one organism  pathogens per se but may contribute to a less
 but as a tightly balanced environment with than ideal host response. Finally, one must  

endogenous
This flora
milieu is  with unique
a product ecological
of the niches.
interactions of consider thatboth
mixed, with some immune
humoral anddefects may be
cell-mediated
the host immune system and the microbial components; and that because there is some
flora, and perturbations in either can upset overlap between components, deficiency in one
the health of the organism. Various conditions
conditions component may still adversely impact another
which compromise the immune system will component that otherwise has all its elements
affect the balance between the pathogen and in working order. 
host, and allow organisms to replicate at higher  
 

386   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 A. Leukocyte
Leukocyte Defici encies 
encies  due to encapsulated bacteria and protozoans.
Development of immunity to invasive
Predilection
leukocyte to parasitic
disorders depends infection in of
on the type  pathogens such as Entamoeba histolytica
histoly tica can
 be impaired, and amebic disease may progress
leukocytes which are numerically or functionally
functionally rapidly. The spleen is a major site for T-cell
affected, and on how prolonged the dysfunction independent immune responses and large
is. The rate of decline and duration are also 
numbers of B-lymphocytes, monocytes, and 
iomu ptcor m  peaur atm
taen.t N r o petenr siath(<at1,i0n0fl0uenecuetr co p
linhiiclas/l macrophages reside. It has a prominent role
mm³) is the most commonly encountered defect in the phagocytosis of circulating opsonized
in inflammatory host defense mechanisms. 
organisms. In several reported cases, malaria 
Susceptibilitytobacterialandfungal infections, appears to be more severe after splenectomy,
 but not usually to protozoan,
protozoan , viral or helminthic
helmint hic while babesiosis, as a clinical disease seems
to occur with unusually high frequency.  
disease, increases dramatically when the
The clinical importance of splenectomy for
 peripheral neutrophil count falls below 500
other protozoans and helminths is less clear.
cells/mm³ and increases more markedly  
Complement deficiencies can affect the
when the count falls below 100 cells/mm³.
clearance of organisms, but whether these
Lymphopenia in adults is defined as having
 predisposee towards specific
 predispos specific parasitic iinfections
nfections
less than 1,000 lymphocytes/mm³. Its clinical is less clear. Treatment with omalizumab, a
consequences depend on which lymphocyte
subsets are affected. Regardless of the total monoclonal antibody against
has led to some concern prIgE for asthma 
of predisposition
edisposition
lymphocytee count, severe infections of various 
lymphocyt
types may occur if profound deficiencies of lmiziendthcioc nitnr f oelc tir oianl,  b
tonwearadns dhoem haust sahtole
wanstno
either B-lymphocytes or T-lymphocytes are additional significant risk.  
 present. Substantial reductions in helper  
Understanding the specific immune
T-lymphocytes have important consequences in deficiency in an immunocompromised patient
ter ms of  susce pti b
 bility to  ppr otozoan T 
( o xo pla ma)  s
is particularly important with regard to
and helminthic (Strongyloides) infections. The  protozoans and helminthic infections since
most common causes of lymphopenia are
hematologic malignancies, corticosteroid
appropriate diagnostic tests for these diseases
may not be routinely requested or may not
therapy, anti-lymphocyte globulins, cytotoxic  be available; and empiric regimens do not
drugs, and infections with certain viruses
usually include protozoan or helminthic
such as cytomegalovirus and the human
immunodeficiency virus (HIV), the etiologic
coverage. Moreover, matching these defects
agent of acquired immune deficiency syndrome
with common, endemic causative organisms in
a given locale is essential. 
(AIDS).  
B. Humoral Deficiencies 
Deficiencies  Protozoans and Helminths of Special
lmportance 
Immunoglobulin deficiencies particularly
Protozoans
Protozoa ns and helminths thatare of special
those that affect IgG and IgA production
concern to immunocompromised individuals
can cause a marked increase in susceptibility are listed and
an d summarized in Table
Table8.3. Multiple
Multi ple
to infections caused by  Plasmodium spp.,  parasitic infections
infe ctions are more likely
likel y to occur in
ia, and Giardia. Patients with significant
 Babesia
 Babes
immunocompromised individuals as well. This
reduction in IgG (usually <200 to 300 mg/
is especially true in AIDS. HIV and AIDS have
dL) characteristically have recurrent
recurrent infections  resulted in a sharp increase in the number of  
 

CHAPTER 8: Special Topics in Parasitology   387 

Table 8.3. Protozoans and helminthic organisms  between protozoan

p rotozoanss or helminths
helmi nths and cellular
of special importance to immunocompromised immunity. Uncontrolled enteric parasite
patients   infection contributes to increasing malnutrition
Protozoans Helminths
from malabsorption and direct damage, which
Toxoplasmagondii Strongyloidesstercoralis
in turn further taxes the immune system.
Metabolic derangements from HIV infection
itself further contribute detrimental effects to
Cysososporabelilit
the host.
A study by Chaisson et al. on the impact 
of opportunistic diseases in the United States
among a cohort of 2,081 patients with HIV
infection between 1989 and 1995 revealed a
total of 1,499 (49%) opportunistic diseases
during follow-ups. The predominance of enteric
 protozoans,
 protozo ans, especiallyCryptosporidium, as causes
of chronic diarrhea has been reported to occur
in 30 to 60% of AIDS patients in Haiti, Africa,
and other developing countries. Infections with
cases of life-threatening
life-threatening opportunistic infections microsporidia,Cystoisospora, Giardia, and other
due to bacteria, fungi, viruses, and parasites.   rarer organisms have also
 A. H IV a nd Par asitic Infe ction  
 protozo
 protozoans
ans are among thebeen reported.
important etioEnteric
etiologic
logic  
HIV depletes the helper (CD4+) subset agaetinetnstos f sdcir aer er nheda ionvAer IDa S1i0n T
 p d.e r 
mhoaniltahn p Oiof d28in8
of T-lymphocytes with drastic consequences 1999 to 2000, 55 (19.2%) hadCryptosporidium 
on cell-mediated immunity. Unmodulated spp., 13 (4.5%) had Cystoisospora oocysts,
inflammation and immune activation increase 11(3.8%) had G. lamblia , 3 (0.9%) had
susceptibility to a host of illnesses and histolytica , and 1 (0.3%) had
 Entamoeba histolytica
malignancies, and may allow previously latent  Iodamoeba
 Iodamoeba b
butschlii infection.
utschlii The prevalence
infections to become active. These latent of microsporidia was 11% in this stud
study.
y. Studies
infections include tuberculosis, herpes viruses, in Dakar, Senegal by Gassama, et al. among
 Leishma
 Leis nia, and Toxoplasma. Low pathogenicity
hmania HlV-infected and non-infected patients with
organisms in immunocompetent hosts such as diarrhea revealed  Micr
 Microspo
ospo ridi um (9.4%),
ridium
 Pneumocystis
 Pneum ocystis jiroveciiand intestinal sporozoans
jirovecii Cryptosporidium sp. (8.2%),  E. histolytica
may develop into life-threatening infections. (5.1%), and Cystoisospora belli (4.4%) to be
Finally, pathogens which may be mild or the more frequent parasites seen among the
less severe such as  Babesia and Plasmodium
 Plasmodium   immunocompromised individuals and were  
may becomeenvironment.
 permissive more virulent
  as a result of the often
count.identified
cystisinhominis
 Blastocystis
 Blasto patients
homin with
is was low CD4+
identified  only
The pattern and types of HIV-related among HIV-infected individuals. Additionally
Additionally,,
opportunistic infections throughout the world high levels of asymptomatic carriage of  A. 
 A. 
is affected by endemic infections, general lumbricoides and T. trichiurawere observed.
health, nutrition, and access to health care A follow-up study on the progression
and medical services. The dramatic frequency of HIV infection performed by Manaloto et
of parasitic infections in AIDS presents an al., in a cohort of 54 HIV-infected Filipino
important lesson about the interrelationship  commercial sex workers from May 1985 to 
 

388   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

July 1992 revealed  Mycoba

 Mycobacteriu
cterium
m tuber
tuberculos
culosis
is formation of pseudocysts and cysts that contain
and  Pneumocys tis carinii  pneumonia as
 Pneumocystis a more slowly
s lowly replicating stage (bradyazoites).
the initial indicators of immunodeficiency The cysts are distributed throughout the body.
following a CD4+ cell count of <200 cells/ In the central nervous system, they appear to
mm. Cryptosporidiosis and brain toxoplasmosis
toxoplasmosis  persist in latent form for the entire lifespan of
were also seen in two patients. Among the 145 the host, provoking little if any inflammatory
 patients with HIV infection
infectio n seen at the Research   response. These dormant organisms can be 
Institute for Tropical Medicine (RITM) from reactivated in immunosuppressed persons. In
1985 to 1996, cryptosporidiosis
cryptosporidiosis was diagnosed recent years, the importance of toxoplasmosis
tox oplasmosis
in 31% of cases. G. lamblia was detected in  in immunocompromised host has been  
13%, Ascari
 Ascariss lumbricoides in 11%, E. histolytica
lumbricoides histolytica  increasingly recognized.
recognized. Patients with a variety
in 9%, E. nanain 7%. B.
 B. homi nis, H.
hominis  H. nana, and
nana of neoplastic diseases, including Hodgkin’s
T. trichiuraeach in 2% of the cases. Follow-up lymphoma, as well as patients receiving
of 103 symptomatic cases through 1998 did not immunosuppressive therapy are at risk of
reveal significant differences in the prevalence reactivation of this infection. The incidence
of the parasitic infections seen previously. of toxoplasmosis has raised dramatically with
Additionally, 2% of the cases revealed CNS the increasing population of AIDS patients.  
toxoplasmosis and 3% had B. hominis.  T. gondii is now the leading cause of space-
B. Toxoplasma gondii  
occupying cranial lesions in persons with AIDS. 
Infection of immunologically normal
Toxoplasma gondii is a sporozoan in   persons with Toxoplasma usually results in a 

waor r alsditse  ptho p
 p ’ t  intof eactsthair 
atuilnatf ieocnts.  uI p
 p  lld  or f detr hse of 90er %
 p nta btiuetntas.yPmr 
sisotef  p  pim r yadtiicseiansf e cistiaolnsoinus8u0altloy
toam
mammals and some birds. The domestic cat is subclinical but in some patients may present as
a definitive host and produces
pr oduces infective oocysts. a mononucleosis-like syndrome with cervical
Handling of cat feces is a strong risk factor lymphadenopathy and rarely with ocular
for contracting primary disease. Ingestion of manifestations.  
food or water contaminated with oocysts, and Toxoplasmosis in AIDS patients usually
eating of undercooked meat is the usual means develops at CD4 counts of less than 100
of infection. Toxoplasma gondii can be passed cells/mm3. While virtually any organ may be
transplacentally to the fetus when a pregnant involved, the most common manifestations are
woman has a primary infection, leading to fetal in the central nervous system and may involve
infection leading to severe congenital anomalies.
anomalies. the eyes. Virtually all toxoplasmosis in AIDS
The prevalence of Toxoplasmaantibodies varies  patients is reactivation,
reactivatio n, and so only Toxoplasma
considerably among different populations and IgG positive patients are considered at risk.
ranges from 3 to 70% in the United States to  Other underlying conditions that may give  

as high as 80% is
Toxoplasma in an
Western Europe.
intracellular  
parasite   rise to reactivation
various malignanciesof(such
to xoplasmosis
toxoplasmosis
as Hodgkins’include
disease,
capable of invading and replicating within non-Hodgkin’s lymphomas, leukemias, and
nucleated cells. Ingested oocysts enter host solid tumor collagen vascular disease, organ  
cells either by rupturing the membrane or transplantation, and prolonged steroid use).
 by invaginating them. After multiplication More than 50% of these patients show altered
 by repeated endodyogeny, the macrophage mental status, motor impairment, seizures,
finally ruptures, liberating the replicating stage   abnormal reflexes, and other neurologic
(tachyzoites) of the parasite and giving rise to the  sequelae. The most common presenting
 

CHAPTER 8: Special Topics in Parasitology   389 

symptom is still seizure, followed by focal rise in antibody titer with serial specimens.
sp ecimens.
neurologic deficits including ocular symptoms.   Since the interpretation of serological tests
Diagnosis of acute disease is through for toxoplasmosis is not uniform, it must be
detection of IgM antibodies or a four-fold rise correlated with other diagnostic techniques
in antibody titer. The presence of high titers including radiographic and other laboratory
l aboratory
(>1:1024) by the Sabin-Feldman dye test, direct abnormalities as well as the clinical situation.  
agglutination tests, or conventional indirect  The detection of Toxoplasma antigen in 
immunofluorescent antibody (IFA) technique serum or other body fluids
fluids (e.g.,
 (e.g., CSF, ocular
is suggestive of acute infection. However, fluid, urine) may be particularly important in
high antibody titers may persist for years after   immunocompromisedd patients in whom active  
immunocompromise
infection. Therefore, in patients with stable disease is not always associated with rises in
high titer and detection of IgM antibody by antibody titers. The gold standard for diagnosis
the IgM-IFA double sandwich IgM enzyme remains demonstration of the organism in
immunoassay (EIA), or immunoblot tests may tissue.
 be useful. Other assays include
i nclude complement
com plement-- Toxoplasma gondii has been identified
fixation test and conventional IgA-EIA. A in biopsy specimens of the bone marrow,
negative IgM test essentially excludes recent myocardium, skeletal muscle, lung, and brain
infection, but a positive IgM test is difficult using both hematoxylin and eosin (H&E) stain
to interpret because Toxoplasma-specific IgM and immunospecific stains for Toxoplasma .
antibodies may
as 18 months be detected
after by EIAinfection.
acute acquired for as long  Biopsy samples
or sensitive cellcan alsotobeisolate
lines inoculated into mice  
the organism.
ectiion oaf nIdgG
 pr ior Dientf ec ntoi b
thea p  bsso b
i dbiles pir nedseicnacte sof er,o b
 bHeoenwevx p s edcatuose T 
mo xan  s
s  hayavhe ave
o pylainmdaiviadnudalm
tissue cysts. In the immunocompromised cysts within tissues, recovery of the organism
hosts, interpretation of serological test is from cell culture or animal inoculation maybe
dependent on understanding of the degree of misleading. Recently, the use of molecular
underlyingg immunosuppression,
underlyin immunosuppression, the serological technology techniques (such as PCR, DNA
status of the patient prior to the development hybridization using ABGTg7 probe) have
of symptoms
s ymptoms indicating acute Toxoplasma  been found to be sensitive, specific, and rapid
infection, and knowledge of the pathogenesis of methods for the detection of T. gondii DNA
Toxoplasmainfection in the risk group to which in amniotic fluid, blood, BAL fluid, tissue
the patient belongs (e.g., transplant recipients). samples, and CSF.These are currently research
res earch
Serologic tests may reveal changes in antibody tools and are considered ancillary diagnostics
titers without necessarily being indicative of especially when only very small amount of
active infection. Therefore, serological rises in specimen is available, when the condition is  
antibody titers in immunocompromised patient   dubious, when the result is required urgently or  
cannot
of activebeinfection
used as the sole
with diagnostic
Toxoplasma criterion
, especially ifexaminations
serological tests
suchareasinconclusive.
computerizedRadiologic
axial
if the clinical manifestations are non- specific. tomography (CAT) scan and nuclear magnetic
In contrast to rises in antibody titers in some   resonance imaging (MRI) have been found to  
immunocompromised patients without any  be extremely useful in the demonstration of
definite signs or symptoms ofactive toxoplasmic abnormalities associated with TE in patients
infection, other immunocompromised patients with no underlying immunosuppression as
with fulminant toxoplasmosis may have low well as in immunocompromised hosts. In
or negative dye test or IFA titers and show no  AIDS patients, the most significant differential 
 

