Accessible Requires Authentication Published by De Gruyter October 22, 2016

Critical analysis of vector-borne infections in dogs: Babesia vogeli, Babesia gibsoni, Ehrlichia canis and Hepatozoon canis in Punjab, India

Lachhman Das Singla, Deepak Sumbria, Ajay Mandhotra, M.S. Bal and Paramjit Kaur
From the journal Acta Parasitologica

Abstract

There are few published studies on various vector borne diseases of dogs in India and most depict clinical infection in dogs, diagnosed by observation of the haemopathogens in stained blood smears. This study provides the first report regarding molecular confirmation and ancestral relationship analysis of blood smears positive cases of assorted haemopathogens in Punjab province of India. On blood smear examination, haemopathogens were observed in 124 out of 778 (15.95%, 95% CI: 13.53– 18.68) blood smears. Further polymerase chain reactions (PCR) was used on bloods smear positive cases to validate the results. Out of 778 blood samples, Babesia gibsoni was most common parasite infecting dogs (15.04%, 95% CI: 12.7–17.72), followed by Ehrlichia canis (0.39%, 95% CI: 0.0–1.13), infection of Babesia vogeli and Hepatozoon canis was same (0.26%, 95% CI: 0.0–0.9). Among various risk factors studied (age, sex, season), prevalence of infection was non-significantly higher in 1–2 year of age group (19.88%, 95% CI: 14.45–26.71), regarding sex same prevalence was recorded (15.94%), and chances of infection was highest in pre-monsoon i.e. summer (18.26%, 95% CI: 14.49–22.76). Phylogenetic analysis revealed ancestral background of Ludhiana isolates of B. vogeli, B. gibsoni, H. canis, and E. canis with the isolates of Philippines, Mongolia and Tunisia.

Care of Animal

Complete care and measures were taken to avoid any acci-dental injury to the canines while collecting the blood sam-ples. Prior consent was taken from the owners of the canines.

Conflict of interests

  1. All authors are having no conflict of interest.

Acknowledgements

Thanks are due to the Dean, College of Veterinary Science and Director of Research, Guru Angad Dev Veterinary and Animal Sciences University for providing facilities and financial support to carry out the research work. We are very grateful to Dr C. S. Mukhopadhyay (Assistant Scientist-Senior Scale, School of Animal Biotechnology, Guru Angad Dev Veterinary and Animal Sci-ences University, Ludhiana, Punjab-141004; India) for constructing phylogenetic tree in Mega 6.

References

Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. 1990. Basic local alignment search tool. Journal of Molecular Biol-ogy, 215, 403–410. 10.1006/jmbi.1990.9999 Search in Google Scholar

Armstrong P.M., Katavolos P., Caporale D.A., Smith R.P., Spielman A., Telford S.R. 3rd. 1998. Diversity of Babesia infecting deer ticks (Ixodes dammini). American Journal of Tropical Medicine and Hygiene, 58, 739–742 Search in Google Scholar

Avizeh R., Mosallanejad B., Jalali R.M.H., Alborzi A.R. 2010. Sero-prevalence of Ehrlichia canis in dogs referred to Veterinary Hospital of Shahid Chamran University of Ahvaz, Iran. Archives of Razi Institute, 65, 21–26 Search in Google Scholar

Azevedo S.S., Aguiar D.M., Aquino S.F., Orlandelli R.C., Fernan-des A.R.F., Uchoa I.C.P. 2011. Seroprevalence and risk factors associated to Ehrlichia canis in dogs from the semiarid of Paraíba State, Northeastern Brazil. Brazilian Journal of Veterinary Research and Animal Science, 48, 14–18 Search in Google Scholar

Baneth G., Barta J.R., Shkap V., Martin D.S., Macintire D.K., Vin-cent-Johnson N. 2000. Genetic and antigenic evidence supports the separation of Hepatozoon canis and Hepatozoon americanum at the species level. Journal of Clinical Microbiology, 38, 1298–1301 Search in Google Scholar

