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Journal of Microbiology, Immunology and Infection (2017) xx, 1e6

Available online at www.sciencedirect.com

ScienceDirect

journal homepage: www.e-jmii.com

Original Article

Treatment of larva migrans syndrome with

long-term administration of albendazole
Amy Hombu, Ayako Yoshida, Taisei Kikuchi, Eiji Nagayasu,
Mika Kuroki, Haruhiko Maruyama*

Division of Parasitology, Department of Infectious Diseases, Faculty of Medicine, University of

Miyazaki, Japan

Received 9 November 2016; received in revised form 24 March 2017; accepted 5 July 2017
Available online - - -

KEYWORDS Abstract Background: Larva migrans syndrome is a food-borne parasitic disease in humans,
Albendazole; caused by accidental ingestion of eggs or larvae of ascarid nematodes, namely, Toxocara canis,
Larva migrans Toxocara cati, or Ascaris suum, the roundworms commonly found in the intestines of dogs, cats
syndrome; and pigs respectively. When a patient is diagnosed as having larva migrans syndrome, oral-
Ascaris suum; administration of albendazole is recommended, however, the regimen remains controversial
Toxocara canis; worldwide. In Japan, the duration of albendazole administration is longer than those of Euro-
Toxocara cati pean and North American countries. The purpose of this study was to assess the efficacy and
safety of long-term administration treatment of albendazole for larva migrans syndrome.
Methods: From 2004 to 2014, our laboratory was involved in the diagnosis of 758 larva migrans
syndrome cases, of which 299 cases could be followed up after the treatment. We analyzed
these 299 follow-up cases on the ELISA results before and after the treatment as well as on
anthelmintic used, dose and duration of medication, clinical findings, and side effects, re-
corded on a consultation sheet provided by the attending physicians. We have 288 cases as
the subjects of this study.
Results: Albendazole represented a 78.0% efficacy rate. The side effects represented 15.0% in
using albendazole alone cases; however, the side effects were mild to moderate and there
were no severe cases reported.
Conclusions: The long-term administration treatment of albendazole is safe and effective for
larva migrans syndrome.
Copyright ª 2017, Taiwan Society of Microbiology. Published by Elsevier Taiwan LLC. This is an
open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-
nc-nd/4.0/).

* Corresponding author. 5200 Kihara, Kiyotake, Miyazaki 889-1692, Japan. Fax: þ81 985 84 3887.
E-mail address: [email protected] (H. Maruyama).

http://dx.doi.org/10.1016/j.jmii.2017.07.002
1684-1182/Copyright ª 2017, Taiwan Society of Microbiology. Published by Elsevier Taiwan LLC. This is an open access article under the
CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Please cite this article in press as: Hombu A, et al., Treatment of larva migrans syndrome with long-term administration of albendazole,
Journal of Microbiology, Immunology and Infection (2017), http://dx.doi.org/10.1016/j.jmii.2017.07.002
 + MODEL
2 A. Hombu et al.

Introduction migrans syndrome with an aim to establish a standardized

effective treatment regimen.
Larva migrans syndrome (LMS) is an important food-borne
parasitic disease caused by Toxocara canis, Toxocara cati, Methods
or Ascaris suum, the ascarid roundworms commonly found
in the intestines of dogs, cats and pigs respectively.1e4
Humans acquire infections by accidental ingestion of Ethical clearance
embryonated eggs or infective larvae of these parasites.
The source of infections is contacting with contaminated This retrospective clinical study was approved by the
soil where infected dogs and cats defecated, or taking Research Ethics Committee of Faculty of Medicine, Uni-
contaminated foods, which include raw or undercooked versity of Miyazaki, under the title of “Surveillance of
meat as well as unwashed fruit or vegetables.2,5 The parasitic diseases in Japan” (permission # 2014-087). Our
magnitude of infection depends on the number of ingested study strictly adhered to the Ethical Guideline for Clinical
larvae or embryonated eggs.6,7 Once the embryonated eggs study released from the Ministry of Health, Labour and
or larvae are ingested, larvae penetrate through the in- Welfare, Japan.
testinal wall and migrate via circulatory system to the liver,
lungs, central nerves system, or eyes causing larva migrans Patients analyzed in the present study
syndrome (LMS). LMS can be classified into four major
clinical presentations based on the involved organs: visceral From 2004 to 2014, our laboratory conducted serological
larva migrans (VLM), neural larva migrans (NLM), ocular tests of 4934 cases, of which 758 were judged positive for
larva migrans (OLM), and asymptomatic type (referred to as ascarid infections (see below). Among them, we had 299
‘covert type’ in some literature).3,7e9 follow-up cases with recovery criteria described herewith,
As for the treatment of LMS, it is widely accepted that there were 288 cases as the subjects of the present study
albendazole is the first choice, though the regimen partic- (Fig. 1). Upon antibody tests, both at initial diagnosis and
ularly the optimal duration has not been standardized follow-up study, we asked attending physicians for
yet.7,10e13 When an individual is diagnosed positive for LMS, providing us with a consultation sheet describing age, sex,
most institutions in Europe and the US recommend treat- place of accommodation, ethnic background, chief
ment with oral-administration of albendazole at 400 mg complaint, medical history, administered drugs and its dose
twice a day for five days for both adult and pediatric.4,5 and duration, dietary history, overseas traveling history,
However, the regimen showed only 32% clinical cured rate medical imaging findings, and laboratory data. Side effects,
in a previous study.14 On the other hand, in Japan, the if any, were also supposed to be recorded on the consul-
recommended treatment for LMS has been 10e15 mg/kg/ tation sheet.
day taken orally for one cycle of four weeks following by Based on the information, the regimen data were cate-
two weeks of drug free and an additional one cycle of four gorized into four groups. Patients treated with only alben-
weeks, which is based on the regimen for echinococcosis.15 dazole were grouped as albendazole group. For patients
In this study, we assessed the efficacy and safety of long- treated with anthelmintic other than albendazole and
term administration treatment of albendazole for larva switched to albendazole or vice versa, these patients were