390   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

diagnosis is central nervous lymphoma, and cysts or by food contaminated with oocysts,
differentiation can be quite difficult. If the susceptible patients should not eat raw or
mass is small and there are no life-threatening undercooked meat and should thoroughly wash,
complications, empiric treatment followed by  peel or blanch fresh produce. Careful hand
serial MRI’s
MRI’s to
 to document improvement can washing after handling potentially contaminated
 be done. However, in cases where diagnosis material including cat litter, raw meat, and fresh
is urgent and delay can lead
l ead to serious clinical   produce is essential. T The
he presence of a ccat
at at 
consequences, brain biopsy must be pursued.  home is a risk for infection, and steps should
Treatment for Toxoplasma infections   be taken to minimize contact between the cat
is indicated for patients who develop and the patient, and if
i f unavoidable, the patient 
acute infection during pregnancy, and for   should follow strict hand washing.  
immunocompromised patients with evidence C. Cryptosporidium  
Cryptosporidium
of reactivation disease. The combination of
 pyrimethamine and sulfadiazine is the most Cryptosporidium was initially described in
effective regimen. Empiric therapy should be mice in 1907, but it was not until 1976 that
instituted in seropositive immunocompromised
immunocompromised it was first reported in humans. The advent
 patients who present with compatible of the AIDS epidemic substantially increased
neurologic symptoms and characteristic the number of cases. Cryptosporidium is an
imaging. Asymptomatic patients may become
imaging. intestinal spore forming protozoa which mainly
symptomatic and symptomatic patients may causes diarrheal illness. Insp.
otherwise
 briefly worsen when initiating antiretroviral  individuals, Cryptosporidium typicallyhealthy
causes 
ther a p f oer tH
Tr yim ho p ethuonxear zeocloen(sT
IVr idmu-esutolf ai mm utPio- n.
titM laastienr gy of or  r msuecvoer idaldi ar yr sheoar  woictcha bsidoonm
w alliynawl  peeakins
SMZ) when used as prophylaxis for  Pn  Pneum
eumocy
ocyst
stis
is that is self-limited even without treatment.
eci is effective prophylaxis for toxoplasm
 jiroveci
 jirov toxoplasmosis.
osis. Cryptosporidium causes far more serious disease
If TMP-SMZ cannot be tolerated, there are in immunocompromised individuals, with no
alternative prophylactic regimens which include effective treatment for those with AIDS.  
clindamycin and dapsone plus pyrimethamine.
p yrimethamine. The most commonly identified species
Atovaquone with or without pyrimethamine considered pathogenic for man is C. parvum.
may also be considered. Patients with a history Two genotypes of C. parvum are responsible
of central nervous system toxoplasmosis should for most human infections. These include the
 be administered
administ ered suppressive
suppres sive therapy with drugs human anthroponotic genotype 1 found almost
active against Toxoplasma to prevent relapse, exclusively
exclusively in humans and thebovine
thebovin e or zoonotic
until the CD4 count is above 100 for over a genotype 2 found in both ruminants and
year, or the initial immunosuppresing condition human. However, studies revealing molecular
has resolved.  diversity among humanCryptosporidiumisolates 
Immunocompromised
 be tested patients
for IgG antibody to should
Toxoplasma to suggest
than onethat multiple
species subgenotypes
may be implicated inorhuman
more
detect latent infection and offered prophylaxis disease. 
as appropriate. Seronegative patients should  Experimental-infection
Experimental-infection studies with mice
 be counseled about the various sources of and calves show that immunity is dependent
toxoplasmic infections and advised appropriate
appropriate on the number of CD4 T-cells generating
methods of preventing exposure especially. gamma interferon. No difference was found
Because infection is usually transmitted by  between cryptosporidiosis in normal and 
ingestion of undercooked meat with viable   B-cell-depleted neonatal mice, suggesting that  
 

CHAPTER 8: Special Topics in Parasitology   391 

antibody production may play a less important  post outbreak period compared with four deaths
role in recovery from infection. Interleukin-12 overall in the two years before the outbreak. This
also plays a role by inducing gamma interferon represented a more than a 13-fold increase in
 production.  cryptosporidiosis-associated mortality. 
All species of Cryptosporidium that Zoonotic and person-to-person
have been studied are obligate intracellular transmission may occur through direct or
 parasites, however,
however , unlike other coccidians,   indirect contact with stool material in the  
their developmental stages do not occur deep environment,
environme nt, day-care centers, and
a nd the hospital
within the host cells but are confined to an setting. Direct transmission may occur sexually
sexually
extracytoplasmic location. Each stage is within a 
extracytoplasmic during oral-anal contact. Indirect contact may 
 parasitophorous
 parasitophorous vacuole within the microvillous
microvillous occur through exposure to positive specimens
region of the mucosal epithelium of several in the laboratory setting or from contaminated
organs including the respiratory tract and the surfaces or food or water. Studies have shown
s hown
 biliary tract, but most commonly that of the that calves and other animals, including
gastrointestinal tract. Cryptosporidium differs kittens, rodents, puppies, and birds may serve
from other coccidians in its ability to undergo as potential sources of human infections. 
complete developmen
dev elopmentt within a single
single host. The Cryptosporidium oocyts, are resistant to most
sporozoites, after being released from the host disinfectants, and are difficult
difficult  to filter  due
 due to
cell, can penetrate the microvillous region of their small size, thus enabling them to persist
other cellsinand
excreted reinitiate
stool the life cycle.
are immediately
i mmediately Oocysts
infective to 
and spread in the environment.
Cryptosporidiosis is a substantial threat to  

id utoteosthtoer tsh. eThr eif sr auctor -iynnf eactuivr e
ilietyhocostnatnr  b
tcha pe as bam r isIkVoif nf iencf tecdtioi ndiovf idaur oalusn, w
H d h1o0%
ha.veTahelif m
etoim
ste
of cryptosporidial infection in patients with common clinical feature of cryptosporidiosis
impaired immunity. is diarrhea. Among adult HIV patients,
Cryptosporidium is ubiquitous around the cryptosporidiosis is the reported cause of
world, with the highest prevalence observed in diarrhea in 15 to 40%.  
less developed countries. It is transmitted via C.  parvum infections are not always
contaminated food or water. Cryptosporidium confined to the gastrointestinal tract; additional
contamination
contamina tion of surface water is quite
quit e common. symptoms (respiratory problems, cholecystitis,
The number of ingested Cryptosporidium hepatitis, and pancreatitis) have been associated
oocysts required to cause illness is quite low, with extraintestinal infections. Chronic
with median human infective dose of 132 cough, dyspnea, and fever have been reported
oocysts. to be the major symptoms in pulmonary
Cryptosporidiosis is the most common cryptosporidiosis, with diarrhea only as an
cause of waterborne disease in the United   associated symptom. 

Kingdom. In the United

cryptosporidiosis States,inthe
outbreak Milwaukee
1993 was  Diagnostic
examination
examination, techniques
, histologic include
examination stool
of intestinal
the largest outbreak of waterborne disease  biopsy, and examination
examin ation of duodenal
d uodenal aspirates.
as pirates.
ever reported in the United States due to Cryptosporidium oocysts in the stool range
Lake Michigan water contaminated with from 4 to 6 µm in diameter and can be very
Cryptosporidiumoocysts. Anestimated403,000 difficult to identify. Stools and other body fluid
residents and visitors of Milwaukee experienced
experienced specimens (e.g., sputum) should be submitted
watery diarrhea and 54 cryptosporidiosis- as fresh material or in 5 or 10% formalin,
associated deaths occurred during the two-year   sodium acetate-acetic acid-formalin (SAF), 
 

392   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

or polyvinyl alcohol (PVA) with zinc sulfate- Cryptosporidium-infected HIV patients in India,
 based Schaudinn’s
Schaudinn’s fixative.
fixative. Fixed spe
specimens
cimens are the efficacy
efficacy  of short-term azithromycin in the
recommended because of potential biohazard management of cryptosporidiosis was studied.
considerations.
considerations. Some techniques
techniques have included Short-term azithromycin (500 mg once daily for
sugar flotation, formalin sedimentation, 5 days) treatment for cryptosporidial diarrhea in
Giemsa stain, trichrome, periodic acid-Schiff AIDS patients was associated with good clinical
(PAS), silver methenamine, acridine orange,   improvement but parasitological benefit  was 
auramine-rhodamine, iodine, modified acid - doubtful. All 13 patients, who had symptoms
fast, Kinyoun and Ziehl-Neelsen acid-fast, of cryptosporidiosis,
cryptosporidiosis, symptomatically improved
i mproved
immunofluorescence assay and immunoassay 
immunoassay   with 5 days of treatment with azithromycin and 
methods. Immunoassay procedures for the  became asymptomatic
asymptomatic after 7 days
days of antibiotic,
direct detection of Cryptosporidium antigen  but the stool sample remained positive for
or oocysts in fecal specimens have proven   Cryptosporidium even after 7 days of therapy.
to be much more sensitive than the routine After 14 days of treatment with azithromycin
acid-fast stains. Enzyme immunoassays, in 13 patients, stool samples from five patient
solid-phase immunochromatographic assays, were free of cryptosporidial oocyst. The  
and immunofluorescence assays, which use drug was well tolerated in all the patients.
monoclonal antibodies against the oocyst   This small study suggests that short-term
wall, are currently available. A flow -cytometric azithromycin can be used as a safe and effective
method
oocysts inforstool
the specimens
quantitation of Cryptosporidium
have been developed  treatment
 but for ctive
symptomatic
is not effective
effe eradicatcryptosporidiosis
in eradicating
ing cryptosporidial
cryptosporidial 
s ane ar lstetr on b
a pp  per vaecr t,itchale. a p
ateivseometwhhoadt,hiomw Cr 
P p R oach itnhf ecmtiaona. gSeum enotr tiovf e cmr y p
 p p r esor air deiaim
eatsous p l  pdioartr ahnetai.n
technologyy also offers alternatives to conventional
technolog conventional  Nutritional supplements and anti-diarrheal
diagnosis and allows the differentiation of agents may be necessary for symptomatic
Cryptosporidium genotypes. Antibody assays treatment of severe disease. In the absence of
using crude extracts of disrupted oocysts or effective therapy, prevention of infection is
recombinant antigens of Cryptosporidium in  paramount. Immunocompromised patients,
an ELISA format andspecific
and specific  Cryptosporidium
Cryptosporidium especially HIV-infected persons, should be
antigens by immunoblot method have been educated and counseled about Cryptosporidium
used for the diagnosis and monitoring of acquisition and transmission. They should 
Cryptosporidium infections.   be advised to avoid contact with feces and to
Although many therapeutic regimens have wash their hands after handling pets or contact
 been tried, there
t here is no completely
completel y satisfactory
satisfact ory with soil. Patients should avoid sexual practices
therapy for cryptosporidiosis in humans. A that might result in oral exposure to feces (e.g.
recent meta-analysis of trials of antiparasitic  oral-anal contact). Cryptosporidiosis may  

drugs in cryptosporidiosis
improvement of non-AIDSnoted significant
patients with  be acquiredwith
or contact by drinking
drin king contaminat
con taminated
contaminated edduring
water water
nitazoxanide, but no clear evidence of efficacy recreational activities. Water from suspect
for other antiparasitic drugs in cryptosporidiosis   sources should be boiled or filtered, and at risk 
or for nitazoxanide in AIDS patients. Drugs  patients should refrain from swimming
swimmi ng in fresh
that have been tried in different regimens water. Since patients with cryptosporidiosis
include paromomycin plus azithromycin, eliminate large amounts of oocysts in their feces,
clarithromycin, and hyperimmune bovine they can easily contaminate the environment
colostrums. In a randomized controlled trial of   and persons in contact with them. Because 
 

CHAPTER 8: Special Topics in Parasitology   393 

of this, some experts recommend that HlV- and duodenal and colonic mucosal biopsies,
infected persons or other immunocompromised numerous Cystoisospora oocysts were detected.
 patients should not share a room with a patient Extraintestinal infections, including biliary
with known cryptosporidiosis.   tract, respiratory tract, lymphatic channel, and
D. Cystoisospora belli  
spleen involvement, have been reported. Relapse
tends to be common and may be associated with
Cystoisospora belli is another sporozoan   extraintestinal stages.
stages. Charcot-Leyden crystals 
that causes diarrhea in immunocompromised derived from eosinophils have also been found
hosts. These organisms can infect both adult in stools of patients with C. belli infection. 
and children, and intestinal involvement Diagnosis is made by examination of a fecal
and symptoms are generally transient unless specimen for oocysts. Wet mount examination
the patient is immunocompromised. C. either by direct smear or concentrated material
belli is thought to be the only species of allows the demonstration of very pale and
Cystoisospora that infects humans, and no other
ot her transparent oocysts. They appear long and
reservoir hosts are recognized for this infection. oval measuring 20 to 33 µm by 10 to 19 µm
Transmission is through ingestion of food or in size. One or, less commonly, two immature
immatur e
water contaminated with mature, sporulated sporonts may be present as well. Similar to other
oocysts. Sexual transmission by direct oral- coccidians, acid-fast and auramine-rhodamine
anal contact has been postulated. The oocysts staining can be used to demonstrate organisms
are in stool. 
andvery
mayresistant to environmental
remain viable for months ifconditions
kept cool  Effective treatment is with TMP-SMZ,

Scohiiszto. genic  and  s  ppor ogenic  stages  have

and m pyhr oism -nintr eo-f sur lf andtioaiznin, eo,r  pr ir m
 pehtahtaem imaaquininee
 been found in the epithelial cells of the distal chloroquine phosphate. TMP- SMZ is the
duodenum and proximal jejunum of the drug of choice. Therapy must be continued
intestines. Eventually, oocysts are passed in indefinitely for immunosuppressed or
the stool. Oocysts continue to mature within immunocompromisedpatients withrecurrent
withr ecurrent or
48 hours after stool evacuation and are then  persistent cystoisosporiasis.
cystoisosporiasis. Since transmission
transmission
infectious. Chronic infections develop in some is via infective oocysts, meticulous hygiene and
 patients and oocysts can be shed for several sanitation are essential for preventing spread of
months to years.  the disease. 
Patients who are immunocompromised, E. Cyclospora cayetanensis 
cayetanensis 
 particularly those with AIDS, often present
with profuse diarrhea associated with weakness, Cyclospora cayetanesisis an acid-fast
anorexia, and weight loss. Bowel movements variable enteric coccidian that can infect
are watery, soft, foamy, and offensive smelling,  travelers in developing countries as well as  
suggestive of a malabsorption
Aside from AIDS patients,process.
C. belli  has immunosuppressed
 patients. hostsulated
including
Spher ical unsporulated
Spherical unspor oocystAIDS
oocysts,
s, 8 to
 been reported
report ed to cause
caus e opportunistic
opportu nistic diarrhea
di arrhea 10 µm in size (twice the size of Cryptosporidium)
in patients with Hodgkin’s disease, non-
non - or ovoid sporocysts, 4 by 6.3 µm in size, are  
Hodgkin’s, human T-cell
T -cell leukemia, and  passed in the stools, and sporulation occurs
acute lymphoblastic leukemia. A case report within approximately 7 to 13 days. Complete
in Iran described a patient with mediastinal sporulation produces two sporocysts that
thymoma with an eight-month history of rupture to reveal two crescent-shaped sporozoites
sporozoites
recurrent diarrhea. On direct fecal smear   measuring 1.2 by 9.0 µm. The transmission of  
 

394   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Cyclospora is thought to be fecal-oral, although in severely immunocompromised patients,

direct person to person transmission has not chronic suppressive therapy may be necessary
 been documented and may not occur since until immune function recovers. 
sporulation takes a number of days. Outbreaks F. Sarcocystis spp.  
linked to contaminated water and various types
of fresh produce such as raspberries, basil, and Sarcocystis spp. include the organism once
lettuce have been reported.  known as Isospora hominis as part of their life  
Cyclospora infection causes disease cycle. Two well-described species are Sarcocystis
manifestations typical of a small bowel bovihominis(bovine) andS. suihominis(porcine).
 pathogen, including
includi ng upper gastrointestinal
gastroin testinal   When raw or poorly cooked meat from infected
symptoms, malabsorption, weight loss, and animals is ingested by a human host, gamogony  
moderate to marked erythema of the distal occurs within the intestinal cells and leads
duodenum.
duodenu m. Two
Two to 11 days following exposure, to the production of sporocysts in the stool.
malaise and low grade fever develops and Humans who ingest meat containing mature
watery diarrhea ensues. Associated symptoms sarcocysts serve as definitive hosts. Fever, severe
include extreme fatigue, anorexia, myalgia, diarrhea, abdominal pain, and weight loss from
vomiting, and weight loss, with spontaneous infection in immunocompromised hosts have
remission of diarrhea in 3 to 4 days followed  been reported,
report ed, but are
ar e relatively uncommon.
uncommo n. 
 by frequent
frequen t relapses lasting from 4 to 7 weeks. Eosinophilic enteritis and ulcerative enterocolitis
enterocolitis
AIDS patients may take longer to resolve may complicate the course of the disease,
(up to 12 weeks) and may develop chronic  especially in severe disease. Humans can also  
diaser ar hse aisif a tkr enaotw
mnenctoim
s p edh.e Bcilliinair cyal
  nloictaitnioitnia. tT stehr evesar scao cyisdtesnthaal tindt er  diaitne huosm
eloe p
vm wuesvcelr e,
tsa;nhom
 presentation of patients infected with this do not usually cause permanent damage. Some
organism is similar to that of patients infected  patients occasionally experience fever,
fever, myalgia,
with Cryptosporidium . In clean wet mounts, weakness, and eosinophilia. Symptomatic
the organisms are seen as non-refractilespheres treatment is usually sufficient and no  specific
specific
and are acid-fast variable with the modified treatment is known to affect the muscle stages
acid-fast stains; those that are unstained appear of Sarcocystis spp. Corticosteroids have been
as glassy, wrinkled spheres. Modified acid -fast used to treat occasional allergic inflammatory
stains show the oocysts as light pink to deep reactions that occur when cysts rupture.  
red, and some contain granules or have a Sporocysts recovered from stool are broadly
 bubbly appearance.
appearance. Oocysts
Oocysts will auto
autofluoresce
fluoresce oval, measuring 9 by 16 µm
µ m in size and contain
 bright green
g reen or intense
int ense blue under ultraviolet
ul traviolet four mature sporozoites and the residual
light. Patients do not respond to antibiotics  body. Normally,
No rmally, two
t wo sporocysts
sporocy sts are contained
commonly used for diarrheal treatment   within the oocyst (similar to C. belli); however, 
such as fluoroquinolones,
metronidazole.
metronida macrolides,
zole. In otherwise healthy and
individuals, in Sarcocystis infections, the sporocysts are
usually already released from the oocyst and
the disease appears to be self-limiting and may normally are seen singly. They are larger than
not require treatment other than supportive  Cryptosporidium oocysts, which contain four  
remedies. In immunocompromised patients or sporozoites. 
severe disease leading
leading to dehydration, TMP-
TMP - For infections in which humans serve as
SMZ, one double strength tablet four times a definitive hosts, prevention involves adequate
day is currently the drug of choice. Duration cooking of beef and pork. For infections in
of treatment depends on immune status, and  which humans are intermediate
i ntermediate hosts, careful 
 

