Iranian Journal of Veterinary Science and Technology

Vol. 3, No. 2, 2011, 49-56 IJVST

A case report of atypical borreliosis in a dog

Amir Rostami1, Mahdieh Zaeemi2#, Norair Piazhak3,

Ramin Mazaheri Nezhad Fard4*
1
Department of Small Animal Internal Medicine, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran
2
Department of Clinical Sciences, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran
3
Department of Parasitology, Pasteur Institute of Iran, Tehran, Iran
4
Rastegar Reference Laboratory, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran

Received: June 7, 2009 Accepted: November 22, 2009

Abstract
Borreliosis is a bacterial zoonosis transmitted by arthropods. The infection is more common
in dogs than other domestic animals. A one-month-old puppy with fever, jaundice and digestion
disorder was referred to Small Animal Teaching Hospital, University of Tehran. Laboratory
findings included severe regenerative anemia, neutrophilia, thrombocytopenia, strong
spirochetemia and significant changes in serum proteins. Attempt to isolate the bacteria in
laboratory animals was unsuccessful. The infection was cured using antibiotics and the animal
was completely recovered.

Keywords: Borreliosis, zoonosis, dog, arthropod, tick, Iran

                                                            
*Corresponding author: Ramin Mazaheri Nezhad Fard
Email: [email protected] 
#Current address for Mahdieh Zaeemi: Department of Clinical Sciences, Faculty of Veterinary Medicine, Ferdowsi
University of Mashhad, Mashhad, Iran

Iranian Journal of Veterinary Science and Technology, Vol. 3, No. 2 

50 Rostami A., et al.

Introduction cases while injection ceftriaxone (third-

Borreliosis is an endemic zoonosis mostly generation cephalosporin) is used in chronic
transmitted by ticks and possibly other and resistant infections or in hypersensitive
arthropods such as fleas and bloodsucker cases (Duffy, 1990, 1987). Furthermore,
insects (Fritz and Kjemtrup, 2003). The Borrelia spp. is sensitive to erythromycin
causative agent is classified in Order (alternative option) and chloramphenicol.
Spirochaetales, Family Spirochaetaceae and Antibiotics should be prescribed for at least 14
Genus Borrelia (Paster and Dewhirst, 2000). days but are recommended to continue for 30
Borrelia spp. are Gram-negative, spirilliform days (Garbe, 1991); however, they do not
and motile bacteria that are host dependent and eradicate the bacteria (Straubinger et al.,
are not found in nature (Steere, 2001). At least 1997). Use of corticosteroids such as
four species—Borrelia persica, B. microti, B. prednisolone for two weeks helps to eliminate
baltazardi and B. latyschewii—have been disease symptoms and reduces the pain,
identified in Iran, mainly transmitted by promising more relief for the patients
Argasidae soft ticks (Nekoei and Asmar, 1996, (Straubinger et al., 2000). Prophylaxis of
1993; Barbour and Hayes, 1986). These ticks borreliosis is based on the vaccination and tick
infect mammals such as dogs, cats and humans control programs including avoid of
while bloodsucking (Bushmich, 1994). Dogs contaminated area, use of appropriate cover,
are the most infected animals amongst the pets body check and tick removal, use of acaricides
(Guerra et al., 2001). The potential risk of and bush trimming (Patey, 2007). Antibiotic
simultaneous transmission of other genera prophylaxis is still not known to be quite
such as Leptospira, Treponema, Ehrlichia, effective and does not guarantee an ideal
Babesia and Giardia with Borrelia increases prevention (Mullegger, 2004).
the importance of the disease (Skarda, 2005;
Case Presentation
Mullegger, 2004). Estimation of infected ticks
in city suburbs such as parks, playgrounds and A one-month-old female mixed puppy with
rural counties is necessary for the evaluation diarrhea, malaise, anorexia and pustules was
of borreliosis risk in societies (Guerra et al., referred to Small Animal Teaching Hospital,
2001). Light or darkfield microscopy is used in Faculty of Veterinary Medicine, University of
dogs for diagnosis of Borrelia infections in Tehran. The puppy was suffering from poor
addition to silver staining and serological health condition and had been attacked by
assays such as enzyme-linked immunosorbent many ectoparasites such as lice and soft ticks.
assay (ELISA), Western blot, and No history of living condition, vaccination or
immunofluorescence antibody techniques treatment was available except that the animal
(FAT) (Appel et al., 1993; Golightly et al., was kept in a rural area with three siblings.
1990). Molecular techniques such as Serial blood samples were collected and sent
polymerase chain reaction (PCR), genome to clinical pathology laboratory. Later, other
sequencing and fingerprinting are more puppies were clinically examined and blood
accurate but need special methods and samples were taken. All cases were followed
facilities (Wang et al., 1999). Bacterial up for a few weeks.
isolation and culture represent the most
reliable methods for the detection of Borrelia Results
spp. but are not easily performed (Nielssen et Fever, icteric mucosa and pain on palpation
al., 2002). Treatment scheme is based on the were found during the clinical examinations.
use of tetracyclines or penicillins (Przytula et No neuropathy, ophthalmopathy, arthritis or
al., 2006). Oral doxycycline and amoxicillin lameness was diagnosed. Laboratory findings
are the most common antibiotics used in usual included severe regenerative anemia

