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Acta Parasitologica

, Volume 61, Issue 4, pp 697–706 | Cite as

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

  • Lachhman Das SinglaEmail author
  • Deepak Sumbria
  • Ajay Mandhotra
  • M. S. Bal
  • Paramjit Kaur
Article

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.

Keywords

Babesia gibsoni Babesia vogeli Hepatozoon canis Ehrlichia canis Polymerase chain reaction Phylogenetic analysis 

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References

  1. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. 1990. Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410. DOI: 10.1006/jmbi.1990.9999CrossRefGoogle Scholar
  2. 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, 739–742CrossRefGoogle Scholar
  3. Avizeh R., Mosallanejad B., Jalali R.M.H., Alborzi A.R. 2010. Seroprevalence of Ehrlichia canis in dogs referred to Veterinary Hospital of Shahid Chamran University of Ahvaz, Iran. Archives of Razi Institute, 65, 21–26Google Scholar
  4. Azevedo S.S., Aguiar D.M., Aquino S.F., Orlandelli R.C., Fernandes 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, 14–18CrossRefGoogle Scholar
  5. Baneth G., Barta J.R., Shkap V., Martin D.S., Macintire D.K., Vincent-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, 1298–1301PubMedPubMedCentralGoogle Scholar
  6. 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., Mendao C., Mottier L., Pachnicke S., Rees B., Siebert S., Stanneck D., Mingote M.T., von Simson C., Weston S., CVBD World Forum. 2012. Vectorborne diseases-constant challenge for practicing veterinarians: recommendations from the CVBD World Forum. Parasite and Vectors, 5, 55. DOI: 10.1186/1756-3305-5-55CrossRefGoogle Scholar
  7. 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. DOI: 10.1645/GE-494R.1CrossRefGoogle Scholar
  8. Baneth G., Shkap V. 2003. Monozoic cysts of Hepatozoon canis. Journal of Parasitology, 89, 379–381. DOI: 10.1645/0022-3395(2003)089[0379:MCOHC]2.0.CO;2CrossRefGoogle Scholar
  9. 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/BF00346576CrossRefGoogle Scholar
  10. Baneth G., Weigler B. 1997. Retrospective case-control study of hepatozoonosis in dogs in Israel. Journal of Veterinary Internal Medicine, 11, 365–370. DOI: 10.1111/j.1939-1676.1997.tb00482.xCrossRefGoogle Scholar
  11. 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. DOI: 10.1016/j.vetpar.2008.05.027CrossRefGoogle Scholar
  12. Chaudhuri S., Varshney J.P. 2007. Clinical management of babesiosis in dogs with homeopathic Crotalus horridus 200C. Homeopathy, 96, 90–94. DOI: 10.1016/j.homp.2007.02.010CrossRefGoogle Scholar
  13. 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. DOI: 10.1016/S2221-1691(13)60100-8CrossRefGoogle Scholar
  14. Coles E.H. 1986. Veterinary Clinical Pathology, 4th edition. W.B. Saunders Co. Philadelphia.Google Scholar
  15. 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, DOI: 10.1007/s00436-011-2544-8.Google Scholar
  16. 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, DOI: 10.1007/s12639-012-0149-5Google Scholar
  17. 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. DOI: 10.1111/j.1748-5827.1983.tb00385.xCrossRefGoogle Scholar
  18. Foldvari G., Hell E., Farkas R. 2005. Babesia canis canis in dogs from Hungary: detection by PCR and sequencing. Veterinary Parasitology, 127, 221–226. DOI: 10.1016/j.vetpar.2004.10.016CrossRefGoogle Scholar
  19. 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. 2–14Google Scholar
  20. 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, 1221–1221Google Scholar
  21. 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. DOI: 10.1016/j.ttbdis.2013.06.006CrossRefGoogle Scholar
  22. 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. DOI: 10.1016/j.ttbdisCrossRefGoogle Scholar
  23. 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. DOI: 10.1016/S0304-4017(02)00065-1CrossRefGoogle Scholar
  24. Juyal P.D., Kalra I.S., Singla L.D. 1994. Prevalence of haemoprotozoans in domestic animals in Punjab. 6th National congress of Veterinary ParasitologyGoogle Scholar
  25. 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. DOI: 10.1016/j.vetpar.2005.08.007CrossRefGoogle Scholar
  26. 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, 2287PubMedPubMedCentralGoogle Scholar
  27. 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, 158–163CrossRefGoogle Scholar
  28. 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.Google Scholar
  29. 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, 167–169Google Scholar
  30. 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. DOI: 10.1111/j.1365-2915.2010.00885.xPubMedPubMedCentralGoogle Scholar
  31. 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, 129–136CrossRefGoogle Scholar
  32. 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:10.5433/1679-0359.2012v33n3p1123CrossRefGoogle Scholar
  33. 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)00378-2CrossRefGoogle Scholar
  34. Otranto D., Dantas-Torres F. 2010. Canine and feline vector-borne diseases in Italy: current situation and perspectives. Parasite and Vectors, 3, 2. DOI: 10.1186/1756-3305-3-2CrossRefGoogle Scholar
  35. 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. DOI: 10.1016/j.pt.2009.01.003CrossRefGoogle Scholar
  36. 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. BioMedResearch International, 5. DOI: org/10.1155/2014/741785Google Scholar
  37. 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. DOI: 10.1007/s12639-011-0055-2CrossRefGoogle Scholar
  38. Soulsby E.J.L. (Ed.) 1982. Helminths, Arthropods and Protozoa of Domesticated Animals. 7th edn. Bailliere-Tindall, London, UKGoogle Scholar
  39. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729CrossRefGoogle Scholar
  40. 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. DOI: 10.1016/j.rvsc.2012.10.007CrossRefGoogle Scholar
  41. Thrusfield M. (Ed.) 2007. Veterinary Epidemiology, 3rd Edn, Wiley-Blackwell. pp. 243Google Scholar
  42. Vipan K., Parvinder K., Charanjeet S., Heigo P., Gagandeep B., Hanish S., Wadhawan V.M. 2015. Prevalence of Canine Babesiosis in Jalandhar District, Punjab, India. Research Journal of Animal, Veterinary and Fishery Sciences, 3, 6–8Google Scholar
  43. 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, Anaplasmaplatys, Babesia canis vogeli, Hepatozoon canis, Bartonella vinsonii berkhoffii and Rickettsia spp. in dogs from Grenada. Veterinary Parasitology, 151, 279–85. DOI: 10.1016/j.vetpar.2007.11.008CrossRefGoogle Scholar

Copyright information

© Witold Stefański Institute of Parasitology, Polish Academy of Sciences 2016

Authors and Affiliations

  • Lachhman Das Singla
    • 1
    Email author
  • Deepak Sumbria
    • 1
  • Ajay Mandhotra
    • 1
  • M. S. Bal
    • 1
  • Paramjit Kaur
    • 1
  1. 1.Department of Veterinary ParasitologyCollege of Veterinary Sciences, Guru Angad Dev Veterinary and Animal Sciences UniversityLudhianaIndia

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