Figure 1. Flow chart of the process to evaluate the efficacy of albendazole.

Please cite this article in press as: Hombu A, et al., Treatment of larva migrans syndrome with long-term administration of albendazole,
Journal of Microbiology, Immunology and Infection (2017), http://dx.doi.org/10.1016/j.jmii.2017.07.002
 + MODEL
Long-term albendazole treatment for larva migrans 3

grouped as albendazole plus other anthelmintic group. Follow-up study was carried out three to four months
Patients treated with anthelmintic other than albendazole after the initial diagnosis in most cases. When follow-up
were grouped as other anthelmintic group. Patients patients became antibody negative, or showed decrease in
received no anthelmintic treatment were grouped as no serum anti-parasite antibody concentration (more than 30%
anthelmintic treatments group. of reduction in optical densities at 1 to 2700 dilution in
Along with the symptoms, we also examined side effects ELISA) and with one of the following findings, we consid-
recorded on consultation sheets to assess the safety of the ered them as ‘recovered’: peripheral blood eosinophilia
anthelmintic used. Although we did not set standardized returned to within the normal range; disappearance of
format for recording side effects on the consultation sheet, symptoms and/or abnormal medical imaging. In addition,
attending physicians who had adverse events with alben- when previously positive local body fluid samples turned
dazole treatment frequently contacted us in e-mails and/or negative or reduced more than 30% of reduction in optical
phone calls because of the lack of the treatment experience densities at 1 to 900 dilution in ELISA, we judged these
(note that nematode infections are rare in Japan). There- patients as ‘recovered’. Fig. 1 showed the flow chart for
fore we consider that we could collect substantial portion, if the evaluation of the efficacy of albendazole.
not all, of the adverse side effects during the treatment.
Disease types
Enzyme-linked immunosorbent assay (ELISA)
In this study, we analyzed the clinical manifestations and
Sera and body fluid samples, such as pleural effusion and divided patients into five disease types based on clinical
ascites, sent by the attending physicians to our laboratory, findings provided in the consultation sheet16: Visceral larva
were tested for specific antibodies in enzyme-linked migrans (VLM) were cases with typical eosinophilic pneu-
immunosorbent assay (ELISA). Antigen preparations used monia, multiple nodular lesions in liver or lungs with
in ELISA were Ascaris soluble worm antigen preparation (As- eosinophilia, or pleural eosinophilia showing symptoms like
SWAP) and excretory/secretory (ES) antigen of T. canis cough, dyspnea or chest pain. Ocular larva migrans (OLM)
larvae (Tc-ES).16 In our standard procedure, samples were were cases of visual disturbance with uveitis and/or retinal
first tested for the binding to As-SWAP and Tc-ES, and in nodular lesions. Neural larva migrans (NLM) were cases
non-visceral types (see below), samples were further associated with neurological disorders showing symptoms
tested in ELISA with ES antigen of A. suum larvae (As-ES), or like paresthesia, muscle weakness, or urination disorder.
in Western blotting (LDBIO Diagnostics, Lyon, France) for Asymptomatic were cases with no specific symptoms or
the confirmation of the diagnosis. objective findings other than simple peripheral blood
In ELISA, wells of microtiter plates (Nunc, Roskilde, hyper-eosinophilia. Miscellaneous were symptomatic cases
Denmark) were coated overnight at 4  C with 2 mg/ml of As- other than VLM, OLM or NLM. This type included cardio-
SWAP or 1 mg/ml of Tc- or As-ES in 0.05 M carbonate- vascular involvement such as myocarditis or pericarditis,
bicarbonate buffer (pH 9.6). Wells were washed with cutaneous involvement such as skin rash, and gastrointes-
PBST (PBS containing 0.05% Tween 20), blocked with 1% tinal involvement such as diarrhea or abdominal pain.
casein (Nakarai Tesque, Kyoto, Japan), and incubated with
diluted sera (1: 900 and 1: 2700) for 1 h at 37  C. After
Statistical tests
washing with PBST, binding of antibodies was detected with
horseradish peroxidase conjugated rabbit anti-human IgG
All the statistical tests (Fisher’s exact test and chi-squared
(Dako, Glostrup, Denmark). For color development, ABTS
test) were performed with a significance threshold of
(KPL, Gaithersburg, MD, USA) was added and incubated at
p < 0.05.
room temperature for 30 min in the dark. Optical density at
405 nm was read in a Microplate Reader (Bio-Rad Labora-
tories, Hercules, CA, USA). Based on negative control serum Results
data, we set a cut-off point at 0.200 for 1: 900 diluted sera,
pleural effusion, and ascites. For body fluids such as CSF
Outcome of the treatment
and vitreous humor fluid, optical density more than 0.1 at
1: 30 dilution were judged positive.
Among 299 follow-up LMS cases, 11 cases were excluded
from the study due to the optical densities were not
Diagnosis of LMS and the criteria for recovered and reduced even the clinical symptoms improved as shown in
unrecovered Fig. 1. We have 288 cases for the present study. There were
246 patients treated with albendazole which represented
At initial diagnosis, the positive cases were determined by 85.4%; and 16 cases (5.6%) were treated with albendazole
at least one of the followings: (1) positive reactivity of plus other anthelmintic; 19 cases (6.6%) were treated with
serum or body fluid samples to Toxocara spp. or A. suum other anthelmintic; and seven cases (2.4%) received no
antigens; (2) clinical information from the applications anthelmintic treatments.
recorded by physicians in charge along with any available In 246 cases which were treated with albendazole alone,
medical imaging techniques such as ultrasound, computed 192 cases recovered and 54 did not, representing recovery
tomography, and magnetic resonance imaging indicated rate of 78.0%. In 16 cases with the treatment with alben-
lesions in lungs/liver with positive reactivity of serum to dazole plus other anthelmintic, eight cases recovered and
support diagnosis of ascarid infections. eight cases failed to recover, which represented 50% of