Iranian Journal of Veterinary Science and Technology, Vol. 3, No. 2

 A Case Report of Atypical Borreliosis in Dog 51

(anisocytosis, hypochromia and had normal blood values (including a mild

reticulocytosis), neutrophilia (toxic regenerative anemia) and lacked
neutrophils), thrombocytopenia and strong spirochetemia. Spirochetes were seen in blood
spirochetemia in direct microscopy of Giemsa- samples of the fourth puppy but the number of
stained blood smears (Figures 1 and 2). The bacteria was significantly low. Since no
hemogram included erythrocyte, 9.1 × 105/µl; special report had been published on antibiotic
hemoglobin, 3.8 g/dl; hematocrit, 12%; MCV, resistance in Borrelia spp., the treatment
133.3 fl; MCH, 42.2 pg; and MCHC, 31%. protocol was planned based on the
The leukogram included leukocytes, 9.75 × recommended antibiotics. Doxycycline (10
103/µl; neutrophils, 87%; band cells, 1%; mg/kg, PO, BID for 30 days) and prednisolone
lymphocytes, 12%; monocytes, 0%; and (30 mg/kg, PO, SID for 7 days) were
eosinophils, 0%. Significant protein changes prescribed. Bacteremia was eradicated from
were shown in serum electrophoresis, the peripheral blood shortly after the use of
including decreases in albumin (1.92 g/dl), antibiotic and the animal’s general condition
alpha-1 (0.17 g/dl), beta (1 g/dl) and gamma seemed better. In follow up, no bacteria were
(0.49 g/dl) fractions. Alpha-2 fraction (0.82 seen in direct microscopy and the blood values
g/dl) was reported normal. Total protein value turned to normal. No clinical manifestation or
was subnormal (4.4 g/dl), while A/G ratio sign of fever, anorexia, diarrhea or pain was
(0.78) was unchanged. The attempt to isolate seen and the animal regained her lost weight.
the bacteria in sensitive laboratory animals Drug regiment and results for other puppies
was unsuccessful. Hematology of other were mostly the same.  
puppies revealed a better situation as 2 puppies

Figure 1. Borrelia spp. in blood smear (100×). Upright: a toxic neutrophil with basophilic cytoplasm.

Iranian Journal of Veterinary Science and Technology, Vol. 3, No. 2

52 Rostami A., et al.

 
Figure 2. Borrelia spp. in blood smear (100×). RBC morphology shows anisocytosis and hypochromia.
 