CHAPTER 8: Special Topics in Parasitology   395 

disposal of animal feces possibly containing in HIV-infected patients and appears to have
infective sporocysts can minimize risk of an ever expanding clinicopathologic spectrum
infection.  among immunocompromised hosts. Severely
immunocompromised patients may have
G. Microsporidia  
Microsporidia
concurrent infections causing diarrhea on top
The microsporidia are obligate intracellular of microsporidia, and so reponse to empiric
 parasites that have been recognized in a  therapy may be blunted and misleading. To  
variety of animals. The organisms found in date, nine genera have been recognized in
humans tend to be smaller, ranging from  humans (Table 8.4). These are Entero
 Enterocytozoo
cytozoon,
n,
1.5 to 2 µm long. They are characterized  Encephali
 Enceph alitozoon, Ple
tozoon  Pleist
istophora, Trachipleistophora,
ophora
 by having spores containin
co ntainingg a polar tubule   a, Nosema
 Brachiola
 Brachiol  Nosema, Vittaforma, Microsp oridium, 
 Microsporidium
which serves as the extrusion mechanism for and Septata. Enterocytozoon bieneusi and the
injecting the spore content into the host cell. three species of Encep
 Encephalitoz oonare the primary
halitozoon
Human microsporidiosis remained rare until microsporidia species associated with human
the AIDS epidemic. Microsporidiosis is an infections. Intestinal microsporidiosis due to
important emerging
emerging opportunistic infection   Enterocytozoonbieneusi causes chronic diarrhea, 

Table 8.4. Microsporidial infections in immunocompromised patients  

Clinicalsyndromes
Enterocytozoonbieneusi  AIDS

Keratoconjunctivitis, rhinosinusitis, peritonitis, fulminant

Encephaii 
t lo zoonhell 
e
  m  AIDS Conjunctivitis, keratoconjunctivitis, bronchiolitis,

ncep a ozoon n es na s  AIDS Diarrhea, disseminated disease  

Pleistophora  AIDS Myositis

TrachipIeistophorahominis  AIDS Myositis

Brachiolavesicularum  AIDS Myositis

Nosemaocularum  
Nosemaocularum Non-HIV Keratitis

Vittaformacornea  
Vittaformacornea Non-HIV Keratitis

malabsorption, and wasting

wasting in AIDS patients. The life cycle includes repeated divisions
Infections with the other species are rare and  by binary fission (merogony) or multiple
sporadic.  fissions (schizogony) and spore
The spore is the only life cycle stage able (sporogony). Both merogony andproduction
sporogony 
to survive outside the host cell (Figure 8.8). can occur in the same cell at the same time.
Acquisition of infection is through ingestion of During sporogony, a thick spore wall is formed.
the spores, and once inside the body,
body, single cells The spores are released into the intestinal
are infected by injection of infective sporoplasm lumen and are passed out with the stool.  
through the polar tubule. The microsporidia Spores are environmentally resistant and can
multiply extensively within a parasitophorous then be ingested by prospective hosts. In the
 vacuole (genus  Encephalitozoon ) or directly  immunocompromised, microsporidial infection
in the host cell cytoplasm (e.g., E. bieneusi). can lead to overwhelming disease and death.  

396   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Figure 8.8. Life cycle of microsporidia

 

CHAPTER 8: Special Topics in Parasitology   397 

Diagnosis of microsporidial infections   octreotide, primaquine, lomotil, loperamide,

is by demonstration of spores in feces, urine, and other anti-diarrheal agents. Fumagillin, an
and other body fluids
fluids or
 or within tissues. This antibiotic derived from Aspergillus fumigatus,
may be challenging due to the small spore has activity against microsporidia,
microsporidia, and solutions
size and irregular spore excretion. A number applied topically have been used in corneal
of techniques for increasing yield for recovery infections. In a randomized, double-blind,
and identification of microsporidia in clinical   placebo-controll
 placebo- controlledtrial
edtrial of fumagillin
fumagill in inpatients
inpatient s 
specimens are available. The organisms can be with chronic E. bieneusi infection, clearance
identified in routine histologic preparations. of microsporidia occurred in all six of the
The spores take on a refractile gold appearance   patients in the fumagillin
fumagill in group, as compared 
in formalin-fixed, paraffin
  paraffin -embedded, routine with none in the placebo group. HIV-infected
hematoxylin-and-eosin-stained sections. Spores  patients should be started on highly active anti-
are occasionally seen very well by using
u sing  retroviral therapy since this facilitates clearance
the periodic acid-Schiff (PAS) stain, the of infection. 
methenamine-silver stain, tissue Gram’s stain, H. Strongyloides stercoralis 
stercoralis 
or acid-fast stains. Spores have a small, PAS-
 positivee posterior body,
 positiv body , while spore coat will is potentially one
Strongyloides stercoralis
stain with silver. Spores are acid-fast variable.  of the deadliest helminthic parasites due to its
Microsporidia spores are difficult to ability to complete its life cycle entirely within
appreciate in stool wet mounts for ova and the humanthebody. Autoinfection can dramatically
 parasites. Chemofluorescent agents such  increase parasite burden of adult. In normal  
iteaxlco2f 8luionr cr W
aUsvC ear sietese2nM iv,itFyu bnugit-Fmluaoyr, bionr d
sitR  usoustasl, itm
h hemauntoein
mf echtiaonisim s;a bnuatgeaabr loegtahtir onugohf
s  m
non-selectively to debris and cause false cell-mediated immunity unbridles this cycle,
 positive results. Use of antisera conjugated allowing for overwhelming and fatal infections. 
with fluorescent
fluorescent reporters
 reporters in detecting spores Filariform larvae are the infective stage;
in clinicalspecimens increases
in creasesspecifiticy. PCR and are acquired by skin contact with fecally-
methods are available as research tools and may contaminated soil. The larva penetrates intact
 be useful as adjuncts for diagnosis
diagnosi s in persistently
persistent ly human skin and sequentially migrates through
negative clinical specimens when clinical the heart and lungs, passes up the trachea, is
suspicion remains high.  In vitro cell culture swallowed, and finally grows to maturity in
remains the gold standard but is not practical the gastrointestinal tract. Eggs are passed out
in routine clinical diagnosis. Serologic tests in the stool, but may hatch before elimination
(carbon immunoassay, indirect IFA, ELISA, offeces.Non-infectiverhabditiformlarvae may
counterimmunoelectrophoresis,
counterimmunoelectrophoresis, and Western transform to infective filariform larvae while still
 blotting) have been used to demonstrate IgG  in the gastrointestinal tract or on the perianal  

and IgM antibodies

of uncertain utility to
in microsporidia,
demonstating but are
active surface. These
or skin and can thenthe
reinitiate penetrate theThis
life cycle. bowelcycle
wall
infections.  can occur asymptomatically at a very low level
Treatment for ocular, intestinal, and over many years except for a mild eosinophilia. 
disseminated disease is with albendazole. Immunocompromised patients who have
Itraconazole can also be used to treat ocular,  previously been infected with Strongyloides
nasal, and paranasal sinus infection caused by E. or who acquire new infection are at risk for
cuniculi parasites
 parasites when albendazole
albendazol e fails. Other hyperinfection. Development or exacerbation
exacerbation
 agents that have been tried are metronidazole,  of gastrointestinal and pulmonary symptoms  

398   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

with detection of increased numbers of larvae and 99% specific, however infections with
in stool and/or sputum is the hallmark of filariae or Ascar is can lead to false-positives
 Ascaris
hyperinfection. Among theconditions that may results and does not distinguish active from
trigger hyperinfection are AIDS, glucocorticoid  past infections. 
treatment, and Human T-lymphotropic virus In disseminated strongyloi
s trongyloidiasis,
diasis, filariform
type 1 (HTLV-1) infection.  larvae can be found in stool samples as well as
Glucocorticoids are strongly associated
associated  sputum, bronchoalveolar lavage fluid, pleural 
with transforming chronic strongyloidiasis to fluid, peritoneal fluid; and surgical drainage
hyperinfection.
hyperinfection. Aside from the decrease in cell- fluid. The
fluid.  The typical rhabditiform larvae of S.
mediated immunity, corticosteroids increase
increase   stercoralis are characterized by short buccal
the production, mainly in the intestinal wall, capsule with an open mouth and the presence 
of ecdysteroid-like substances which may act of a conspicuous genital primodial packet  
as molting signals and increase production of of cells. Extreme care should be taken when
auto-infective larvae.  working with materials from a patient suspected
Patients who
who have developed severe systemic
syste mic  of having strongyloidiasis because of possible
S. stercoralis infections include those with filariform larvae in the specimen. Gloves should
hematologic malignancies, connective tissue  be worn tto
opprevent
revent skin penetration by these
these
disease such as systemic lupus erythematosus, larval forms. 
solid organ transplant recipients, and other Thiabendazole is the drug of choice in both
underlying immunosuppresive
When migrating increaseconditions.
larvae increase in numbers,  uncomplicated
due to potentiallyand disseminated
severe infections,
side effects, but 
alternative
ao bf  duonm
exi pnal linceodm b tsemaniadore pmeeanteindgei p
 palacitner  tisisowditehs meotahtter m
ane b
ch r mr oes p
edit. hInivae p
apytw ctienctainved, ar l b aziozeled,
anednodm
enteric bacteria may occur. This is likely due open-labelled study comparing a seven-day
to larval penetration of the bowel leading to course of oral albendazole 800 mg day versus
translocation of bowel flora into the bloodstream a single oral dose of ivermectin 200 µg,
µg , cure
either from the sites of microperforation, rates were 38.1% and 76.2%, respectively. In
attached to the larva, or excreted by
b y the larvae a different randomized trial in rural Zanzibar,
in circulation.  a single dose of 200 µg/kg of ivermectin and
Diagnosis of Strongyloides infection is 400 mg/day for 3 days of albendazole in 301
 best made by detecting rhabditifor
rhab ditiform
m larvae in children with Strongyloides stercoralis resulted
concentrates of multiple stools. Single stool in cure rates of 83% and 45%, respectively. In
exam may miss up to 70% of cases; while three another open randomized study of 60 patients
stool samples increases diagnostic sensitivity with Strongyloides stercoralis infection treated
to 50% and seven serial stool samples
sam ples raises with albendazole 400 mg/day for 3 days or  
sensitivity to more
m ore than 90%.  ivermectin 150 to 200 µg/kg single dose,  
S. stercoralis resides in the duodenum,  parasitol
 parasitological
and 83%ogical cure
curlatter.
for the e with  the
th e former was
w as 38%
making recovery of the larvae in the stool
difficult in
difficult  in patients with low worm burden. The efficacy of therapy should be monitored
Ancillary techniques like the Entero-Test string   with serial examinations until a negative stool or
capsule and the duodenojejunal aspiration may upper small bowel fluid is obtained.
obtain ed. Treatment
increase yield. Other techniques for recovering failure and relapse are not infrequent. In patients
Strongyloides larvae include the Harada-Mori with the hyperinfection syndrome, case fatality
and petridish culture techniques. ELISA to rates are high (up to 87%) despite appropriate
 detect Strongyloides antibody is 88% sensitive   anthelminthic therapy due to the concomitant 

CHAPTER 8: Special Topics in Parasitology   399 

immunosuppression and bacteremia. Detection disease with focal granulomatous lesions in

and eradication of Strongyloides infection prior the brain. Conditions associated with GAE
to initiation of immunosuppressive therapy   include amebic keratitis, skin ulcers, liver
is important in preventing the occurrence of disease, pneumonitis, diabetes mellitus, renal
disseminated strongyloidiasis.   failure, rhinitis, pharyngitis, and tuberculosis.
Predisposing factors include alcoholism,
Other Parasitic Infections 
 pregnancy,
 pregnancy, SLE,
SLE, hematologic
hematologic disorders, AIDS, 
 Entamoeba histolytica, the cause of amebic
histolytica chemotherapy, radiation therapy, and steroid
dysentery and amebic liver abscess, infects a treatment. Acanthamoeba spp. are now well-
large number of people throughout the world. described as opportunistic pathogens in AIDS
Morbidity and mortality due to E. histolytica  patients, particularly
particular ly those with a low
l ow CD4+  
varies, depending on the geographic area, cell count. Unfortunately, the diagnosis of
organism strain, and patient immune status. this rare infection requires a high index of
In patients with intestinal disease, symptoms suspicion, since both clinical and histological
range from minimal to acute or chronic amebic findings may mimic those of disseminated
colitis. Extraintestinal infection occurs when fungal or algal disease. Clinical manifestations
the organisms invade the mucosal lining and of AIDS patients infected with Acantha
 Acanthamoeba
moeba
are carried via the bloodstream to the liver. E. include non-specific systemic complaints
histolytica infection in an immunocompromised such as fever and chills, nasal congestion,
host can lead to a higher risk of extraintestinal neurologic symptoms, andpatients
musculoskeletal and 
disease. AIDS patients in endemic areas are at  cutaneous lesions. Some may develop
high Br l ias skt of oc yr  st sie svheor m
e iinnif  se,caticoonm.  mon commensal eskr yinthlem
sioatnosu, sonr  oa b onviecr  u1l0c0er actaisves  of
duscl es,secsh. r O
in the colon, is considered a non-pathogenic GAE caused by Acanth
 Acanthamoeb
amoebaa spp. have been
intestinal protozoan. However, in the absence recorded worldwide and 53 of these occured in
of other parasites, bacteria or viruses, it has been AIDS patients in the United States. Although
known to cause diarrhea, and constitutional  Acanthamoeb
 Acanth a infection typically stimulates
amoeba
symptoms in immunocompromised hosts. B. granuloma formation, the response in AIDS
hominis is the most frequently detected parasite  patients is minimal or absent due to severe
among adults; including immunocompromised immunosuppression.  
 patients, institutionali
institu tionalized
zed psychiatric
psychiatr ic or elderly The leptomyxid ameba  Balamuthia
subjects, immigrants from developing countries, mandrillaris is uncommon and was previously
and travelers to developing countries. In the thought to have no pathogenic potential. B.
same study population,  B. hominis showed a mandrillaris is very similar to GAE and has
significant correlation with gastrointestinal an unknown incubation period. Its clinical
symptoms only when detected in subjects course tends to be subacute to chronic. There 
with severe immunodepression. Its role as   have beenworldwide,
over 74 cases
an opportunistic parasite has been described   reported 11ofof B.whom
mandrillariss GAE
mandrillari
were AIDS
among HIV-infected patients, with a prevalence  patients in the USA. Giardia duodenalis is a
of up to 52% among in this population.  parasitic flagellate co mmonly found in  many 
commonly
Free-living ameba can cause severe  parts of the world. Giardia infection generally
disease in immunocompromised individuals. manifests as intestinal diarrhea. Infection  
Granulomatous amebic encephalitis (GAE) in healthy hosts is usually self-limited, but
caused by Acanthamoeb
 Acanthamoebaa spp. and Balamuthia may contribute to morbidity from diarrhea
 mandrillaris occurs as a subacute or chronic   especially in malnourished children and the  