Please cite this article in press as: Hombu A, et al., Treatment of larva migrans syndrome with long-term administration of albendazole,
Journal of Microbiology, Immunology and Infection (2017), http://dx.doi.org/10.1016/j.jmii.2017.07.002
 + MODEL
4 A. Hombu et al.

recovery rate. In cases which patients were not treated cases from a few days to 17 weeks with most cases allo-
with albendazole, 11 cases recovered and eight cases un- cated in four weeks and eight weeks; there were some
recovered, which represented 57.9% recovery rate. In those cases without indication. The recovery rates of different
cases using other anthelmintic, ten cases were adminis- medication groups were not different significantly, reach-
tered ivermectin, showing the recovery rate of 70% ing approximately 80% in each groups (Table 2). It appears
(Table 1). that at least a portion of LMS caused by ascarid roundworms
is self-limiting.
Age and sex distribution
Side effects
We examined age and sex distribution of recovered and
unrecovered patients to see if age or sex could have
We analyzed the side effects from using albendazole alone
affected the efficacy of albendazole. The male to female
cases. There were a total of 37 cases out of 246 cases re-
ratio was 2.15 (131:61) in recovered group and 2.86 (40:14)
ported side effects representing 15.0%. Among them, there
in unrecovered group. The average age was 49.0 (range
were 25 cases from recovered group with the following
8e82 years old) in male and 47.1 (range 20e85 years old) in
symptoms: 21 cases of liver dysfunction, two cases of
female in the recovered group. The average age was 54.5
depilation, one case of vomiting, and one case of skin rash.
(range 30e84 years old) in male and 55.7 (range 25e76
There were 12 cases from unrecovered group with the
years old) in female in the unrecovered group. In both
following symptoms: 11 cases of liver dysfunction, and one
groups, the peak for male patients was in their 50s whereas
case of nausea (Table 3). Thus, the occurrence rate for
in female patients was pretty much evenly spread out
recovered group was 13.0% (25/192); the occurrence rate
among the age groups of 20s, 30s, 50s, and 60s. Male pa-
for unrecovered group was 22.2% (12/54).
tients were more than female patients in every age group
Then we examined when side-effects appeared by
except in 20s (Fig. 2). There were no significant differences
comparing groups with different medication duration. We
in the age and sex distribution between recovered and
found that patients treated less than four weeks or treated
unrecovered groups.
for five to seven weeks had higher side effects rate
compared to other groups (Table 4). It should be noted that
Disease types patients treated for eight weeks or more had less side ef-
fects rate. These findings indicate that the appearance of
We then investigated the disease types among recovered side effects does not simply depend on the duration of
and unrecovered groups, suspecting that some disease type medication.
might have resistant to the treatment. In the recovered There were four cases in each of the recovered and the
group, there were 91 cases of VLM, 23 cases of OLM, 30 unrecovered groups that used albendazole and when the
cases of NLM, 34 cases of Asymptomatic, and 13 cases of liver dysfunction side effect appeared, they switched to
Miscellaneous (n Z 191). There was one case that was not other anthelmintic mainly ivermectin. There were three
included due to lack of medical information on the liver dysfunction cases worth mentioning: (1) one case
consultation sheet. In the unrecovered group, there were which was treated for four weeks and when liver dysfunc-
22 cases of VLM, 11 cases of OLM, five cases of NLM, 13 tion occurred the treatment stopped for two weeks and