Discussion glucocorticosteroids (Whitney et al., 2007;
Jackson et al., 2007). Chioa et al. (2000)
Regarding to literature reviews, borreliosis studied the preventive effect of Borrelia OspA
is mostly prevalent in dogs rather than other surface antigen on lymph cell proliferation
animals (Eng et al., 1988). Despite its heavy resulting in lymphopenia.
infection, the present case lacked typical Anemia and thrombocytopenia are other
symptoms and only showed general symptoms laboratory findings in borreliosis (Shaw et
including fever, anorexia and malaise. al., 2005); both seen in this case. Unlike
Although puppies usually present symptoms recent report by Whitney et al. (2007) that
sooner than adults do, some infected animals indicates degenerative anemia in dogs with
may not present clinical symptoms (Appel et borreliosis, the patient had macrocytic
al., 1993). Experiments have shown that hypochromic regenerative anemia. This
Borrelia is potentially able to stimulate a difference seems to link to the sufficient
broad spectrum of host cells such as time needed for the activation of bone
endothelials, monocyte/macrophages, marrow hematopoiesis and release of
lymphocytes and neutrophils (Hodzic et al., reticulocytes into the bloodstream following
2008); therefore, the neutrophilia of the case is the anemia onset; as the animal’s blood
sensible. Other abnormal blood values, values shifted to normal during the disease.
including lymphopenia and eosinopenia, may Despite the laboratory findings that suggest
occur in response to endogenous an increase in blood proteins and

Iranian Journal of Veterinary Science and Technology, Vol. 3, No. 2

 A Case Report of Atypical Borreliosis in Dog 53

gammaglobulins (Scorpio et al., 2008), the References

animal suffered from a general decrease in Appel, M. J., Allan, S., Jacobson, R. H.,
serum proteins. The albumin deficiency Lauderdale, T. L., Chang, Y. F., Shin,
matches to a study by Whitney et al. (2007) S. J., Thomford, J. W., Todhunter, R.
that reports 2.5 mg/dl albumin in dogs with J., and Summers, B. A. (1993)
borreliosis. Direct microscopy of Giemsa- Experimental Lyme disease in dogs
stained blood smears and observation of produces arthritis and persistent
spirochetes seem to be the only available infection. The Journal of Infectious
diagnostic tools in the case of atypical Diseases 167, 651–64.
borreliosis because Borrelia spp. are not Barbour, A. G., and Hayes, S. F. (1986)
usually suspected in infections lacking the Biology of Borrelia species.
key signs. Furthermore, nonspecific test Microbiological Reviews 50, 381–400.
results (e.g. ESR, CBC and hepatic enzymes) Bushmich, S. L. (1994) Lyme Borreliosis in
are not practically reliable because they are domestic animals. Joural of Spirochet
subjected to change (Steere et al., 1983). Tick Disease 1, 24−28.
However, the viability of this method in Chiao, J. W., Villalon, P., Schwartz, I., and
asymptomatic dogs is questioned because Wormser, G. P. (2000) Modulation of
spirochetemia is found in healthy dogs as lymphocyte proliferative responses by
well (Greene, 1991). Since most of the a canine Lyme disease vaccine of
commercial ELISA kits and fluorescent recombinant outer surface protein A
antibodies are designed against B. (OspA). FEMS Immunology and
burgdorferi, evaluation of serum antibodies Medical Microbiology 28, 193−196.
in areas contaminated by other species is Post, J. E., Shaw, E. E., and Wright, S. (1986)
uncertain, especially in absence of a proper Suspected borreliosis in cattle. Annals
diagnostic assay. On the other hand, no of the New York Academy of Sciences
accurate data on the prevalence of Borrelia 539, 488.
spp. are available in many areas due to the Duffy, J. (1987) Lyme disease. Infectious
lack of a comprehensive survey plan. Disease Clinics of North America 1,
Therefore, establishment of a Borrelia 511–27.
survey and monitoring program is necessary to Duffy, J. (1990) Lyme disease. Annals of
prevent and control the infection and to assist Allergy 65, 1–13.
the patients. Unfortunately, blood findings Eng, T. R., Wilson, M. I., Spielman, A., and
have not already been concerned in borreliosis Lastavica, C. C. (1988) Greater risk of
and most of the papers have focused on Borrelia burgdorferi infection in dogs
borreliosis clinical symptoms and than in people. Journal of Infectious
manifestations, evaluation of serum analysis or Disease 158, 1410−11.
molecular assays for the disease (Littman, Fritz, C. L., and Kjemtrup, A. M. (2003) Lyme
2003). Therefore, papers that focus on borreliosis. Journal of the American
hematology, urinalysis and other similar Veterinary Medical Association 223,
subjects will generously support the 1261−1270.
development of a practical diagnostic protocol, Garbe, C. (1991) Borrelia infections of the
especially in case of atypical borreliosis. skin--progress of knowledge since the
Acknowledgment discovery of Lyme disease. Hautarzt
42, 356–65.
We wish to thank staffs within the Small Golightly, M. J., Thomas, A., and Viciana, A.
Animal Teaching Hospital for their kind L. (1990) The laboratory diagnosis of
help.