Baneth G., Bourdeau P., Bourdoiseau G., Bowman D., Breitschwerdt E., Capelli G., Cardoso L., Dantas-Torres F., Day M., Dedet J.P., Dobler G., Ferrer L., Irwin P., Kempf V., Kohn B., Lappin M., Little S., Maggi R., Miró G., Naucke T., Oliva G., Otranto D., Penzhorn B., Pfeffer M., Roura X., Sainz A., Shaw S., Shin S., Solano-Gallego L., Straubinger R., Traub R., Trees A., Truyen U., Demonceau T., Fitzgerald R., Gatti D., Hostetler J., Kilmer B., Krieger K., Mencke N., Mendão C., Mottier L., Pachnicke S., Rees B., Siebert S., Stanneck D., Mingote M.T., von Simson C., Weston S., CVBD World Forum. 2012. Vector-borne diseases-constant challenge for practicing veterinarians: recommendations from the CVBD World Forum. Parasite and Vectors, 5, 55. 10.1186/1756-3305-5-55 Search in Google Scholar

Baneth G., Samish M., Shkap V. 2007. Life cycle of Hepatozoon canis (Apicomplexa: Adeleorina: Hepatozoidae) in the tick Rhipicephalus sanguineus and domestic dog (Canis familiaris). Journal of Parasitology, 93, 283–299. 10.1645/GE-494R.1 Search in Google Scholar

Baneth G., Shkap V. 2003. Monozoic cysts of Hepatozoon canis. Journal of Parasitology, 89, 379–381. 10.1645/00223395(2003)089[0379:MCOHC]2.0.CO;2 Search in Google Scholar

Baneth G., Shkap V., Presentey B.Z., Pipano E. 1996. Hepatozoon canis: the prevalence of antibodies and gametocytes in dogs in Israel. Veterinary Research Communications, 20, 41–46. DOI: 10.1007/BF00346576 Search in Google Scholar

Baneth G., Weigler B. 1997. Retrospective case-control study of hepatozoonosis in dogs in Israel. Journal of Veterinary Internal Medicine, 11, 365–370. 10.1111/j.1939-1676.1997.tb00482.x Search in Google Scholar

Cardoso L., Costa A., Tuna J., Vieira L., Eyal O., Yisaschar-Mekuzas Y., Baneth G. 2008. Babesia canis canis and Babesia canis vogeli infections in dogs from northern Portugal. Veterinary Parasitology, 156, 199–204. 10.1016/j.vetpar.2008.05.027 Search in Google Scholar

Chaudhuri S., Varshney J.P. 2007. Clinical management of babesio-sis in dogs with homeopathic Crotalus horridus 200C. Homeopathy, 96, 90–94. 10.1016/j.homp.2007.02.010 Search in Google Scholar

Chhabra S., Uppal S.K., Singla L.D. 2013. Retrospective study of clinical and hematological aspects associated with dogs naturally infected by Hepatozoon canis in Ludhiana, Punjab, India. Asian Pacific Journal of Tropical Biomedicine, 3, 483–486. 10.1016/S2221-1691(13)60100-8 Search in Google Scholar

Coles E.H. 1986. Veterinary Clinical Pathology, 4th edition. W.B. Saunders Co. Philadelphia Search in Google Scholar

Dantas-Torres F., Latrofa M.S., Weigl S., Tarallo V.D., Lia R.P., Otranto D. 2011. Hepatozoon canis infection in ticks during spring and summer in Italy. Parasitology Research, 10.1007/s00436-011-2544-8 Search in Google Scholar

Eljadar M.S.M., Singla L.D., Mustafa R.A.A., Uppal S.K. 2012. Morphometric variations in gametocytes of Hepatozoon canis from naturally infected dogs. Journal of Parasitic Diseases, 10.1007/s12639-012-0149-5 Search in Google Scholar

Ezeokoli C.D., Ogunkoya A.B., Abdullahi R., Tekdek L.B., Sannusi A., Ilemobade A.A. 1983. Clinical and epidemiological studies on canine hepatozoonosis in Zaria, Nigeria. Journal of Small Animal Practice, 24, 445–460. 10.1111/j.17485827.1983.tb00385.x Search in Google Scholar