cases of Asymptomatic, and three cases of Miscellaneous resumed treatment for two weeks; (2) one case was treated
(n Z 54). Again, there were no significant differences in the for one week and reduced dosage for three weeks; (3) one
efficacy of albendazole treatment among the disease types. case ignored the side effect and continued treatment for a
total of ten weeks. All these three patients were recovered
Duration of medication and once albendazole treatment stopped, liver dysfunction
was reversed.
The recommended treatment in Japan is orally adminis-
tration of albendazole at 10e15 mg/kg/day for a cycle of
Discussion
four weeks followed by two weeks of drug free interval and
repeat another cycle of four weeks of medication. How-
ever, the length of treatments varied among follow-up Albendazole is a broad spectrum anthelmintic effective to
nematode infections in general,17 and has been used for the
treatment of larva migrans syndrome (LMS) caused by
ascarid roundworms as well. However the regimen of
Table 1 Outcome of treatment.
albendazole for ascarid LMS treatment still remains
Medication Recovered Unrecovered Recovery controversial. Literatures and institutions recommend
rate 400 mg twice a day for five days without specifying opti-
Albendazole 192 54 78.0% mum duration,3,4,13 though in neurotoxocariasis, albenda-
Albendazole 8 8 50.0% zole is used for a period of at least three weeks, which
þ Other often needed to be repeated.18 In cases with cardiac
Anthelmintic involvement, various regimens have been employed, such
Other Anthelmintic 11 8 57.9% as 800 mg/day for two weeks, 50 mg/kg/day for 28 days,
(Ivermectin) 7 3 70.0% 600 mg/day for 14 days, or 1000 mg/day for four weeks
(reviewed by Kuenzli E et al.).19 Importantly, Sturchler

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Journal of Microbiology, Immunology and Infection (2017), http://dx.doi.org/10.1016/j.jmii.2017.07.002
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Long-term albendazole treatment for larva migrans 5

Figure 2. Age and sex distribution in male and female patients in recovered and unrecovered groups.

Table 4 Onset of side effects in different administration

Table 2 Recovery rate in different administration
duration.
duration.
Duration Cases %
Duration Cases %
<4 weeks 11/46 23.9%
<4 weeks 35/46 76.1%
4 weeks 14/76 18.4%
4 weeks 60/76 78.9%
5e7 weeks 7/22 31.8%
5e7 weeks 18/22 81.8%
8 weeks 2/75 2.7%
8 weeks 61/75 81.3%
>8 weeks 2/17 11.8%
>8 weeks 14/17 82.4%
not described 1/10 10.0%
not described 4/10 40.0%
Total 37/246 15.0%
Total 192/246 78.0%

et al. reported that the standard five days regimen of

albendazole showed only 32% cure rate.14
In the present study, we showed that albendazole had
Table 3 Symptoms of side effects. overall recovery rate of 78.0% against LMS caused by ascarid
Symptom Recovered Unrecovered Total nematodes when used for four or eight weeks, which was
much higher than the five days regimen.14 Recovery rate
Cases Cases was 78.9% and 81.3% for four weeks- and eight weeks-
Liver dysfunction 21 11 32 administration, respectively. Furthermore, the present
Nausea and vomiting 1 1 2 study also indicates that the long-term albendazole
Skin rash 1 0 1 administration was effective equally to all disease types
Depilation 2 0 2 including OLM. This is in the accordance to the previous
Total 25 12 37 studies that revealed that OLM required a long-term
administration treatment.20e23 To the best of the author’s

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6 A. Hombu et al.

knowledge, this is the first research that has included a 5. Woodhall D, Fiore A. Toxocariasis: a review for pediatricians. J
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Journal of Microbiology, Immunology and Infection (2017), http://dx.doi.org/10.1016/j.jmii.2017.07.002