400   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

elderly. Inadequate sanitation is a major risk million cases of malaria occur every year, at least
factor for acquisition of giardiasis, and drinking a million of which cause deaths. An estimated
of contaminated water is the usual mode of 30 to 36 million people are living with HIV in
infection to travelers in developing countries. Africa, resulting in more than 3 million deaths
AIDS patients presenting with diarrhea should every year. Malaria is more common and severe
 be screened for
fo r giardiasis.
giardi asis. Trophozoites
Trop hozoites can in adults with HIV, pregnant women, and
 be seen on wet mounts and are better seen  children. 
with Giemsa staining. Lateral flow assays Guidelines for treatments of the two
that detect antigen in stool are commercially infections are often conflicting. There are also
available and are usually combined with   issues around drug resistance and cross-reactions 
Cryptosporidium. While treatment of giardiasis  between drugs,
dru gs, as well as concerns that some
som e
in healthy hosts is straighttforward with medications used to treatHIV-positive persons
metronidazole or tinidazole, those who are could be harmful for malaria treatment in
severely immunocompromised may require certain settings. 
longer duration of treatment and may have HIV not only increases the incidence and
more frequent relapse. severity of malaria, it also compromises malaria
Epidemiological studies also suggest that treatment. HIV infection can decrease the
malaria is a deadly co-factor for AIDS. The response to standard antimalarial treatment. For
results of Ugandan study by Whitworth, et al. HIV-positive adults with a weakened immune
involving 484 participants making 7,220 clinic system (a low CD4 count), antimalarial drugs
visits between 1990 and 1998 did show an   are less likely to be effective. Malaria contributes
contributes 
iancdr  p
easr eadsif tr emqia
uen(1c1y.8o% r iaith(2H.0I%
f   c)liansiscoacliamteadlaw V)-  p nliencwr heaicseh incavni p
toeoa p r aloltoeandtiam
llyonacgcH
eleIr Va- p
te otshiteive
1 infection as opposed to their HIV-negative  progression from HIV to AIDS.  
counterparts, 0.7% and 6.3%, respectively. In a prospective, cross-sectional study, in
Lower CD4 cell counts were associated with the Central Hospital of Maputo, Mozambique
increased parasite densities and increased risk last October 2006, risk factors for fatal outcome
of clinical malaria. In addition, infants born to were determined and impact of HIV on the
mothers co-infected with HIV and malaria had accuracy of malaria diagnosis was assessed. 
a four-fold higher mortality rate than infants Among 333 included patients, 15% (51/333)  
 born to mothers infected with either HIV or had “presumptive
“presumptive  malaria,”
malaria,” 10%
 10% (28 of 285
malaria alone.  tested persons) had positive malaria blood slides,
There is considerable geographical overlap
overlap while 69.1% (188/272) were HIV positive.
 between malaria and HIV and increasing Seven percent (n=23) had confirmed malaria,
evidence on a direct link with one disease after the diagnosis was rejected in patients with
making the other worse and more difficult
difficult  to  neck stiffness or symptom duration longer than  
treat.
Malaria and HIV/AIDS are two of the two weeks
(n=19) (n=5) and
or unknown persons
malaria with
blood negative
slide (n=4).
most important infectious diseases worldwide, Clinical stage of HIV infection, hypotension,
accounting for almost 9% of the total burden and hypoglycemia were associated with fatal  
of disease in sub-Saharan Africa (Figure  outcome. The study suggests that the fraction
8.9). Malaria and HIV cause more than four of febrile illness attributable to malaria is lower
million deaths a year combined, and are both in HIV positive adults. HIV testing should be
concentrated primarily in sub-Saharan Africa, considered early in evaluation of patients with
 Asia, and South America. More than 500  suspected malaria.

CHAPTER 8: Special Topics in Parasitology   401 

Figure 8.9. Distribution of malaria

Superimposed
Superimposed endemic parasitic infections  parasitic infections
infection s among HIV infected
infect ed and
in tropical countries present a major health uninfected children with diarrhea in Thailand,
 problem among HIV-infected individuals intestinal parasites were identified in the
and malnourished hosts. Non-opportunistic stool specimens of 27 out of 82 (33%) HIVHI V
intestinal parasites such as hookworms, infected children and were significantly higher
Opisthorchis viverrini , and  A. lumbricoides
lumbricoides than the uninfected children [12 out of 80
are common regardless of HIV status. In a (15%)]. In Africa faster progression to AIDS
  prospective
 prospecti ve observational
observ ational study
st udy on intestinal
i ntestinal   and increased HIV viral load occurred in areas 

402   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

highly endemic for helminths. These long- Bangkok, Thailand.Southeast

Thailand.S outheast AsianJ Trop
Trop
lasting parasitic infections cause widespread Med Public Health. 2001;32(4):770 – 775.
775.
activation and dysregulation, inducing a DuPont HL, Chapelli CL, Sterling CR,
dominant Th2 cytokine immune profile
immune profile and
 and Okhuysen PC, Rose JB, Jakubowski W.
an immune hyporesponsive state. Helminths The infectivity of Cryptosporidium parvum
induce a predominantly Th2 response, and this in healthy volunteers. N Engl J Med.
has been associated with progression of HIV.   1995;332(13):855 – 99..
Endemic tropical non-opportunistic parasitic Farthing MJ. Clinical aspects of human
infections present a special and significant cryptosporidiosis.
cryptosporidiosis. Contrib Microbiol.
risk in immunocompromised individuals. It   2000;6:50 – 7
74.
4. 
is important for the clinicians and laboratory Foreman EB, Abraham PJ, Garland JL. Not
 personnel to be aware of the p
problems
roblems these your typical Strongyloides infection: a
organisms can cause and recognize their clinical literature review
r eview and case study
study.South Med
relevance.  J. 2006;99(8):847 – 52.
52.
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Gassama A, Sow PS, Fall F, Camara P, Gueye-
 Ndiaye A, Seng R, et al. Ordinary and
Abubakar I, Aliyu S, Arumugam C, Usman N, opportunistic enteropathogens associated
Hunter P. Treatment of cryptosporodiosis with diarrhea in Senegalese adults in
in immunocompromised individuals: relation to human immunodeficiency virus
systematic review and meta-analysis. Br J serostatus.
8. 
Int J Infect Dis. 2001;5(4):192 –  
Clin Pharmacol. 2007; 63(4):387 – 93.
93. 

9e6s;ea1r 9ch97G
AID1S9R   – r 
1o9u9 p8..BM
ienaniilaal  R  ir t  p1i9n9e5s – 
(Pe phiol p ): r thunM
imom
Heyw ocFo.m pPar or amsiitsiecddihseoasstess:  in
Research Institute for Tropical Medicine, cryptosporidiasis, isosporiasis and
Department of Health; 1999.  strongyloidiasis.
strongyloidiasis. Gastroenterol Clin
C lin North
Essid R, Mousli M, Aoun K, Abdelmalek R, Am. 1996; 25(3):691 – 707.
707. 
Mellouli F, Kanoun F, et al. Identification Hunter P,Nichols G. Epidemiology
Epidemi ology andclinical
andcl inical
of Cryptosporidium species infecting features of Cryptosporidium infection
humans in Tunisia. Am J Trop Med Hyg. in immunocompromised patients. Clin
2008;79(5):702 – 5.5. Microbiol Rev. 2002;15(1):145 – 5
54.
4. 
Berg A, Patel S, Langeland N, Blomberg   Husni RN, Gordon SM, Longworth DL, Adal
B. Falciparum malaria and HIV-  KA. Disseminated Strongyloides stercoralis
1 in hospitalized adults in Maputo, infection in an immunocompetent
i mmunocompetent patient.
Mozambique: does HIV-infection Clin Infect Dis. 1996;23(3):663.
obscure the malaria diagnosis? Malaria J. Kadappu K, Nagaraja M, Rao P, Shastry  
2008;7:252.  B. Azithromycin as treatment
Chaisson RE, Gallant JE, Keruly JC, Moore for cryptosporidiosisvirus
in human  
RD. Impact of opportunistic disease on immunodeficiency disease. J Postgrad  
survival in patients with HIV infection. Med. 2002;8(3):179 – 81. 81.
AIDS. 1998;12:29 – 3 33.
3. Keiser P, Nutman T.Strongyloides stercoralis in
Chokephaibulkit K, Wanachiwanawin D, immunocompromised population. Clin
Tosasuk K, Pavipok J, Vanprapar, N, Microbiol Rev. 2004;17(1):208 – 1
17.7. 
Chearskul S. Intestinal parasitic infections Lim S, Katz K, Krajden S, Fuksa M, Keystone J,
among HIV-infected and uninfected Kain K. Complicated and fatalStrongyloides
 children hospitalized with diarrhea in   infection in Canadians: risk facto
factors,
rs, 

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diagnosis and management. CMAJ. Montoya JG, Liesenfeld O. Toxoplasmosis.  

2004;171(5):479 – 84. 84. Lancet. 2004;363(9425):1965 – 77..
Mac Kenzie WR, Hoxie NJ, Proctor ME, Reithinger R, Kamya M, Whitty C, Dorsey G,
Gradus MS, Blair, KA, Peterson DE, et Vermund
Verm und S. The link between malaria and
al. A massive outbreak in Milwaukee of HIV in Africa. BMJ. 2009;338:b2141. 
Cryptosporidium infection transmitted Shrikhande S, Chande C, Shegokar V, Powar  
through the public water supply. N Engl J  R.  Pulmonary cryptosporidiosis in HIV
Med. 1994;331(3):161 – 7. 7. negative, immunocompromised host.
Manaloto
Manal oto CR,
C R, Perrautl
Perrautl JG, Caringal LT
LT.. Natural   Indian J Pathol Microbiol. 2009;52(2:)267 –  
history of HIV infection in Filipino 8.
commercial sex workers. J Acquir Immune Siddiqui AA, Berk, SL. Diagnosis of Strongyloides
Strongyloides
Defic Syndr. 1994;7:1157– 68.
68.  stercoralisinfection. CID. 2001;33:1040 – 7
7.. 
Marti H, Haji HJ, Savioli L, Chwaya HM, Mgeni Suputamongkol Y, Kungpanichkul N,
AF,
AF, Ameir JS, et al. A com
comparative
parative trial of a Silpasakorn S, Beeching NJ. Efficacy and
single-dose ivermectin versus three days of safety of a single-dose veterinary preparation
albendazole for treatment of Strongyloides of ivermectin versus 7-day high-dose
 stercoralis and other soil-transmitted albendazole for chronic strongyloidiasi.sInt
helminth infections in children. Am J Trop J Antimicrob Agents. 2008;31(1):46 – 9. 
Med Hyg. 1996;55(5):477 – 81. 81. Vadlamudii S, Chi D,KrishnaswamyG
Vadlamud D,KrishnaswamyG.Intestinal
Meamar A, Rezaian M, Mirzaei A, Zahabiun   strongyloidiasis and hyperinfection
F, Faghihi A,Oormazdi H, et al. Severe   syndrome. Clin Mol Allergy. 2006;4:8. 
diarrhea due to
with
 Isospora belli
in a patient
thymoma. J Microbio Immuno Infect.   Whitworth J, Morgan D, Quigley M, Smith A,
Mayanja B, Eotu H, et al. Effect of HIV-
HIV-ll 
2009;42:526 – 9.
9. and increasing immunosuppression on
Molina J, Tourneur M, Sarfati C, Chevret S, malaria parasitemia and clinical episodes
de Gouvello A, Gobert J, et al. Fumagillin in adults in rural Uganda: a cohort
cohor t study.
treatment of intestinal microsporidiosis. N Lancet. 2000;356(9235):1051 – 6 6..
Engl J Med. 2002; 346:1963 – 9.
9 . 
 

404   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Neglec ted Tr opic al Diseases 

Vicente Y. Belizario, Jr., Amelia M. Breyre, Francis Isidore G. Totañes

eglected Tropical Diseases (NTDs) are relatively neglected by research; (b) they have an
a biologically diverse group of chronic  important impact on morbidity and mortality; 
diseases unified by their strong association and (c) they can be prevented or possibly
p ossibly
with poverty. NTDs are caused by a disparate eliminated using effective and feasible strategies.  
group of pathogens, including viruses, bacteria, NTD Disease Distribution 
 protozoa, and helminths. Their modes of  
transmission also vary tremendously; some Internationally, more than a sixth of the
are parasitic diseases that spread through hosts world’s population suffer from one or more
and vectors (e.g., fish, snails, mosquitoes, etc.),  NTDs. The distribut
d istribution
ion of these
t hese diseases
diseas es varies
while others are transmitted through water. All tremendously regionally. Figure 8.10 is a map
 NTDs, however,
however , share several of the following
followi ng that shows the global distribution and overlap
features: (a) they affect populations with low of the most common NTDs. One-third of the
visibility and little political voice; they are  global prevalence of intestinal helminthiasis, and  

Figure 8.10. Global distribution of neglected tr opical

opical diseases (NTDs) by nu
number
mber of NTDs per country

a majority of foodborne trematode infections

infections schistosomiasis are also in this region. Table 8.5
can be found in Southeast Asia and China. enumerates the NTDs targeted by the World
Approximately one-half of the active trachoma Health Organization (WHO) for control, with
infections, and a significant proportion of the a focus on those endemic to the Philippines. 
 number of cases of lymphatic filariasis (LF) and 

CHAPTER 8: Special Topics in Parasitology   405 

Table 8.5. Neglected tropical diseases targeted year is attributable to schistosomiasis in the
by the WHO Philippines. 
The concept of disability-adjusted life years
Disease in the (DALYs) was developed to quantitatively assess
Philippines the burden of individual diseases. DALYs take
into account both premature mortality (years
of life lost) and disability (years of life lived  
with a disability weighted by the severity of the
disability). DALYs assigned to a specific disease
Dracunculiasis (guinea-worm disease)*
at a particular time gives the estimated sum of  
Echinococcosis*
years of potential life lost due to premature
Fascioliasis*
mortality and years of productive life lost. For
example, it is estimated that 5,941,000 years of
 potential
 potenti al life are lost globally due to lymphatic
Leishmaniasis*
filariasis. The use of DALYs, however, is
Leprosy
somewhat controversial since its design contains
Lymphatic filariasis*
inherent systematic flaws
flaws that
 that result in under
Onchocerciasis* evaluation of the importance of chronic diseases
Rabies such as NTDs. Because DALYs focus more on
Schistosomiasis* individual risk rather than the ecology of the
Soil-transmitted helminthiasis* disease, the weight of disability for chronic  
pover ty tend to  b
matthed.context of   p
uinsdeaesr estin
d  b e
*Diseases caused by parasites The concept of a quality-adjusted life years 
(QALYs) is an alternative means to quantify 
losses attributableto disease. The QALYs system 
Burden of Neglect 
uses estimates from preference-based health
 NTDs disproportionat
dispropo rtionately
ely affect the poorest related quality-of-life interviews administered to
and most marginalized, including the rural groups of patients or to members of the general
 poor, residents of urban slums, out of school  population
 populat ion in an endemic community.
communi ty. QALYs
youth, women, and indigenous people whose are better able to assess the societal context  
access to formal health services are limited for of disease impact that may not be accurately
cultural, social, or geographic reasons. It is captured by DALYs. Improvement of DALYs
difficult to quantify the social burden associated calculations and development of new metrics
with crippling disabilities and reductions in such as QALYs are ongoing.
ongoing . Such efforts are an
 productivity
 producti vity of individu
i ndividuals
als and communities
com munities important aspect of assessment of the burden of  
caused by NTDs. Nevertheless, efforts to
measure the social and economic impact of  NTDs becau sehealth
because
determining they provide
pr ovide a mechanism
priorities.me
  chanism for
 NTDs can provide an understanding of the Polyparasitism 
extent of disease burden, and are important in
order to guide policies and prioritize disease The burden of NTDs is further compounded
control programs. Calculations of disability  by the fact that infection with multiple parasite
rate, for example, estimate that a total of   species, known as polyparasitism, is more often
45.4 days off-work lost per infected person/   the norm rather than the exception. Community  
 

