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.
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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.1990.9999
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
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, 21–26
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, 14–18
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, 1298–1301
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: 10.1186/1756-3305-5-55
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.1
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;2
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
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.x
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.2008.05.027
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.2007.02.010
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)60100-8
Coles E.H. 1986. Veterinary Clinical Pathology, 4th edition. W.B. Saunders Co. Philadelphia.
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.
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/s12639-012-0149-5
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.x
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.2004.10.016
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
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
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.2013.06.006
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.ttbdis
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)00065-1
Juyal P.D., Kalra I.S., Singla L.D. 1994. Prevalence of haemoprotozoans in domestic animals in Punjab. 6th National congress of Veterinary Parasitology
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.2005.08.007
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
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
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.
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
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.x
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
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:10.5433/1679-0359.2012v33n3p1123
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
Otranto D., Dantas-Torres F. 2010. Canine and feline vector-borne diseases in Italy: current situation and perspectives. Parasite and Vectors, 3, 2. DOI: 10.1186/1756-3305-3-2
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.2009.01.003
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/10.1155/2014/741785
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/s12639-011-0055-2
Soulsby E.J.L. (Ed.) 1982. Helminths, Arthropods and Protozoa of Domesticated Animals. 7th edn. Bailliere-Tindall, London, UK
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
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.2012.10.007
Thrusfield M. (Ed.) 2007. Veterinary Epidemiology, 3rd Edn, Wiley-Blackwell. pp. 243
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, 6–8
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.2007.11.008
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Singla, L.D., Sumbria, D., Mandhotra, A. et al. Critical analysis of vector-borne infections in dogs: Babesia vogeli, Babesia gibsoni, Ehrlichia canis and Hepatozoon canis in Punjab, India. Acta Parasit. 61, 697–706 (2016). https://doi.org/10.1515/ap-2016-0098
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DOI: https://doi.org/10.1515/ap-2016-0098