Iranian Journal of Veterinary Science and Technology, Vol. 3, No. 2

54 Rostami A., et al.

Lyme borreliosis. Laboratory Medicine Sierakowski, S. (2006) Diagnosis and

21, 299−304. treatment of Lyme arthritis. Przegl
Greene, R. T. (1991) Canine Lyme borreliosis. Epidemiology 60 Suppl (1), 125–30.
Veterinary Clinics of North America: Scorpio, D. G., Wachtman, L. M., Tunin, R.
Small Animal Practice 21, 51–64. S., Barat, N. C., Garyu, J. W., and
Guerra, M. A., Walker, E. D., and Kitron, U. Dumler, J. S. (2008) Retrospective
(2001) Canine surveillance system for clinical and molecular analysis of
Lyme borreliosis in Wisconsin and conditioned laboratory dogs (Canis
northern Illinois: geographic familiaris) with serologic reactions to
distribution and risk factor analysis. Ehrlichia canis, Borrelia burgdorferi,
The American Journal of Tropical and Rickettsia rickettsii. Journal of the
Medicine and Hygiene 65, 546−52. American Association for Laboratory
Hodzic, E., Feng, S., Holden, K., Freet, K. J., Animal Science 47, 23−8.
and Barthold, S. W. (2008) Persistence Shaw, S. E., Binns, S. H., Birtles, R. J., Day,
of Borrelia burgdorferi following M. J., Smithson, R., and Kenny, M. J.
antibiotic treatment in mice. (2005) Molecular evidence of tick-
Antimicrobial Agents and transmitted infections in dogs and cats
Chemotherapy 52, 1728–1736. in the United Kingdom. Veterinary
Jackson, S., Gilchrist, H., and Nesbitt, L. T. Record 157, 645−8.
(2007) Update on the dermatologic use Skarda, J. (2005) Lyme borreliosis, the present
of systemic glucocorticosteroids. diagnostic criteria. Folia Veterinaria
Dermatology and Therapy 20, 187– 49, S33−S34.
205. Steere, A. C. (2001) Lyme disease. The New
Littman, M. P. (2003) Canine borreliosis. England Journal of Medicine 345,
Veterinary Clinics of North America 115−125.
Small Animal Practice 33, 827–62. Straubinger, R. K. (2000) PCR-based
Mullegger, R. R. (2004) Dermatological quantification of Borrelia burgdorferi
manifestations of Lyme borreliosis. organisms in canine tissues over a 500-
European Journal of Dermatology 14, day postinfection period. Journal of
296–309. Clinical Microbiology 38, 2191–2199.
Nekoei, H., and Asmar, M. (1993, 3 Straubinger, R. K., Straubinger, A. F.,
December) The new studies on Summers, B. A., and Jacobson, R. H.
borreliosis in Pasteur Institute of Iran. (2000) Status of Borrelia burgdorferi
The 2nd National Congress of infection after antibiotic treatment and
Zoonoses in Iran, Tabriz, Iran. the effects of corticosteroids: an
Nekoei, H., and Asmar, M. (1996) Distribution experimental study. Journal of
of borreliosis in Iran. The 3rd National Infectious Diseases 181, 1069–1081.
Congress of Zoonoses in Iran, Straubinger, R. K., Summers, B. A., Chang,
Mashhad, Iran. pp.23−25 Y., and Appel, M. J. G. (1997)
Nielssen, A., Carr, A., and Heseltine, J. (2002) Persistence of Borrelia burgdorferi in
Update on canine Lyme disease. experimentally infected dogs after
Veterinary Medicine 1, 604–609. antibiotic treatment. Journal of Clinical
Paster, B. J., and Dewhirst, F. E. (2000) Microbiology 35, 111–116.
Phylogenetic foundation of spirochetes. Wang, G., van Dam, A. P., Schwartz, I., and
Journal of Molecular Microbiology Dankert, J. (1999) Molecular typing of
and Biotechnology 2, 341–344. Borrelia burgdorferi sensu lato:
Przytula, L., Gindzienska-Sieskiewicz, E., and taxonomic, epidemiological, and