406   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

surveys in Cote d’Ivoire  demonstrated infection (15-24 years old), and are more common in
with at least two intestinal parasites S (chistosoma males. A community parasitologic survey in
mansoni , soil-transmitted helminths and/or Cote d’Ivoire observed the highest frequency
intestinal protozoans) in 90.2% of the sampled of polyparasitism among adolescents and young
 populat ion. In Brazil, co-infection
 population. co-infecti on with Necato
 Necatorr adults (15-24 years old). 
americanus and S. mansoni was observed Geographic distribution, in relation to
in 41.0% of the community participants the overlapping of areas of endemicity, also  
examined. In a community survey in China, contributes to the occurrence of polyparasitism.
27.8% of those surveyed were infected with at In addition, behavioral factors may also be
least two parasite species (  Ascariss, Trichuris, and/ 
Ascari attributed to polyparasitism. Behavior related 
or S. japonicum). to personal hygiene can greatly contribute to
Local sentinel parasitologic surveys on infection of parasites with similar modes of
school-age children revealed multiple infections transmission. Socioeconomic status, living
with at least two helminths (soil-transmitted
(soil -transmitted conditions and access to health and sanitary
helminths, Schistosom a japonicum and/or
Schistosoma facilities also influence the distribution of
heterophyids) in 20.4% of those examined.  polyparasitism and parasitic infections in
Similarly, co-infections between different general. Individuals of lower socioeconomic
STH species and S. japonicum were observed status are less likely to have adequate water
in 13.1% of school-age children in indigenous and sanitation, and are less likely to invest in
 peoples in Davao del Norte.   bed nets for protection
protecti on against mosquito-borne
mosquito-bor ne
Although there are existing data   diseases. Similarly, low education levels have  
oi nditvhiedugallo b asr iteivcaldeinsecaeseasn, dth beur er daer ne ostf ill  no
 palr  p  btr  eantmasesnotc,iantedlewsistcholm piltieadncaeccweistsht por ef vf encti
im tivve
accurate estimations on the global burden of measures.  
 polyparas itism. Estimates
 polyparasitism. Est imates of populations
populat ions at A study by Ellis et al . that looked into
risk of multiple parasitic infections have been environmental and genetic predispositions to
described by looking into co-distribution rather  polypar asitism revealed that the risk of Ascari
 polyparasitism  Ascariss
than co-infection. Currently, there are limited and Trichuris co-infection, and S. japonicum
studies on the epidemiology and impact of and Trichuris co-infection were significantly
 polyparas itism. Research looking
 polyparasitism. lookin g into the use influenced by environmental or household
of polyparasitism as a parameter for effective conditions. Data from this study also revealed
disease control needs to be explored.   that there is a significant  genetic component
significant genetic
attributed to the risk of multiple
mu ltiple parasitic
Risk Factors for Po lyparasitism 
infections. This suggests that polyparasitism
The risk for polyparasitism, as with may aggregate in a familial pattern.  
individual infections, is influenced by the
combined
factors areeffects of several
attributed to hostfactors. Intrinsic
resistance that
Combined Impact of Polyparasitism 
Infection with multiple parasites intuitively
is influenced
influenced by
 by age and sex; and linked to results in higher morbidity than the impact of
frequency of exposure to infection, as well as a single infection. Malnutrition, as exemplified
development of immunity, or a combination  by wasting and stunting, arises as a result
of both. Ascaris and Trichuris infections, for of co-infections with malaria, STH, and/or
example, are most prevalent among the 5 to15 Schistosoma . Intestinal helminth infections
years old age group. Hookworm infections are cause intestinal inflammation and reduced
 most prevalent among middle-aged individuals  food intake, while malaria and schistosomiasis 

CHAPTER 8: Special Topics in Parasitology   407 

may trigger inflammatory cytokines that cause A synergistic effect has also been demonstrated
anorexia and induce a catabolic response.    between Ascar is and Trichuris infections, while
 Ascaris
Anemia in malaria infection is from  protectivee effects against
 protectiv agai nst malaria
mal aria have been
hemolysis and phagocytosis, while anemia from reported as a result of Ascar is or S. haematobium
 Ascaris
STH infections arises from chronic inte
intestinal
stinal infections.
 blood loss. A local study has demonstrated a
Strategic Approaches 
significant association between anemia and  
S.  japonicum infection. Given the different  A. Disease Surveillance
Surveillance  
mechanisms by which these infections bring Successful control of NTDs requires
about malnutrition and anemia, it is possible  
active surveillance programs at the local level
that the effects of co-infection on malnutrition in order to understand prevalence and disease
and anemia are additive. Studies in Kenya
distribution. Information on the burden of
revealed significantly lower hemoglobin among
 preschool and school age children with malaria-  NTDs is important
importa nt to determine
determin e specific disease
hookworm co-infections, compared to those
control and prevention strategies. On the other
hand, data on the geographical distribution of
with single infection. Another study done in
 Nigeria has shown lower mean hemoglobin
 NTDs can help direct resources to priority
priori ty areas,
especially in low-income countries where NTDs
among pregnant women with co-infections with are prevalent and resources are limited.
malaria and STH, although the difference was
not statistically significant.  Strengthening
 professi
 professionals the capacity
onals is important
i mportant of diagnosis
for early health s
diagnosi
An increasing number of studies have  
and treatment of cases. The local medical  
d tioi ntsh bs p
coe-minof necs tr ioatnesdws igthnifidcif af ner teanstsohceilam etewceiesn. technologist plays a major role in the
Helminth infection has been shown to elicit  performance of appropriate and accurate
an immune response that either results in
laboratory examinations. Accurate and timely 
the production of non-cytophilic antibodies
diagnosis will not only contribute to the proper
allowing increased susceptibility to further
treatment and early prevention of morbidity,
infection, or results in effective inflammatory  but also limit under- or over-reporting
over-rep orting of cases.
factors that offers protection against other
This will also result in reporting of reliable data
 parasitic infections. 
for proper disease monitoring
monitoring and surveillance. 
A notable increase in hookworm intensity B. Preventive Chemotherapy  
has been described with
wi th an increasing numberof The WHO defines  preventive chemotherapy
co-infecting helminths ( Ascaris
 Ascaris and S. mansoni).
as a major strategy for the control of a number
With regard to Ascaris infection, there was a
of parasitic diseases through morbidity and
significant increase in intensity of infection in
the presence of hookworm co-infection, and a  transmission control. Preventive chemotherapy  

co-infection. decrease in the presence

effect ofof hookworm
significant S. mansoni e  crr o  m
trr ec
h h en
ugm onintr isotlr aotf iolnymi ph
mdaesds  f dor rr u  gtheadcm s atic
The synergistic filariasis, onchocerciasis, schistosomiasis, and
infection with other helminth infections may be soil-transmitted helminthiasis. Given the
attributed to immunomodulation resulting in 
overlapping distribution of many NTDs, the
reduced cellular reactivity. T-regulatory cells WHO recommends combined control strategies
(Tr1) that secrete cytokines may play a role
in a drug-based rather than a disease-based
in the down-regulation of the host’s  immune
host’s immune
approach. The drug-based approach looks into
response to subsequent helminth infections,
 combined control of diseases that are targeted
thus resulting in greater intensities of infection.   by the same drugs. 

408   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Co-administration of praziquantel and are severely affected and underserved. For

albendazole, as well as co-administration of example, combined control of schistosomiasis
ivermectin and albendazole are recommended and STH infections may be conducted through
for use in mass treatment strategies in co- deworming of school children as part of the
endemic areas. Initial studies on the co- school health and nutrition program.  
administration of albendazole, praziquantel, Recognizing the importance of local health
and ivermectin have shown no clinically   systems, collaboration between the health  
significant pharmacokinetic
pharmacokinetic interactions when and education sectors, as well as the local
given together to healthy volunteers. These government units are important for a more
suggest that co-administration of the three   unified and concerted approach to the control 
control  
drugs is not expected to yield additional adverse of parasitic infectionsin the community.Futur
communi ty.Futuree
reactions; however, it is important to consider operational researches
researches on combined control
 precautionary
 precautio nary measures
measur es when administeri
ad ministering
ng strategies and their impact on the prevalence
drug combinations to infected individuals.   of NTDs and associated morbidities, as well
 Infrastruct
 Infrastructural
ural interventions: Since NTDs
interventions as cost- benefit
 benefit studies will be important in
are strongly associated with poverty, many of establishing evidence-based guidelines for
those afflicted
afflicted tend
 tend to have limited access to effective disease control.
clean water and proper sanitation facilities.
References 
Access to clean water is necessary in order for
any control program to have a lasting impact Belizario VY Jr, Totañes FG, de Leon WU,
WU ,
on reducing transmission.
transmission. Improvements in  Lumampao YF,Ciro RN. Soil-transmitt
Soil-t ransmitted
ed 
r er onger eadmtsoto biencsr ue pa pseleam
iendf ur acsatr iuonctaul p waenr etnedesswainthd h r eanr aisnitic
inef lemctiinotnhs aanmdoontghesr chionotel sctihnialdl  p
to promote habits that reduce transmission, indigenous people communities in Davao
such as proper hygiene.  del Norte. Acta Trop. 2011;120S:S12 – 118.
8.  
Belizario VY Jr, Totañes FG, de Leon WU,
C. Integrated Control  
Lumampao YF, Ciro RN. Sentinel
Because many of the NTDs are parasitic, surveillance of soil-transmitted
control of these diseases share similar helminthiasis in school children in selected
intervention strategies. They can be integrated local government units in the Philippines:
into a streamlined control program in order to follow-up assessment. Asia Pac J Public
increase efficiency and reduce costs. Integration Health. Forthcoming 2013.  
of health programs should consider capitalizing Briand V, Watier L, Le Hesran JY, Garcia A,
on existing infrastructure and programs.   Cot M. Coinfection with  Plasmodium
Targeting groups that are at high-risk for  falciparum and Schistosoma haematobium:
multiple infections, such as pre-school children,  Protective effect of schistosomiasis on

school-age children,
groups at high andmorbidity,
risk for farmers; assuch
well as
as malariaHyg.
Med in Senegalese
Seneg alese children?
2005;72(6):702 7.Am
 – 7 . J Trop
Trop
 pregnant and adolescent females, should  Conteh L,Engels T, Molyneux D.Socioeconomic
D.Socioeconomic
 be considered in integrating NTD control aspects of neglected tropical diseases.  
 programs. These groups can be reached Lancet. 2010;375(9710):239.
through the same channels, such as existing Drake LJ, Bundy DA. Multiple helminth
health and education systems with extended infections in children: Impact and control.
community-based coverage where populations  Parasitol. 2001;122:S73 – 81.
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Ellis MK, Raso G, Li YS, Rong Z, Chen HG, Lazdins J. Assessment of pharmacokinetic
McManus DP. Familial aggregation of drug interactions and tolerability of
human susceptibility to co- and multiple albendazole, praziquantel and ivermectin
helminth infections in a population from combinations.
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Trop Med Hyg.
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45.
5. 
Parasitol. 2007;37(10-3):1153 – 61.
61. Pullan RL, Bethony JM, Geiger SM, Cundill
Egwunyenga AO, Ajayi JA, Nmorsi OPG,   B, Correa-Oliveira R, Quillen RJ, et al.  
Duhlinska-Popova DD.  Plasmodium / Human helminth co-infection: analysis
intestinal helminth co-infections among of spatial patterns and risk factors in a
 pregnant Nigerian women. Mem Inst  Brazilian communi
c ommunity.
ty. PLoS Negl Trop
TropDis. 
Oswaldo Cruz. 2001;96(8):1055 – 9.
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Bellinger DC, Langdon GC, Manalo DL, of polyparasitism in humans: are we  
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8. Raso G, Luginbühl A, Adjoua CA, Tian-Bi  
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maendt  pf oartInetr esr nuantiitoentaol cD r o penict.a l
ev belaot ptm
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S , Pawab KK,
Hanpitakponga W, Na-Bangchangc C, 
 

410   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Preventive Chemotherapy 
Vicente Y. Belizario, Jr., Francis Isidore G. Totañes, Paul Lester C. Chua

eglected tropical diseases (NTDs) occur First, PCT utilizes population-based

most commonly in the setting of extreme  diagnosis in assessing the burden of helminth  
 poverty, especially among the rural poor and infections in a population through rapid
disadvantaged urban populations. Four of the community assessments and/or sentinel surveys
most prevalent NTDs are due to helminths which applied to a sample of its individuals. Surveys
are lymphatic filariasis  (LF), onchocerciasis, 
filariasis (LF), can utilize appropriate diagnostic tests or  
schistosomiasis, and soil-transmitted standard questionnaires screening for symptoms
helminthiasis (STH). Epidemiological studies or signs, or for behaviors associated with risk
reveal a broad geographic overlap among of infection. Population-based diagnosis can
these diseases, especially among impoverished
i mpoverished also be carried out retrospectively by analyzing
 populations with limited access to health existing epidemiological data. Based on results
services and sanitation. The focus of public of parasitologic assessment, an appropriate
health interventions against these helminth intervention is selected. Population-based
infections has transformed over the years; from diagnosis distinguishes PCT from the clinical
measures targeting extra-human
extra-human stages of the life approach in which diagnosis is performed at the
cycle of the worms, such as vector control or   individual level prior to treatment. 
nietcaitfiiocnal;lytothmr oeausguhr etsr etaatr m
ethnevihr ounmmanenhtoasl ts,as p geetnint g tr eatSmeecnotntdh,r PoC
ugThim livuelr aytioof ns b
deo p
r glee-msceanlets p
la p -inagsleed-
with the use of anthelminthics at regular administration drugs by non-medical personnel
intervals. The control of these neglected diseases (e.g., teachers, volunteers,
volunteers, or community drug
is considered a vital step towards achieving the distributors), and the use of non-medical
majority of the eight Millennium Development settings (e.g., schools, barangay halls, churches)
Goals, but despite the availability of low-cost
low- cost as fixed
fixed points
 points for drug distribution (Figure
and effective public health interventions, a 8.11). On the other hand, personalized case
large number of the world’s poorest individuals management treatment is performed by  
remain affected with these diseases. 
The main strategy, recommended by
the World Health Organization (WHO)
for controlling these infections, is the
implementation of large-scale preventive  
chemotherapy (PCT) among population groups  
at risk. PCT isinvolving
intervention the regular,
thesystematic, large-scale
administration of one
or more anthelminthics to selected population
groups, with the aim of reducing morbidity and
transmission of selected helminth infections. 
Characteristics of PCT  Figure 8.11. School teachers administering
deworming tablets to students in a public
Three key characteristics determine PCT
 elementary school in Biñan, Laguna
as a public health intervention.  (Courtesy of Dr. Vicente Belizario, Jr.)

CHAPTER 8: Special Topics in Parasitology   411 

specialized personnel
personnel on individuals reporting complete their life cycle. Consequently, direct
to health facilities.   human-to-human spread is unfeasible and
Lastly, PCT is implemented
im plemented at regular disease transmission becomes a slow process.
intervals based on the parasitologic status These facts suggest that the rate of increase in
as determined by the population-based number of worms within a human
huma n host that
surveillance. The intervention is repeated contributes to the intensity of infection is slow
without the need for further diagnostic   depending on subsequent re-infection episodes.
episodes. 
interventions, although implementation of a The risk of developing morbidity and the
monitoring system is important.   likelihood of disease transmission are dependent
dependent
on the individual’s
individual’s intensity
 intensity of infection. As  
Modalities of Implementation 
the intensity of infection increases slowly, the
There are three modalities by which PCT individual’s risk of developing morbidity also
interventions can be implemented.   increases slowly, explaining why early-stage
manifestations associated with the targeted
•  Univers al trea tmen t is the helminth infections are frequently overlooked.
administration of anthelminthics to Second, community diagnostic procedures are
the entire population of an area (e.g., available for each of the four diseases. Third,
Third,
state, region, province, district, sub- drug delivery strategies relying on resource
district, village) at regular intervals,  persons based in schools or within
within communities
irrespective of the individual infection
status. have been developed; and lastly, recommended
anthelminthics are low cost or given by 
•   Targe ted trea tme nt is the
administration of anthelminthics at t heasr emf acetuor 
 p i  bb puatne ietos acsondtoaninaticonsst.s aAnlld
tsicacloncotr m
regular intervals to specific high-risk make the PCT interventions feasible for
groups in the population, defined
defined  by
by implementationn against the four target diseases.  
implementatio
age, sex, or other social characteristics In addition, all anthelminthics currently
(e.g., school-age children, farmers), used in PCT interventions [albendazole (ALB),
irrespective of the individual infection diethylcarbamazine
diethylcarbamaz ine (DEC), ivermectin (IVM),
status. mebendazole (MBD), and praziquantel (PZQ)]
•  Sele ctive trea tment is the are safe (i.e., adverse events are rare, mild, and
administration of anthelminthics to transient), and therefore appropriate for use
all infected individuals (confirmed or in interventions targeting infected, as well as
suspected) who are identified
identified after
 after a non-infected individuals. Temporary minor
regular parasitologic screening of a reactions following treatment occur mainly  
 population
 populat ion group living
livin g in an endemic as a result of the body’s
the body’s response
 response to the dying
area. worms. Thus, heavily infected individuals are  
Currently Targeted Diseases  expected to experience the most reactions. In
general, the number of individuals reporting
PCT targets
tar gets four
f our NTDs
NT Ds (L,Fonchocerci
(L,Fonchocerciasis,
asis, for adverse reactions is highest during the first
schistosomiasis, and STH) because of a number round of treatment and tends to decrease during 
of reasons. First, helminths responsible for the succeeding rounds.  
four diseases are unable to replicate in humans Such effective anthelminthics are also simple
and require one or more obligate passages
passag es to administer allowing the drug distribution by
outside the host (e.g., in an intermediate host, non-medical personnel possible. In the War on
 in a vector, or in the environment) in order to  Worms — Western
Western Visayas approach,
approach, a local 

412   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

government unit (LGU) led, school-based, in the prevalence and intensities of infection
school teacher-assisted mass drug administration
administration among the school children after two years
y ears of
(MDA) has resulted in significant
significant reductions
 reductions  implementation (Figure 8.12).

Figure 8.12. Cumulative STH prevalence and heavy intensity infections in school-age children in Aklan,  
 Antique, and Capiz, 2007-2009
(Courtesy of Dr. Vicente Belizario, Jr.) 