Foldvari G., Hell E., Farkas R. 2005. Babesia canis canis in dogs from Hungary: detection by PCR and sequencing. Veterinary Parasitology, 127, 221–226. 10.1016/j.vetpar.2004.10.016 Search in Google Scholar

Gill H.S., Gill B.S. 1977. Qualitative district-wise distribution of adult ixodid ticks in the Punjab state. Ixodid ticks of Domestic Animals in the Punjab State. PAU, Ludhiana, pp. 2–14 Search in Google Scholar

Gupta M.P., Nauriyal D.C., Juyal .P.D., Kalra I.S., Khahra S.S., Mohan R. 1994. Therapeutic trials of Hepatozoon canis infection in dogs. Indian Veterinary Journal, 71, 1221–1221 Search in Google Scholar

Imre M., Farkas R., Ilie M.S., Imre K., Darabus G. 2013. Survey of babesiosis in symptomatic dogs from Romania: Occurrence of Babesia gibsoni associated with breed. Ticks and Tick-borne Diseases, 4, 500–502. 10.1016/j.ttbdis.2013.06.006 Search in Google Scholar

Inokuma H., Yoshizaki Y., Matsumoto K., Okuda M., Onishi T., Nakagome K., Kosugi R., Hirakawa M. 2004. Molecular survey of Babesia infection in dogs in Okinawa, Japan. Veterinary Parasitology, 121, 341–346. 10.1016/j.ttbdis Search in Google Scholar

Inokuma H., Okuda M., Ohno K., Shimoda K., Onishi T. 2002. Analysis of the 18S rRNA gene sequence of a Hepatozoon detected in two Japanese dogs. Veterinary Parasitology, 106, 265–271. 10.1016/S0304-4017(02)00065-1 Search in Google Scholar

Juyal P.D., Kalra I.S., Singla L.D. 1994. Prevalence of haemoproto-zoans in domestic animals in Punjab. 6th National congress of Veterinary Parasitology Search in Google Scholar

Karagenc T.I., Pasa S., Kirli G., Hosgor M., Bilgic H.B., Ozon Y.H., Atasoy A., Eren H. 2006. A parasitological, molecular and serological survey of Hepatozoon canis infection in dogs around the Aegean coast of Turkey. Veterinary Parasitology, 135, 113–119. 10.1016/j.vetpar.2005.08.007 Search in Google Scholar

Kawamoto F., Miyake H., Kaneko O., Kimura M., Dung N.T., Liu Q., Zhou M., Dao L.D., Kawai S., Isomura S., Wataya Y. 1996. Sequence Variation in the 18S rRNA Gene, a Target for PCR Based Malaria Diagnosis, in Plasmodium ovale from Southern Vietnam. Journal of Clinical Microbiology, 34, 2287 Search in Google Scholar

Kim C., Blanco L.B.C., Alhassan A., Iseki H., Yokoyama N., Xuan X., Igarashi I. 2008. Diagnostic real-time PCR assay for the quantitative detection of Theileria equi from equine blood samples. Veterinary Parasitology, 151, 158–163 Search in Google Scholar

Kumar P., Kumar V., Gopal H., Sharma H., Wadhawan V.M. 2015. Prevalence of Canine Babesiosis in and around Jalandhar (Punjab), India. Veterinary Clinical Science, 3, 1–3 Search in Google Scholar

Kundu K., Kumar S., Maurya P.S., Mandal M., Ram H., Garg R., Pawde A.M., Raina O.K., Banerjee P.S. 2012. PCR based identification of Babesia canis vogeli in clinically affected dogs. Journal of Veterinary Parasitology, 26, 167–169 Search in Google Scholar

Lorusso V., Dantas-Torres F., Lia R.P., Tarallo V.D., Mencke N., Capelli G., Otranto D. 2010. Seasonal dynamics of the brown dog tick, Rhipicephalus sanguineus, on a confined dog population in Italy. Medical and Veterinary Entomology, 24, 309–315. 10.1111/j.1365-2915.2010.00885.x Search in Google Scholar