Iranian Journal of Veterinary Science and Technology, Vol. 3, No. 2

 A Case Report of Atypical Borreliosis in Dog 55

clinical implications. Clinical N. (2007) Spirochetemia caused by

Microbiology Reviews 12, 633–653. Borrelia turicatae infection in 3 dogs
Whitney, M. S., Schwan, T. G., Sultemeier, K. in Texas. Veterinary Clinical
B., McDonald, P. S., and Brillhart, M. Pathology 36, 212−6.

Iranian Journal of Veterinary Science and Technology, Vol. 3, No. 2

‫‪Iranian Journal of Veterinary Science and Technology‬‬
‫‪Vol. 3, No. 2, 2011, 49-56‬‬ ‫‪IJVST‬‬

‫ﮔﺰارش ﻳﻚ ﻣﻮرد ﺑﻮرﻟﻴﻮز ﻏﻴﺮ ﻣﻌﻤﻮل در ﺳﮓ‬

‫‪*4‬‬
‫اﻣﻴﺮ رﺳﺘﻤﻲ ‪ ، 1‬ﻣﻬﺪﻳﻪ زﻋﻴﻤﻲ ‪ ، 2 #‬ﻧﻮراﻳﺮ ﭘﻴﺎژاك‪ ،3‬راﻣﻴﻦ ﻣﻈﺎﻫﺮي ﻧﮋاد ﻓﺮد‬

‫‪ 1‬ﮔﺮوه ﺑﻴﻤﺎرﻳﻬﺎي داﺧﻠﻲ داﻣﻬﺎي ﻛﻮﭼﻚ‪ ،‬داﻧﺸﻜﺪه داﻣﭙﺰﺷﻜﻲ داﻧﺸﮕﺎه ﺗﻬﺮان‪ ،‬ﺗﻬﺮان‪ ،‬اﻳﺮان‬
‫‪ 2‬ﮔﺮوه ﻋﻠﻮم درﻣﺎﻧﮕﺎﻫﻲ‪ ،‬داﻧﺸﻜﺪه داﻣﭙﺰﺷﻜﻲ داﻧﺸﮕﺎه ﺗﻬﺮان‪ ،‬ﺗﻬﺮان‪ ،‬اﻳﺮان‬
‫‪ 3‬ﮔﺮوه اﻧﮕﻞ ﺷﻨﺎﺳﻲ‪ ،‬اﻧﺴﺘﻴﺘﻮ ﭘﺎﺳﺘﻮر اﻳﺮان ‪ ،‬ﺗﻬﺮان‪ ،‬اﻳﺮان‬
‫‪ 4‬آزﻣﺎﻳﺸﮕﺎه رﻓﺮاﻧﺲ رﺳﺘﮕﺎر‪ ،‬داﻧﺸﻜﺪه داﻣﭙﺰﺷﻜﻲ داﻧﺸﮕﺎه ﺗﻬﺮان‪ ،‬ﺗﻬﺮان‪ ،‬اﻳﺮان‬