The following general precautionary for individuals who may experience

measures are recommended to ensure the safe adverse reactions during rounds of
implementation of large-scale drug delivery:   treatment; 
•   Any serious adverse reactions should
  Seriously ill individuals, who are
•

 be carefully
carefull y recorded
record ed and relayed to
unable to engage in normal activities of
daily living without assistance, should the appropriate authorities;
  Individuals who have previously
 be excluded from large-scale treatment;  •

suffered rare serious adverse reactions  

  Program managers must ensure
•

caused by the drugs should be excluded

that targeted individuals for drug from treatment; 
administration are adequately
•  Scored tablet
tablet s should be broken
informed about the possible adverse into smaller pieces or crushed before
reactions and necessary intervention
i nterventionss administration to young children to
 in the event of such reactions;
 prevent choking or asphyxiation;
asphyxi ation; and 
•  Program managers must ensure the •   Program managers should be aware of
availability of medical care and support   other MDA for other diseases in the

CHAPTER 8: Special Topics in Parasitology   413 

same area. This is to minimize the

th e risk In the Philippines, three helminth
of targeted individuals suffering from infections are targeted for control or elimination
adverse reactions due to interac
interactions
tions  by the Department of Health through national
 between drugs distributed
distributed by different  programs that utilize MDA as a major strategy
 programs.  (Table 8.6). 

Table 8.6. Target population, drug recommended, and mass drug administration frequency of health
programs in the Philippines 

MBD/ALB

Filaria sis Elimin ation Program DECplus

DECplusALB
ALB

Drug Combinations 
edarr c uhg m tauintionng sitystoew
diastinrr i  b MlaDnA
mn,  p ,  p
nincgam f uanigdnin, g,
A number of studies have investigated the monitoring, and evaluation. Because of the
safety of drug combinations in the treatment of similarities of program strategies, epidemiologic
helminth infections.  overlap of targeted diseases among affected
•   ALB and PZQ can be safely co-  populations, and the availability of drugs,
administered for STH and these NTD control/elimination programs are
schistosomiasis. suited for an integrated implementation in a
•  MBD and PZQ have been widely way where coordinated MDA interventions for
co-administered in many countries multiple
multip le diseases are implemented
implemented to reduce the
and reported to be safe for STH and duplication of efforts in treating the diseases
schistosomiasis. separately. Such integration and coordination
•   ALB plus DEC is also a safe
safe of program activities among different disease-
combination in the treatment of specific programs should lead to better drug
delivery, increased health benefits, and better  
lymphatic filariasis
filariasis and
 and STH.
The WHO has endorsed the co- use of limited
l imited resources reaching more affected
and at-risk individuals. 
implementation of MDA, also referred to as
the integrated approach
appro ach to PCT. Ancillary Benefits and Advantages 

Promise of Integrated PCT  Sustained, large-scale PCT againsthelminth

infections results in a number of benefits
of benefits and
 and
Reports have revealed that many Ministries/ advantages: 
 Departments of Health in disease-endemic
countries have supported the control of NTDs •   Relief from other NTDs (e.g.,
through independent and parallel programs, with   foodborne trematode infections) and

414   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

from ectoparasitic infections (e.g., relevant government units, and donors to

scabies and lice) with commensurate maintain their interest in and support for the
health benefits;   program.
•   Significant increase in weight and Monitoring and evaluation should be
height among children leading to carried out with as little expense as possible so as
improvement of nutritional status and not divert resources away from implementation
implementation
general health; activities. The WHO recommends that
•   Increase in school participation and approximately 5 to 10% of the program
pr ogram budget
improvement of school performance  be allocated for monitoring aactivities.
ctivities.  
in children; and Monitoring and evaluation are based on the
•   Reduced maternal anemia in pregnant  periodic collection and analysis of variables or
women and improved infant birth indicators with the aim of measuring changes
weight and survival. occurring during program implementation. The
suggested indicators for schistosomiasis and
Monitoring and Evaluation 
STH control programs in school-age children
Monitoring and evaluation are integral can be grouped into three categories (Figure
components of any control program and are 8.13). Process and performance indicators
in dicators are
vital to ensure both effective implementation used for monitoring, and performance and
and maximum benefit for infected individuals, impact indicators for evaluation (Table 8.7). 
their families, and communities. An appropriate Drug coverage is the minimum indicator
evaluation system allows
allows proper documentation
documentation  for assessing the performance of large-scale PCT 
of r atchtiece psr , oagnr dam
 p gusidiem
’ , e p
f uatcutr 
s  p u pr doagtr easmcduir r r eecnttion. ionf tienr dveivnitdiounals.  iCn othv er tagr eger te pf eor  pu pnr o p
s tolathioe  p r gorotiuo pn
It is important that the outcome of monitoring who have actually swallowed s wallowed the recommended
and evaluation activities (i.e., good practices drug/s. 
and challenges) be shared
s hared with communities, 
 Figure 8.13. Process, performance, and impact indicators for helminth control  
(From World Health Organization. Helminth control in school-age children: a guide for managers of
control programmes. 2nd ed. Geneva: World Health Organization; 2011.)  

CHAPTER 8: Special Topics in Parasitology   415 

Table 8.7. Categories, usage, and frequency of  policy formulation

for mulation for NTD control
c ontrol
collection of indicators   and elimination.
•  Difficulties encountered during
rounds of MDA can be revealed such
Process
as the identification
identification of
 of areas where
fewer individuals receive drugs than
intended.
•  Providers of drugs and funds to
support drug delivery, including the
governments of disease-endemic
countries, can be assured that the
 provided support is cost-effective. 
•    Work
 Workers
ers and volunteers involved in
drug delivery can be informed about
their efforts, which can contribute to
maintaining staff
s taff m
morale.
orale.
Source: World Health Organization. Helminth control in school-age •    Advocacy for more support for NTD
children: a guide for managers of control programmes. 2nd
ed. Geneva: World Health Organization; 2011.
control is strengthened by knowledge
that many people in need are getting
Every effort should be made to ensure
ensuredirect treatment.
observation of MDA (i.e., administration of the   •  Forecastingfor drug supplies for future

a p pr o pr iate dose in the  pr esence of  the dr u

 pr ovider ) (Figur e  8.14).  If  actual  swallowing
treatment rounds is supported.
Role of Social Mobilization  
of tablets by targeted individuals cannot be
observed directly, random cluster surveys can These neglected diseases, especially
 be undertaken
undertake n to estimate
estimat e the actual coverage.   helminth diseases, do not rapidly cause death
Monitoring drug coverage has several and are more insidious in nature than many
important outcomes.  diseases of acute onset. Health care providers
therefore consider NTDs a low priority.  
•  Reliable drug coverage rates contribute The objective of PCT interventions is to
to accurate information necessary for   ensure that all eligible individuals in affected
communities swallow the recommended
drugs. This behavioral change is dependent
on the acceptance of targeted individuals for
treatment, as wellason the health care provid
 providers’
ers’
capacity to adequately inform and motivate the
community.
 process Social
olvesmobilization
that involves
inv is a complex
program implementation,
implementatio n,
health care delivery services, health care
 providers, and strategies for mobilization  
and communication interacting to influence
 behavior al change in people. Experien
 behavioral Experiences
ces with
Figure 8.14. Checking for tongue discoloration
after administration of deworming tablets to
existing health care programs have shown that
 school children tto
o ensure compliance this aspect of social mobilization is not given
(Courtesy of Dr. Vicente Belizario, Jr.) adequate priority during the planning of PCT  

416   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

interventions.
interventions. As characteristics of communities
communities References 
and responses to various communications
from the health care providers differ, proper Amarillo ML, B elizario VY Jr, Sadian
Sadiang-
g-
abay JT, Sison SA, Dayag AM. Factors
understanding is essential in planning effective
social mobilization campaigns. Investment 
associated with acceptance of mass drug
administration for the elimination of
in social mobilization strategies is critical in
lymphatic filariasis in Agusan del Sur, 
sustaining high drug coverage throughout  
the duration of health programs (Figures Br adPyhM iA, iHneoso. pPear r aPsJi,t V
il pp Oetctetoser sn. 2E0A0.8P;1r o( j1e)c:1te4d.
8.15 – 8.16).
8.16).
 benefits from
fr om integr
integrating
ating NTD
N TD programmes
progra mmes
in Sub-Saharan Africa. Trends Parasitol.
2006;22:285 – 291.
291.
Department of Health. Intergrated helminth
control program: mass treatment guide.
Manila (Philippines): Department of
Health; 2006. p. 6 – 221.
1. 
Gabrielli AF,
AF, Montresor A, Chitsulo L, Engels
D, Savioli L. Preventive chemotherapy
in human helminthiasis: theoretical and  
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Hyg. 2012;105:683 R Soc Trop Med
 – 93.
93.
Figure 8.15. Former DOH S ecretary Francisco
Hotez PJ, Molyneux DH, Fenwick A,  
dinf o
DuPqeur ezIIIaadnm e r e
isr tm inr g ntniq
 Aa Gio
thuelm ntvheicr nsoto clhvo
r  Ssa aoclion Kumaresan J, Sachs SE, Sachs JD, et al.
children in Pandan Central Elementary School, Control of neglected tropical diseases. N
 Antique during the launch of the War on Worms—
Worms—
Western Visayas (From War on worms goes to
Engl J Med. 2007;357:1018 – 27.
27.
Western Visayas. Philippine Star. 2007 Nov Liese B, Rosenberg M, Schratz A. Programmes,
27;Health & Family:E-2.)  partnerships, and governance for
elimination and control of neglected
tropical diseases. Lancet. 2010;375:6
2010;375:677 – 776.
6. 
Linehan M, Hanson C, Weaver A, Baker M,
Kabore A, Zoerhoff KL, et al. Integrated
implementation of programs targeting
neglected tropical diseases through
 preventive chemotherapy: proving the
feasibility
feasibili ty at national scale.
sc ale. Am J Trop
TropMed
Hyg. 2011;84(1):5 – 14.
14.

Loukinasf f eAc,tiH ar kinetr rh 
onost.ezInP:J.BCr uhnetmonotLhe,r r aL  ppayzo f Jh, ePlm
Figure 8.16. Parade of school children and
K, editors. Goodman and Gilman’s the
teachers during the launch of War on Worms— 
Biñan, Laguna   pharmacological
 pharmacological basis of therapeutics.
therapeutics. 11th
(Courtesy of Dr. Vicente Belizario, Jr.) ed. New York: McGraw-Hill; 2006.  
 

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Spiegel JM, Dharamsi S, Wasan KM, Yassi Geneva: World Health Organization;
A, Singer B, Hotez PJ, et al. Which 2010. p. 1 – 7.
7.
new approaches to tackling neglected World Health Organization. Working to
tropical diseases show promise. PLoS Med. overcome the global impact of neglected
2010;7(5):1 – 5.
5 .  tropical diseases: first WHO report on
War on worms goes to Western Visayas. neglected tropical diseases. Geneva: World
Philippine Star. 2007 Nov 27;Health & Health Organization; 2010. p. 1 – 5
5..
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World Health Organization. Report on active   of preventive chemotherapy interventions
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9.
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6.
 

418   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Emporiatrics for the Filipino Traveler

Edsel Maurice T. Salvaña, Arthur Dessi E. Roman

he past years have shown an exponential (48%) by road (39%), rail (3%), or over water  
increase in the amount of local and   (6%).
international travel. The United Nations’ This large increase in travel activity, coupled
T 
World Tourism
Tourism Organization
O rganization reported that
international tourists numbered around 922
with the threat of various geographically-
associated emerging diseases including influenza
million in 2008. This number is expected to   A (H1N1), avian flu (H5N1), and the severe  
exceed one billion in 2010 and 1.6 billion acute respiratory syndrome (SARS), makes
 by 2020. Not only
onl y are more people
pe ople traveling, emporiatrics or travel medicine increasingly
 previous ly inaccessible
 previously inaccessi ble areas are now
no w being   relevant. The various risks that travel poses
po ses
explored due to increased technology and urban to health can be challenging to prevent and
sprawl. Locally, the Department of Tourism identify. In general, these can be divided into
reported that tourist volume grew by 6.64% environmental hazards, physical hazards, and
in the Philippines’
Philippines’  top destinations during the medical hazards. There may be substantial
first  quarter of 2010, with foreign tourist arrivals overlap between these categories.  
increasing by 7.89%, while domestic
do mestic tourism Environmental hazards are those due to
increased by 6.09%. Metro Manila remains the  weather, terrain, altitude or depth, and wildlife 
lSeuar dif nogllodwes.tination, while Ce bu and Camar ines  binecaluddir nesgsefldo br ay caanr def uf al p e ihthazaatr tdens tcioan
unlaan. nTinhgesw
Several factors have contributed to the   to adequate clothing, equipment, and logistics.
rise in domestic and foreign travel. Among Physical hazards include conditions which may
these are socio-cultural factors such as the cause physical harm to the t he traveler. Potentially
recognition that travel is a highly desirable dangerous activities such as rock-climbing,
activity which expands one’s knowledge  and hang-gliding, and diving, as well as prevailing
outlook in life, more favorable economics of  political and safety issues including war and
travel including lower transport and travel loose firearms, crime, drugs, safety practices,
costs, higher disposable incomes, built-in and access to appropriate medical care are
leave as part of employment benefits
ben efits and considered physical hazards. Some physical
 perks, simplification  of logistics in terms of
simplification of hazards are more difficult to address since
availability of online facilities for arranging some travelers deliberately place themselves in
travel, ecotourism, medical tourism, and all- harm’s way. Medical hazards include the risk of
inclusive packages.  contracting infectious diseases such as typhoid,  
In 2008, more than half of all international malaria, and dengue, as well as issues of food
arrivals were motivated by leisure, recreation,  poisoni ng, unclean
 poisoning, unclea n water, poor
poo r hygiene,
hygi ene, risk
and holiday travel, while business accounted of pulmonary embolism, and exacerbation
for another 15%, and 27% was due to other of existing medical conditions. Taking into
 purposes such
s uch as visiting
visi ting friends
fr iends and family,
f amily, consideration all of these potential hazards in
religious travel, and medical tourism among the chosen destination, plus one’s own health
others. More than half (52%) arrived via air status, emporiatric medicine aims to maintain
 transport, while the rest used surface transport  the health and well-being of the traveler and  
minimize the risk of acquiring disease.  

CHAPTER 8: Special Topics in Parasitology   419 

The Pre-Travel Medical Consultation  new vaccines. Allergies to food and drugs are
elicited, as well as any reactions to previous
In order to minimize the possibility of vaccinations. Some vaccines may cause allergic
travel related illness, the traveler must gather reactions in those who are hypersensitive to
as much information about the travel  poultry products
products because these
these may beprod
beproduced
uced
destination(s)) and possible activities that
destination(s in chicken or duck eggs. Influenza vaccines in
he will engage in. A traveler should ideally  particular may give a reaction in those allergic
allergi c 
cinontr sauvltelammeeddiiccianle par tacletiatsitonf oeur   r wwitehekexs p
 per r iioer ntcoe to poultry. A list of current medications is also
departure. A longer preparation period may be useful to determine whether drug interactions
may occur with those that may be prescribed for  
needed if long-term travel or overseas work is  prophylaxis
 prophyl axis or treatment.
t reatment. An adequate supply
expected, while consults as late as the day before of medication should be brought with the
travel may still be of benefit.
of benefit. 
traveler since obtaining medication abroad may
Itinerary   be difficult,
difficul t, along with the rrisk
isk of counterfeit
cou nterfeit
medication.  
A detailed itinerar y should be made
Physiologic states such as pregnancy,
available to the travel medicine provider prior or breastfeeding status may present special  
to the consultation so that the practitioner
 problemss during travel. For
 problem Fo r instance, access
can adequately determine possible medical, to birthing facilities abroad may need to  
environmental, and physical
traveler. This includes dates ofrisks to theand
departure  be determined when traveling during late
 pregnancy.. Certain airlines place
 pregnancy pl ace restrictions
restrict ions  
return, countries and cities which will be visited
including accommodations, and whether the eer deignganmt owthoem
otenr mtr .aBver leaostf f  p n  awyhoavaer etonsetao p
r sem r 
traveler will stay within urban limits or sojourn  breastfeedingg if certain prophylactic medicines
 breastfeedin
into rural and sylvan areas. Transit
Transit cities should are used, such as doxycycline doxycycline and ciprofloxacin. 
also be included, as some countries have specific
vaccination requirements for visas going to and Interventions 
from srcin countries and entry may be denied
Patient education on avoiding food- and
on this basis.  
water-borne diseases, as well as use of insect
An excellent reference that is used for risk repellents such as N,N-diethyl-meta-toluamide
assessment is the Centers for Disease Control (DEET)-containing preparations to avoid
and Prevention (CDC) Yellow Book, which has arthropod and other vector-borne diseases should
detailed descriptions of destinations and risks  be done. Instructions for self-medication for
therein. Commercial travel medicine websites travel-related diarrhea (including antimicrobial
such as 
as www.travax.com can
can be used to generate use and oral rehydration solutions), as well
w ell as
useful information, including patient handouts   avoidance of contaminated water and ice should
to help guide the traveler during his or her trip.  
Clinic Visit 
 be emphasi zed. Use
emphasized.
clothing should be
of sunblock
su nblock and
an d protective
protect ive
b e mentioned, especially 
since some prophylactic medications such as
Basic demographic
demographic data along with specific
doxycycline
doxycycline can cause photosensitivity.
photosensitivity. Special
health data is needed by the travel physician to instructions regarding avoidance of specific
make a complete
complet e risk assessment
assessment for the traveler. illnesses (e.g., avoid wading in fresh water in
Aside from age, sex, and past medical history, schistosomiasis- and leptospirosis-endemic
a good vaccination history is also imperative in
 areas) should be given on a case-by-case basis.
order to determine the need for boosters and  
Risks of sexually transmitted diseases (STDs), 