Milanjeet, Singh H., Singh N.K., Singh N.D., Singh C., Rath S.S. 2014. Molecular prevalence and risk factors for the occurrence of canine monocytic ehrlichiosis Veterinarni Medicina, 59, 129–136 Search in Google Scholar

Murphy G.L., Ewing S.A., Whitworth L.C., Fox J.C., Kocan A.A. 1998. A molecular and serologic survey of Ehrlichia canis, E. chaifeensis and E. ewingii in dogs and ticks from Oklahoma. Veterinary Parasitology, 79, 325–339. DOI:10.5433/16790359.2012v33n3p1123 Search in Google Scholar

O’Dwyer L.H., Massard C.L., de Souza J.C.P. 2001. Hepatozoon canis infection associated with dog ticks of rural areas of Rio de Janeiro State, Brazil. Veterinary Parasitology, 94, 143– 150. DOI: 10.1016/S0304-4017(00)00378-2 Search in Google Scholar

Otranto D., Dantas-Torres F. 2010. Canine and feline vector-borne diseases in Italy: current situation and perspectives. Parasite and Vectors, 3, 2. 10.1186/1756-3305-3-2 Search in Google Scholar

Otranto D., Dantas-Torres F., Breitschwerdt E.B. 2009. Managing canine vector-borne diseases of zoonotic concern: part one. Trends in Parasitology, 25, 157–163. 10.1016/j.pt.2009.01.003 Search in Google Scholar

Singh A., Singh H., Singh N.K., Singh N.D., Rath S.S. 2014. Canine Babesiosis in Northwestern India: Molecular Detection and Assessment of Risk Factors. BioMed Research International, 5. org/10.1155/2014/741785 Search in Google Scholar

Singla L.D., Singh H., Kaur P., Singh N.D., Singh N.K., Juyal P.D. 2011. Serodetection of Ehrlichia canis infection in dogs from Ludhiana district of Punjab, India. Journal of Parasitic Diseases, 35, 195–198. 10.1007/s12639-011-0055-2 Search in Google Scholar

Soulsby E.J.L. (Ed.) 1982. Helminths, Arthropods and Protozoa of Domesticated Animals. 7th edn. Bailliere-Tindall, London, UK Search in Google Scholar

Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729 Search in Google Scholar

Tanikawa A., Labruna M.B., Costa A., Aguiar D.M., Justiniano S.V., Mendes R.S., Melo A.L.T., Alves C.J., Azevedo S.S. 2013. Ehrlichia canis in dogs in a semiarid region of Northeastern Brazil: Serology, molecular detection and associated factors. Research in Veterinary Science, 94, 474–477. 10.1016/j.rvsc.2012.10.007 Search in Google Scholar

Thrusfield M. (Ed.) 2007. Veterinary Epidemiology, 3rd Edn, Wiley-Blackwell. pp. 243 Search in Google Scholar

Vipan K., Parvinder K., Charanjeet S., Heigo P., Gagandeep B., Han-ish S., Wadhawan V.M. 2015. Prevalence of Canine Babesiosis in Jalandhar District, Punjab, India. Research Journal of Animal, Veterinary and Fishery Sciences, 3, 6–8 Search in Google Scholar

Yabsley M.J., McKibben J., Macpherson C.N., Cattan P.F., Cherry N.A., Hegarty B.C., Breitschwerdt E.B., O’Connor T., Chandrashekar R., Paterson T., Perea M.L., Ball C., Friesen S., Goedde J., Henderson B., Sylvester W. 2008. Prevalence of Ehrlichia canis, Anaplasma platys, Babesia canis vogeli, Hepatozoon canis, Bartonella vinsonii berkhoffii and Rickettsia spp. in dogs from Grenada. Veterinary Parasitology, 151, 279–85. 10.1016/j.vetpar.2007.11.008 Search in Google Scholar

Received: 2015-7-28
Revised: 2016-4-11
Accepted: 2016-5-13
Published Online: 2016-10-22
Published in Print: 2016-12-1

© 2016 W. Stefański Institute of Parasitology, PAS