‫ﭘﺬﻳﺮش ﻧﻬﺎﻳﻲ ‪1388/9/1 :‬‬ ‫درﻳﺎﻓﺖ ﻣﻘﺎﻟﻪ ‪1388/3/17 :‬‬

‫ﭼﻜﻴﺪه‬
‫ﺑﻮرﻟﻴﻮز ﺑﻴﻤﺎري ﻣﺸﺘﺮك اﻧﺪوﻣﻴﻜﻲ اﺳﺖ ﻛﻪ ﺑﻮﺳﻴﻠﻪ ﻛﻨﻪ ﻣﻨﺘﻘﻞ ﻣﻲﺷﻮد‪ .‬در ﻣﻴﺎن ﺣﻴﻮاﻧﺎت ﺧﺎﻧﮕﻲ ﺳﮓﻫﺎ ﺑﻴﺸﺘﺮ ﺑﻪ ﺑﻮرﻟﻴﻮز دﭼﺎر ﻣﻲﺷﻮﻧﺪ‪ .‬ﻳﻚ‬
‫ﺗﻮﻟﻪ ﺳﮓ ﻣﺎده ﻣﺨﻠﻮط ﻳﻚ ﻣﺎﻫﻪ از ﻣﺠﻤﻮع ﭼﻬﺎر ﺗﻮﻟﻪ ﺑﺎ ﻋﻼﺋﻢ ﺗﺐ‪ ،‬زردي و ﻣﺸﻜﻼت ﮔﻮارﺷﻲ ﺑﻪ ﺑﻴﻤﺎرﺳﺘﺎن آﻣﻮزﺷﻲ ﺣﻴﻮاﻧﺎت ﻛﻮﭼﻚ داﻧﺸﻜﺪه‬
‫داﻣﭙﺰﺷﻜﻲ داﻧﺸﮕﺎه ﺗﻬﺮان ارﺟﺎع ﺷﺪ‪ .‬ﻳﺎﻓﺘﻪﻫﺎي آزﻣﺎﻳﺸﮕﺎﻫﻲ ﺷﺎﻣﻞ ﻛﻢ ﺧﻮﻧﻲ ﺷﺪﻳﺪ ﺟﺒﺮان ﭘﺬﻳﺮ‪ ،‬ﻧﻮﺗﺮوﻓﻴﻠﻲ‪ ،‬ﺗﺮوﻣﺒﻮﺳﺎﻳﺘﻮﭘﻨﻲ‪ ،‬اﺳﭙﻴﺮوﻛﺘﻤﻲ ﻧﺴﺒﺘﺎً‬
‫ﺷﺪﻳﺪ و ﺗﻐﻴﻴﺮات ﺷﺪﻳﺪ در ﭘﺮوﺗﺌﻴﻦ ﻫﺎي ﺳﺮم ﺑﻮده اﺳﺖ‪ .‬ﺗﻼش ﺑﺮاي ﺟﺪاﺳﺎزي ﺑﺎﻛﺘﺮي در ﺣﻴﻮان آزﻣﺎﻳﺸﮕﺎﻫﻲ ﻧﺎﻣﻮﻓﻖ ﺑﻮد‪ .‬ﻋﻔﻮﻧﺖ ﺑﺎ اﺳﺘﻔﺎده از‬
‫آﻧﺘﻲ ﺑﻴﻮﺗﻴﻚ درﻣﺎن ﺷﺪه و ﺣﻴﻮان ﺑﻬﺒﻮد ﻳﺎﻓﺖ‪.‬‬

‫واژﮔﺎن ﻛﻠﻴﺪي‪ :‬ﺑﻮرﻟﻴﻮز‪ ،‬ﺑﻴﻤﺎري ﻣﺸﺘﺮك‪ ،‬ﺳﮓ‪ ،‬ﺑﻨﺪﭘﺎﻳﺎن‪ ،‬ﻛﻨﻪ‪ ،‬اﻳﺮان‬

‫‪ #‬آدرس ﻛﻨﻮﻧﻲ‪ :‬ﮔﺮوه ﻋﻠﻮم درﻣﺎﻧﮕﺎﻫﻲ‪ ،‬ﺑﻬﺪاﺷﺖ و ﭘﻴﺸﮕﻴﺮي ﺑﻴﻤﺎرﻳﻬﺎي داﻣﻲ‪ ،‬داﻧﺸﻜﺪه داﻣﭙﺰﺷﻜﻲ داﻧﺸﮕﺎه ﻓﺮدوﺳﻲ ﻣﺸﻬﺪ‪ ،‬ﻣﺸﻬﺪ‪ ،‬اﻳﺮان‬

‫‪Iranian Journal of Veterinary Science and Technology, Vol. 3, No. 2‬‬