420   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

including HIV and AIDS, should be assessed Table 8.8. Vaccines for travelers

and appropriate
arrangements measures
should be madetaken. Finally,
regarding access
to medical treatment in emergent situations.   tetanus
The need for any vaccinations and Hepatitis B
 prophylaxis
 prophyl axis will depend on multiple
multipl e factors.
Most travel medicine authorities will make 
Seasonal influenza*
recommendations on the use of these
interventions depending on risk of exposure,
clinical impact, potential adverse reaction to  
the medication, and quarantine and infection
risk to others. The only consistently required Varicella
vaccine for travel purposes is yellow fever (for
travel to endemic areas), while all others are
recommended in varying degrees and depend
on the type of exposures anticipated.  
Vaccine-Preventable Diseases 

Local recommendations for the

immunization of adult Filipinos have been
developed by the Philippine Society for  
M ir o p
Phiicl p  binoleoFgoyuannddatIinof necf toir oV
usacDciinseaatsioesnw
init2h0t0h9e general travelers
and are available online at at www.pcp.org.ph. **Included in the routine immunization program in sev eral
countries
Indications for age, exposure, risk, and specific (Adapted from WHO International Travel and Health 2010)

 populat ion are included,

 population include d, and travelers areurged
to keep their immunizations up to date, whether either as an individual or a combined vaccine in
or not international travel is planned. During three weeks time, rather than the more lengthy
 pre-travel medical consultation, physicians standard 6-month
6- month dosing
dosi ng schedule.
schedule. It should be
have an excellent opportunity to review the noted though that while it is certainly better to
immunization status of the traveler. Routine have vaccination than not to have vaccination,
vaccinations are listed in Table 8.8 and are accelerated
accelerated schedules may offer only partial
available in the country, while Tab
Table
le 8.9 shows  protection. 
vaccine-preventable
vaccine-preve ntable diseases for selective use Travelers’ Diarrhea 
 by travelers. In cases where there is uncertainty
uncertaint y
about vaccination status, serologic testing for The most predictable and invariably the
antibody where available may be warranted most common
(TD),travel-related illness
70%is
travelers’
depending on perceived risk of exposure.  diarrhea affecting 30 to (up to 80%
Accelerated
Accelerated schedules are available for for high-risk destinations) of travelers depending
the travelers without adequate time prior   on the destination and length of stay.
s tay. Persons
to travel for routinely recommended travel most affected are those traveling from an area
immunizations. The U.S. Food and Drug of more highly developed standards of hygiene
Administration (FDA) has approved an and sanitation
sanit ation to
t o a less developed one. However,
However, 
 accelerated dosing schedule that can afford TD can still occur when traveling from a
 protectionn against hepatitis
 protectio h epatitis A and hepatitis
hepat itis B,   less developed to a more developed country  

CHAPTER 8: Special Topics in Parasitology   421 

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e e
422   H MEDICAL PARASITOLOGY IN THE H 
PHILIPPINES
   
  

Dilea,e
Dilea,e//  N
 N  
 N  
 N
Etitio
o lo c;c Tr an
an smi
smiss
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atur e or
or dilea,e  Occ
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ence  Rilk ra tr avel
avelers
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eventive
ve m ea,u
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r es 
es 
ac;ient
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Typh
pho oid on
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Acut
ute
e ill
illn
nessw
esswith
ith f cf igue
gue,,  •  South
South, East and Sout
South
heas
eastt  •  R.isk is g r eatest
eatest f or tr 
tr avel
ave lerst
rs t o    O r al live-ot
• ive-otttenud ed vacc ine 
pa r olyphoi
olypho id tr onslTissi
onslTiss ion on   headac he, r elot
otii'-8
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 Asio, A
 Af 
f rica
rica,, the Cari
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South  Asiia (6-30 lilim
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rom
o
  m Ty2y211a •str ain"
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Typhi,  
f ever
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and   and C entr 
entr al and Sout
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caused by contact
co ntact,, f eve<I
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t)'PIW,S.
t)'PIW, S.   sex with
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 parafyphi A, A,   hos been tr unk
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•

r ec
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ts   srn: 
docume nte d  0 
B, o r C 

C hci era 
era  rall r oute 
Feca l-ora •  An acute enta ic d isise
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r-
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ons characterized
c haracterized   viral encepha ll s in As
viral  Asiia  season, destination, duration 
duration  •  Vacc ine ava ilab
ilablle t:,ut
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(JE)  of the ge nus by f ebr ile
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 Asiaia   of tr avel
avel and ad MlMliies  ma r keted
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the   "'(J
"'(J  
caused by Cu/ex;  
Cu/ex; aseptic menln enlng
glts or   •  Inddence dec
decli
linin
ning in •   Rsk • hi
 high
gher
er In long ser m  endem ic cou ntries
ntries   ;i;; 
Japanese Nd ural
ural reserv
reservooirs
irs::   encephdltls to severe
severe(rapi
(rapid
d  Japan and Korereaa due to   tr avelem
avelem a n d expd r  ri al
ales
es  C:  
C:
encepha llts pigs and onset and progression wit
ith
h  Imm unizat
unizatiion
on   •   Risk
Riskf 
f o r trave
ravellersw
rs w ith
ithextensive
extensive   "'(J
"'(J  
"'(J 
"'(J 
vir us-a
vir us-a va rious v,1Id h eadac h e, h ig h f ev
ev er and •  lna eoslng
eoslng lndd ence In   outd
utdoor
oor expa;ure (camp ing, g,  
f lavM1us
avM1us   bir ds 
ds  men ln
lngea
gea lsl(TS
l(TS,, permcinent some re
reggior6 of Ch
Chiina, hiking, bicyc le toum
toum,, outd
outdoo
oor r  
rn 
neurologica
neurologica lsequelae)
sequelae)   Bangladesh, Ind
Bangl ndiia, Nepal
Nepal, occ upat
upatiional ad rvit
rvitiies,
es,   (/)  
(/)
•   App
 Appr r oxlmol
oxlmoleely 25% of
of seve
sever 
r e  Pakstan,, Northern Tha
Pakstan Thalllano. In po rtlcul
rtlcula , In a ,eas
eas  
d lnlcal
lnlcal coses have a fola l  and VltS!
tS!n
nam, du e l o f lood in
ingg  w h ere f lood ing lrr 
lrr lgotlon
lgotlon Is
outcom e  and ,elated e, ents
ents   pr actic
actic e d)
d)  
 

424   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

as a consequence of non-immunity to non- on the use of self-administered antibiotics.

native enteric pathogens. Associated signs and Prophylaxis using non-pharmacologic agents
symptoms include nausea, vomiting, abdominal has been suggested, including the use of
cramps, and fever. Bacterial pathogens account  bismuth sulfate and probiotics,
probio tics, but the evidence
 for 80 to 90% of cases.  for these interventions is still controversial.  
The most common pathogen causing TD Prophylactic antibiotics are generally not
is enterotoxigenic  Escherichia coli (ETEC). recommended due to the possible emergence of  
Enteroadherent (EAEC) and other  E. coli  resistance and potential side effects. However,
subtypes are also common pathogens in bacterial  short-term travelers who are high-risk hosts
diarrhea.Campylobacter jejuni, Shigellaspp., and
jejuni (e.g., immunosuppressed) or those taking  

 but presentspp.
Salmonella arebloody
likewise usual pathogens critical trips during which
with diarrhea. Viruses, affect the purpose may bediarrheal bouts could
given prophylaxis.
including norovirus, rotavirus, and astrovirus, Attack rates
rat es of TD can be decreased from
fro m 40%
have been isolated in 5 to 8% of TD. Protozoal down to 4% with prophylactic antibiotics but
 pathogens, whose symptoms are slower to continuing changes in the patterns of resistance
manifest and may be the cause of persistent of the various choices of antibiotics should be
diarrhea, collectively
collectively account for about 10% of considered. Fluoroquinolones have replaced
diagnoses in longer-term
longer-t erm travelers.
travelers.Giardiais the cotrimoxazole and doxycycline as effective
major protozoan pathogen found in travelers.  prophylactic
 prophyl actic agents.
agent s. However,
However , Campylobacter
 Entamoeba
 Entam oeba hhistolytica is relatively uncommon
istolytica resistance to fluoroquinolone in Southeast
 but can cause severe disease. Asian countries has prompted some authorities  
ooidarr 
as  “f D  phoeiasof nr oinmg,t”oixninvos,lvceoslltohqeuinalglyesktinoonwonf tdoiaurr  a.acr olides instead, es  ppecially f or   b
seh em  bloody
 preformed toxins in food, and present within Most diarrheal diseases are self-limited  
3 to 6 hours as vomiting and/or diarrhea that and patients will recover in a few days. If
usually resolves spontaneously within 12 hours. warranted, as in bacterial TD, empiric treatment
Examples of the toxin mediated diarrhea include with an antibiotic directed at suspected

those caused
aureus.Some by Bacillus
more exoticcereus
and and Staphylococcus
potentially deadly  bacterial pathogens are
include single-dose of
of benefit.
 benefit. Examples
or 1-day  Examples
therapy with a
toxins in food include neurotoxins from algal fluoroquinolone, or azithromycin 500 mg/
 blooms (paralytic shellfish poisoning or red day for 1 to 2 days. More than antibiotics,
tide), ciguatera, and scombroid.  however, it is very important for patients with
The importance of prevention can never diarrhea to replace volume losses. Fluid intake
 be over-emphasized
over-emphas ized especially
especiall y with regard to should be maintained with safe liquids. Special
TD. For travelers to high-risk areas, education attention should be given to the use of ice in
on food and beverage food choices is key   beverages, as ice may be made from unsafe 
to decreasing the risk of ingesting potential water. If moderate to heavy diarrheal losses
 pathogens. These include avoiding
avoiding undercooked
undercooked continue, oral rehydration salt (ORS) solution
and raw food, meticulous hand hygiene, should be considered especially for children
exclusive use of bottled, boiled or filtered   and the elderly.  
water (including water for tooth brushing),
Malaria 
and eating only at hygienic and sanitary food
establishments. Since a subset of travelers make Malaria has been fully discussed in a
it a point to eat indigenous cuisine from street
 previou s chapter, but because it is preventable
 previous
vendors, these travelers should be educated  in travelers, prophylaxis will be briefly discussed 

CHAPTER 8: Special Topics in Parasitology   425 

in this section. Malaria is found in over  plains.  Plasm

 Plasmodium
odium falcip arum accounts for 70
falciparum
100 countries, and greater than 125 million to 80% of cases, while
while P. vivax
vivax accounts for 20 to
international travelers are at risk every year. It 30%. P falciparum resistant to chloroquine and
 P.. falciparum
remains the most common cause of fever in sulfadoxine-pyrimethamine has been reported,
 returning travelers. Many travelers continue to and so chloroquine should not be taken to
acquire malaria, and more than 10,000 reported prevent malaria when traveling to endemic
cases likely represent only the tip of the iceberg.  areas (Table 8.10). 
Malaria, especially falciparum malaria can be a Anophelene mosquitoes that transmit
life-threatening disease, but is quite amenable malaria are known to be night biters. Preventing
to treatment when recognized early. In the   mosquito bites can be done through: wearing  
Philippines,
year in areasmalaria
below risk
600exists throughout
m, except
exce pt in thethe22 long-sleeve
long-sleeved
night; use ofdinsect
clothing and trousers,
repellents especially
including DEET- at
 provinces declared as malaria-free:
malaria-free: Aka
kaln
ln,, Albay
Albay,, containing and citronella-based preparations
Benguet, Bilaran, Bohol, Camiguin, Capiz, with periodic reapplication; and mosquito nets
Catanduanes, Cavite, Cebu, Guimaras, Iloilo, which should ideally be treated with insecticide.
 Northern Leyte, Southern Leyte, Marinduque,
Marindu que, Garlic, vitamin B, and ultrasound devices do
Masbate, Eastern Samar, Northern Samar, not prevent bites. Travelers should be wary
Western Samar, Siquijor, Sorsogon, Surigao of the symptoms of malaria especially fever
Del Norte, and Metropolitan Manila. No risk occurring 1 week after the possible exposure
is considered to exist in urban areas or
o r in the  and up to 2 years after the return. 

Table 8.10. Recommended drugs used in the prophylaxis for malaria

Contraindications:

Should be taken with food

Not available in the

Philippines

426   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

Specific Infectious Diseases involving Tuberculosis is highly prevalent in the

Potential Health Risks for Travelers  Philippines, so no prophylaxis is needed for
Specific infectious diseases that pose health
residents since everyone is considered exposed.
Visitors from developed countries, who are not
 risks to travelers have been listed and described
in International Travel and Health 2010
tuberculin test (PPD) positive, should have their
status checked shortly after returning home
 published
 publish ed by the World Health
Heal th Organization
Organizati on  
to their native country. Influenza
Influenza A
 A (H1N1)  
(eW . Ir nevcalulesniocne  in tthise lcisotuisn btr ayseodf  otnr aavehligtho
ugOh) p
noH is present, and has been reported in most of
 pose a significant risk to visitors (e.g., malaria, the urban destinations, and so vaccination, if
dengue), potentially fatal or severe morbidity available, should
should be done. Hand and general 
resulting from exposure even if the agent is  personal hygiene, as well as cough etiquette
not very common (e.g., Ebola, rabies), and are recommended. All four dengue serotypes
the potential for public health threat such as are present, and the country is considered
epidemics(e.g.avian influenza, HIV, influenza hyperendemic for dengue, with transmission
A/H1N1). The possib ility of exposure is occurring throughout
throughout the year. According to the
dependent on the presence of the infectious Department of Health National Epidemiology
agents in the country of travel, while the risk of Center, an increase in the number of HIV cases
infection will depend on the itinerary, purpose has been reported in Metro Manila, Cebu, and
of travel, and the traveler’s
traveler’s behavior
 behavior (Table Davao. Safe sexual practices and avoidance of
8.11).  risky behavior, especially in these areas, are
advised. In Boracay Island in Aklan province, 
aer aseiteins atnhde coalsief sor omf  sS,TskDins
diaser ar hsesa, canudseadn biyn pcr 
Travel within the Philippines 
Domestic destinations pose specific
infectious and parasitic disease risks to the local have been reported. Malaria, food- and water-
traveler. Similar to international travel, food-
food-  borne and skin diseases are the major concerns
in traveling to Palawan. In Cagayan Valley,
and water-borne diseases still account for most
travel-relatedd illnesses locally, and so the same
travel-relate  precautions for
for animal-borne
animal-borne diseases should be
 precautions
 precautio ns for these diseases should be taken.   undertaken, most
In addition, an significantly,
outbreak for leptospirosis.
of anthrax was recently
The Filipino traveler has likely been
exposed to similar enteric pathogens in his place reported. Infectious risks with travel to Davao
include STDs, parasitism such as intestinal
of srcin so certain vaccinations such as that for
hepatitis A may not be warranted. In those with heterophyidiasis, leptospirosis, influenza, and
dengue. 
co-morbid conditions such as HIV and hepatitis
B, serologic testing for hepatitis A antibody may The Returned Traveler  
 be warranted, and vaccination
vaccinatio n offered, if there  
Factors that influence
influence the
 the risk of illness
issunr f fo aciemamnutingietny. (SHer Bo pSAr egv)alaem
ncoenogf   H
Fielipaitniotis  B
H is during travel is similar to the pre-travel
high (>8%), and so vaccination is recommended risks modified by the traveler’s adherence to
for everyone, travelers and non-travelers alike.  prescribed chemoproph
chemoprophylaxis
ylaxis and vaccination
vaccination
Typhoid fever is endemic in the country, regimens (e.g., malaria prophylaxis), as well
occurring in all places all year round, causing as activities during travel, and actual exposure
a morbidity rate of 30.5/100,000 population, to infectious agents during travel. Illnesses
and a mortality rate of 1.7/100,000 population. may begin during the travel period or may
Therefore, typhoid vaccination is advised. 
take weeks, months, or even years after return,
to manifest, depending on the pathogen’s
the pathogen’s 

Tab le 8 .11. Sped ic infec

nfec1i
1ious
ous diseases
seasesiinvolv
nvolviing po
pott en1ia l hea l1h risk
risks
s f or tr ave
vellers
ers  
CHAPTER 8: Special Topics in Parasitology  427 
Geog
Geogr  r aphi
aphic 
Disease
sease   Ca use
se   Transmss
Transmssiion  Natur e or
or disease
sease   Risk
Riskttor tr avel
aveleis
eis   Pr eventia,
eventia,  
distr ibu ti
tiai
ai  
Ameb
Amebicg
icgis
is    / dscussed 
Prew:,.u y 

 Av ia, influ

 Avi influenza
enza  Hig,ly
Hig,lypathogen
pathogeniic  •  Contact with
Cont witha.,
a.,iian •  Influenza-
Influenza-lilike
ke illn
illness,
ess, O,tyspOJOOc humrn  •  Conlo::
o::II wrrh
rrh      Avoid consum i::li
• ::liond
ond  
a.ii
a.iia n influ
influenza
enza  feed mder ial  da1hea.and dh er inf ec
ec ti ons hOJe erwir 
erw onm enfo s uc h a.
ir onm und
un d ercooked eg;;p,
eg;;p,  
 A (H5NI)
(H5NI) vir u;
u; a  •  Bird-to-hu ma man n,  GI comp lcinl:.   occu rr eded t o dd
dd e It.le a, ima l maket:. outtry Of   pou
p outt pou tt,
tt,y y 
dher non-huma,   pccsib
pccs ib ty
tyenvilonment-
envilonment- •  Pneumoni
Pneumonia a with
with Between N01embe! and pou tt,tt,y
yf arm
rms,s, prodJch;:  
infl uenza subtypes  
influenza to-
o-huma'I
huma'I a, d, d, very
very r od
od og 1q:::,h
q:::,hiic infiltr at e. 
e.  2000 aid July 2008 2008,, arry free-ra, Qng a   Hand hyQene 
•

(eg.,H7, H9) H9)   r a ely,

ely, li
lim
m it
ited.
ed. n o n- d va ying pattens   neaty 400humm  Caged poultry, Cl    A
•  Avvoidco ntcd with
con ith  
sustainedhum
ustainedhumai ai -t
-to-
o- •  Hem
Hemq:fyst.
q:fyst. fr equen
equentt  Ce&e$d HSNl we,e surf 
su ac es thd mic;ilt
rf ac anim
nimds
ds and dead
dead   n 
huma,tr 
huma, tr crismi'
crismi'i.iosn   •  tv'IJlti- Of g:::ri f ailur e,  r eported
eported l o WH WHO be con
conttan in
incied
cied  migrator v bi,
i,ct
ct  I 
•  l o e.r iClence that
that   sepsis ike sysynd
nd orne.   fr om
om 15 countries
countriesinin by poult
poultry
rydd opp in
ing,
g,   Tr eatment
• eatment aid t- 
t-  )> 
-0 
p,ope,ly cooked
cooked   •  F
d  d fy  rd e  anong  Af rica,
rica,S
South-Ea:t
outh-Ea:taid
aid inc
inc1ea. e 1616k
k  ecpa.ur 
ecpa. ur e prophy
prophy((il)(6
l)(6::  -I 
poultry or poult
poultry
ry   hcs
cspil
pilollzed pd ieols Ceotrd
Ceo trdk ia. Eur op
op  cse#aml
cse#a mlvvir , zcnam tvi,
tvi,  m
;o
;o  
 prod.I cts ca, be a wrrh H5N
H5NII hi<;/,  ai d th e Midd e Ecs
Ecstt     Allhou<;I, th
• the
e
sou,,c ed inf e ction 
sou (- 60%
60%)  vo: cin
cins
s a e  co 
co 
 •  Severe illlln
neES
eESdso
dso   lmmun ogen
ogeniic, CJ) 
CJ) 
fa H7N77N7but
but milmild fa
fa   unkno.vn eff ecf
ecf tveos s in
in   -0 
(1) 
d her
her QI ia, inf lueo
ueozza p r eventin
eventingg th
thee HSN
SN1 1 ()
 
sul:fyp,s (<!.9 , H9N2)   Inf ecti
ection
on or
or1ed.J
1ed.Jcl
cln
ng
dis ese1erlty  -I
0 
-0 
-0 
 An
 Anth
thrax
rax  Bacil lus
lu s anthracis   •  Contactw
Contact with
ithp
pr od.J
d.Jet
ets
s  •   Ac ut
ute
e skJn inf ec tion   Sporadc ca:83 occur 
• occur   •  Vefy lo.vfor
o.vforma:t
ma:t   •  Moprophyo
Moprophy oi ds  i"i' 
V,  
from Inf ect
ected a,lm
a,lm    (mat common f 01m01m) in a, im
imaa b:w or 
b:w dl  vide  h01
01e
elera  v o: c ln
lne
e ava ilcbl e 
(md
(md nlvcolli
nlvcoll ie, gods,
gods,  •  Untr ed
ed ed Inf ection
ectionss    Occ cc:iona
• cc:iona l outbted<s 
outbted<s  fa peop
peoplled  s 
sheep)
heep),, such cc:  m01sp-eodto  Inttililea
ea and Cenhd
Cenhd   hlg,r isk
isk becruse -0
-0  
led he, 01
01woolen
woolen r eg
eg ond lymph Asiia 
As d oec upd l ond Ill 
Ill 
g:xx:k , 01saiv en
enlrs
lrs node; a nd to t he
he ecpa:
ecpa: ur e to B.  el 
modefr 
mode fr om
skin s 
om cnlmd bloocht
bloochtr 
r eom,
eom, a, d
ma,,befatd.
ma,,befatd.  
anthr o:.IS
o:.IS nd
commeiclaUy
commeicl
s·
•  Contact with
withsoi
soill  avalk
ava lkb
b le In ma.I 0
(!J  
(!J 
conttcin
con cinin
ing
g a,f hr 0<
0<   co untries  '<  
'<
sp01es  •   Avoid
 Avoidd dir ect
ect con
contto:.
o:.tt 
with so
solli aid with
ith  
prod.Jets d cn imd
or igin. 
Bruc
Brucell
ellcc
cc  Sev
Sever 
er al spec
specii es d   •  Dir ect
ect con
contto: t with
ith   •  Generalized
Generaliz ed inf ecfi
ecfioo n  •  Wor ldv i d in a, imah  Lo.v  
Lo.v    No p,oph yl oco 
• oco 
Brucello ba cter ia  inf ecledcdt
ecledcdtlle  roiid ou;: on.e-t,
withiro on.e-t,   •  t'v'tc:stt common in
t'v'tc:s in   •  Vcitt
Vc itto
o rurd a,d
a,d      Avoidconsumi:;tion
• i:;tion  
(Bruce/
Bruce/la la a borlus)
borlus), cru sin
sing g con tinu
tinuous
ous or   00/ elopin
elopingg countries
countries,, ag icuttur a l aecc,
aecc,   of  unparleu1 ized   m ililk
ized k
clog;((8. can fa ), p i g:
clog; g:   intermit
int ermitttent f ever
ever a,d South
Sou th Amer 
 Amer ica, intake
ake d   10.v,  and mililkk products 
(8. ..,;,), a sheep aid  mdct:e,whi
mdct:e,w hich mO{   Centr 
d  Asi
Asia,
a,  th
th  e unpa;:
un pa;:teu,iz
teu,iz ed m ilk    Avoidd
•  Avoiddir 
ir ect
ect con
contto:.
o:.tt 
Gods (B.mei- • •   I  la;f for months if net
net   Mediterra,
Mediterra, ern , aid increccethe r k   with a,
a,iimah, 
•  ConsumPiond 
ConsumPion d   lr eded
eded o::leq,dely   the
the MddeE
MddeEa;t   paf icula ly cd ll lle;
e;  
unpa.teu1 i.?:ed 
i.?:ed  ( 10.v) •  Rel
Relap.e
ap.e commo n ,;iods aid sheep,   -I>
-I>  
milkor
milk or chee.e
ee.e   ctte
ctt e, tr ed
ed ment
ment  --.J  
"'
 

Geog
Geograph
raphiic
Disease
sease   CHAPTER
Cau
Cause
se   8: Special
anTopics
Tr an smIssiin
smIssi Natur e ot  disease 
on Parasitology
on   431 Risk
sktor
tor trav
traveeletS
etS   Pr eva1tl01
eva1tl01 
dist
stri
ribu
bu ti 01  
ti01
Hu m a1 
a1  HIV-I ond HIV-2
HIV IV-2,, whi
hicc h  •  T,
T,ai
ai sm ti:si
ti:sion fhr ou c;ti 
c;ti  •   Acute1
 Acute 1eh01i1a l  •  WOf dl  vide,
de,   in
incc r ea; 
ea;   ed •  Unp,d ecfed sex
sex   •  Mo v a:: cin
c ine
e yef  
lmmunodef iciencv  o,e 1et
etr 
r 01in
01in...ise;  bloodondbod{-
bloodondbod{-flui
fluid,
d,   synd ome
synd om e s
siimililo
or with 0 1easuch a:
in0
in and dhe,high-rtk
dhe,high-rtk   •   Paf -e::pa.
-e::pa. u,
u,e 
virus (HM CClJS
irus CClJSiing
ng   •  Veriicd tr a-ismisslon
a-ismisslon   lnfluenzo
lnflu enzo ike illne;:s
illn e;:s    Af rica,p
rica,p r eval
evalenc
ence
e   behOY'iors  p r ophyl
ophy l O(.is 01d lobl e  
/J,cq.. r ed
ed •   Se<
e<ud
ud fr orem
orem 6Si
6Sion
on   •  WCEfin g.  
fing. dffers in dfferent r isk ·  •  Hi1#, -oclwe 
Immunodef iciency •  Blood
oodhhQ"E:fus
Q"E:fusiion lvmphodenopolhy  goup;:(men
goup;: (men h01in
h01ing
g  onti
ntie
,  t101i1
e ds
Svnd om e (,6JC6)
(,6JC6)   pod.,ct,  •  Ptog r esstve
esstve dec:lin
dec:line
e in
in   eec:with men , rv diug  avoililci:>l
ci:>le
e fc:lf  
CD4 + cou nt rr wtthoul
wtthoul   1£ers,, com merci
1£ers mercid sex  fle
fled m ent 
hed menf 
menf   WO<!<= ) 
)    Sdesec: 
•

•   AIDS-do/ lnln
 AIDS lnlng
g 
111n onceCD4+
slgnlflca"ltty,kw   n 
I 
lnfl
lnfluen
uenz (HI NI I 
zo A (HI Infl
Influen
uenzz a A(HlMl) v ir us
us   •  Droplets "" pel
pellle d b{ •  Similila
ar to secsonol 
to secsonol •  WOf dl  vid e  Riskd ocq.i irin
iring
g •  Vaccin
accine e 01oil ilcb
cblle  )> 
- ne.v r eassortment
eassortment   coughin
coug hing
g or sneez
eezin
ing
g  influenza
influ enza   influenzo
influenzo A (HI
(HINNI I •  Coul#, et etiiq,,ett
q,,ettee  "'(J  
"'(J

vl1u
l1uss nd r ek
ek ded to •  Di
Dir 
r ect
ect contoc.t wtth no.vedsts
no.v edsts wodd
wodd vtde,
vtde,  Hondhygene  -I 
•  M ldd sea e e  • 
m
previous or cun
cunent
ent   Infected
Infect ed surfex.es  •  Hlg,
Hlg,rlak
rlak goupo
goupo   ,.peclotly In aeaad •  Serr -iaold lon OI  ;:o
;:o  
hum o nsea onal •  l o kn01vn lnstonct:S
lnstonct:S   such a eldert.{ or   01ercr 
01erc r 01vdng
01vdng   quarantineIf
quarantine If Infected 
Infected 
Influenza
Influenz a vlru
lrust:S
st:S  d peoplebeng
peoplebeng   chllid
ch idr 
r enmaydevelop
enmaydevelop •  Trotelers shou
shoulld be (f)  
(f)
Infect ed b{ ep o; ur e  cornpllcatlons,  c,,,vaed sl gi gi d -0 
-0 
(1) 
to pl or dher •   Acute
 Acuter r esplrd
esplrd or y  seve.ltyands   ()
  a,iimct 
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e
L  CHAPTER 8: Special Topics in Parasitology
e
L    433 
 

CHAPTER 8: Special Topics in Parasitology   437 

incubation period. According to the CDC, in the likelihood of infection vis-a-vis an infection
terms of clinical severity, most travel-related with a bacterial etiology increases with the
illnesses are mild. Approximately 1 to 5% of duration of symptoms. Parasites may also be the
travelers become sick enough to seek medical likely etiologic agent for diarrhea unresponsive
 care either during or after travel. A careful travel to antibacterials. Examples of intestinal parasites
history, therefore, should be part of the routine that may cause persistent symptoms include
medical history for every ill patient, especially  Cryptospo ridium parvum , Cystoisospora belli, 
belli, 
those with a febrile illness. Of particular concern  Entamoeba histolytica , microsporidia , and
are adventure travelers and persons visiting  Dientamoeba fragilis , as well as Cyclospora
friends and relatives overseas, since they are at   cayetanensis. Other tests that may be requested
greater risk for becoming ill due to increased
exposure to pathogens.  
in the evaluation
includes of patients
stool microscopy with
with p ersistent
persistent
at least TD 
three ova
The most frequent health problems and parasite stool examinations, Clostridium
encountered by returned travelers are broken difficile toxin assay, D-xylose test, duodenal
down as follows: aspirate, or empiric treatment for Giardia. 
1.  Persistentgastrointestinalillness(10%)  References 
 –  diarrhea
 diarrhea was more common for
Centers for Disease Control and Prevention.
travelers returning from South Central CDC health information for international
Asia 
travel 2010. Atlanta: U.S. Department of
2.  Skin lesions or rashes (8%) – 
(8%) –  insect
 insect
Health and Human Services, Public Health 
 bites, pyoderma,
pyoderma, scabies, allergic
allergic rash,
and cutaneous larva migrans; most er ivniceeD
iS p
Phil p ; 2e p
00a9r t.ment of  Tour ism. Industr y
frequent diagnoses among travelers  performance statistics article: tourist
returning from the Caribbean, Central volume in top destinations grew by
or South America  
6.64% in the first quarter of 2010
3.  Respirat ory infect ions (5-13% ), [Internet]. 2010 [cited 2010 Nov 15].
depending on the season of travel 
4.  Fever (up to 3%) –  associated with the Available from www.tourism.gov.ph/Pages/
from www.tourism.gov.ph/Pages/
IndustryPerformance.aspx.
most serious complaints since certain Philippine Society for Microbiology and
conditions may be life-threatening
Infectious Diseases with the Philippine
(malaria) or may pose public health
Foundation for Vaccination. Handbook
hazard (measles, tuberculosis);
tuberculosis); malaria, on adult immunization for Filipinos
typhoid, and dengue were identified as [Internet]. 2009 [cited 2010 Nov
the most frequent causes of systemic 15]. Available from http://www.
from http://www.
febrile illness among travelers from 
 psmid.org.ph/contents/Handbook_
any region  on_Adult_Immunization_2009_%28con
While bacteria accounts for most TD tents%29.pdf
cases, persistent
persistent symptoms suggest protozoan World Health Organization.
Organizatio n. International travel
 parasites as
as the etiology. In fact, in chronic and health 2010. Geneva: World Health
diarrhea, parasites are commonly isolated, and  Organization; 2010.

 
  Appendices
 Appendices 

437 

 
 

 APPENDICES 439 
 

440   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

 APPENDICES 441 
 

442   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

 APPENDICES 443 
 

444   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

 APPENDICES 445 
 

446   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

 APPENDICES 447 
 

448   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

 APPENDICES 449 
 

450   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

 APPENDICES 451 
 

452   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

 APPENDICES 453 
 

454   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

 APPENDICES 455 
 

456   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

 APPENDICES 457 
 

458   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

 APPENDICES 459 
 

460   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

 APPENDICES 461 
 

462   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

 APPENDICES 463 
 

464   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

 APPENDICES 465 
 

466   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

 APPENDICES 467 
 

468   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

 APPENDICES 469 
 

470   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

 APPENDICES 471 
 

472   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

 APPENDICES 473 
 

474   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

 APPENDICES 475 
 

476   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

 APPENDICES 477 
 

478   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

 APPENDICES 479 
 

480   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

 APPENDICES 481 
 

482   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

 APPENDICES 483 
 

484   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

 APPENDICES 485 
 

486   MEDICAL PARASITOLOGY IN THE PHILIPPINES 

 

 APPENDICES 487 
 

488   MEDICAL PARASITOLOGY IN THE PHILIPPINES