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Licensed Unlicensed Requires Authentication Published by De Gruyter July 5, 2017

A PCR survey of vector-borne pathogens in different dog populations from Turkey

Huanping Guo, Ferda Sevinc, Onur Ceylan, Mutlu Sevinc, Ege Ince, Yang Gao, Paul Franck Adjou Moumouni, Mingming Liu, Artemis Efstratiou, Guanbo Wang, Shinuo Cao, Mo Zhou, Charoonluk Jirapattharasate, Aaron Edmond Ringo, Weiqing Zheng and Xuenan Xuan
From the journal Acta Parasitologica


In the present study, a total of 192 blood samples were collected from pet dogs, kennel dogs and shepherd dogs in Konya district, Turkey, and tested by specific PCR for the presence of vector-borne pathogens. Several pathogens were identified, most of which can cause substantial morbidity in dogs. PCR results revealed that 54 (28.1%) dogs were infected with one or more pathogens. Positive results were obtained for Babesia spp. in 4 dogs (2.1%), Hepatozoon spp. in 8 dogs (4.2%) and Mycoplasma spp. in 46 dogs (24%). Three dogs (1.6%) were infected with two or three pathogens. The sequence analysis of the positive DNA samples revealed the presence of Babesia canis vogeli, Hepatozoon canis, Hepatozoon sp. MF, Mycoplasma haemocanis and Candidatus Mycoplasma haematoparvum. Ehrlichia canis and Anaplasma platys were not detected. Regardless of ownership status, vector-borne diseases were common in these dog populations. There was significant difference of pathogen prevalence among the different dog populations. Mycoplasma spp. was more frequent in the kennel dogs (31.9%) than in the pet (21.4%) and shepherd dogs (13.8%). Additionally, the frequency of Babesia spp. and Hepatozoon spp. was higher in the shepherd dogs which account for three quarters and half of the total number of Babesia spp. and Hepatozoon spp., respectively. To our knowledge, this is the first report of Mycoplasma infection in dogs in Turkey. The results of the present study provide a foundation for understanding the epidemiology of canine vector-borne diseases (CVBDs), and for strategies to control these diseases in Turkey.


This study was supported by a Grant-in-Aid for Scientific Research, from the Ministry of Education, Culture, Sports, Science, and Technology (MEXT) (26304036) of Japan and The Scientific and Technological Research Council of Turkey (TUBITAK, 113O336).


Abd Rani P.A., Irwin P.J., Coleman G.T., Gatne M., Traub R.J. 2011. A survey of canine tick-borne diseases in India. Parasites & Vectors, 4, 141. 10.1186/1756-3305-4-141Search in Google Scholar

Aktas M., Ozübek S., Ipek D.N. 2013. Molecular investigations of Hepatozoon species in dogs and developmental stages of Rhipicephalus sanguineus. Parasitology Research, 112, 2381–2385. 10.1007/s00436-013-3403-6Search in Google Scholar

Aktas M. 2014. A survey of ixodid tick species and molecular identification of tick-borne pathogens. Veterinary Parasitology, 200, 276–283. 10.1016/j.vetpar.2013.12.008Search in Google Scholar

Aktas M., Özübek S., Altay K.,İ., Utuk AE., Kirbas A., Şimsek S., Dumanlı N. 2015a. A molecular and parasitological survey of Hepatozoon canis in domestic dogs in Turkey. Veterinary Parasitology, 209, 264–267. 10.1016/j.vetpar.2015.02.015Search in Google Scholar

Aktas M., Özübek S., Altay K., Ipek N.D., Balkaya İ., Utuk A.E., Kirbas A., Şimsek S., Dumanli N. 2015b. Molecular detection of tick-borne rickettsial and protozoan pathogens in domestic dogs from Turkey. Parasites & Vectors, 14, 8, 157. 10.1186/s13071-015-0763-zSearch in Google Scholar

Aydin M.F., Sevinc F., Sevinc M. 2015. Molecular detection and characterization of Hepatozoon spp. in dogs from the central part of Turkey. Ticks and Tick-Borne Diseases, 6, 388–392.10.1016/j.ttbdis.2015.03.004Search in Google Scholar

Aysul N. 2006. Comparison of microscopic and PCR-RLB findings in detection of Babesia species of dogs in Istanbul. PhD Thesis, Istanbul University, Institute of Health Science, Parasitology Department, Istanbul, TurkeySearch in Google Scholar

Aysul N., Ural K., Ulutas B., Eren H., Karagenc T. 2013. First detection and molecular identification of Babesia gibsoni in two dogs from the Aydin Province of Turkey. Turkish Journal of Veterinary & Animal Sciences, 37, 226–229Search in Google Scholar

Baneth G. 2011. Perspectives on canine and feline hepatozoonosis. Veterinary Parasitology, 181, 3–11. 10.1016/j.vetpar.2011.04.015.Search in Google Scholar

Boozer A.L., Macintire D.K. 2003. Canine babesiosis. Veterinary Clinics of North America: Small Animal Practice, 33, 885–904.10.1016/S0195-5616(03)00039-1Search in Google Scholar

Cetinkaya H., Haktanir D., Arun S., Vurusaner C. 2016. Molecular detection and prevalence of feline hemotropic mycoplasmas in Istanbul, Turkey. Acta Parasitologica, 61, 165–171. 10.1515/ap-2016-0022Search in Google Scholar PubMed

Colwell D.D., Dantas-Torres F., Otranto, D. 2011. Vector-borne parasitic zoonoses: emerging scenarios and new perspectives. Veterinary Parasitology, 182, 14–21. 10.1016/j.vetpar.2011.07.012Search in Google Scholar PubMed

Compton S.M., Maggi R.G., Breitschwerdt E.B. 2012. Candidatus Mycoplasma haematoparvum and Mycoplasma haemocanis infections in dogs from the United States. Comparative Immunology, Microbiology and Infectious Diseases, 35, 557–562. 10.1016/j.cimid.2012.06.004.Search in Google Scholar

Conrado Fde O., do Nascimento N.C., dos Santos A.P., Zimpel C.K., Messick J.B., Biondo, A.W. 2015. Occurrence and identification of hemotropic mycoplasmas (Hemoplasmas) in free ranging and laboratory rats (Rattus norvegicus) from two Brazilian zoos. BMC Veterinary Research, 11, 286. 10.1186/s12917-015-0601-8Search in Google Scholar

Cook S., Swann J.W. 2016. Canine babesiosis: autochthonous today, endemic tomorrow? The Veterinary Record, 178, 417–419. 10.1136/vr.i2168Search in Google Scholar

Criado-Fornelio A., Martinez-Marcos A., Buling-Saraña A., Barba- Carretero J.C. 2003. Presence of Mycoplasma haemofelis, Mycoplasma haemominutum and piroplasmids in cats from southern Europe: a molecular study. Veterinary Microbiology, 93, 307–31710.1016/S0378-1135(03)00044-0Search in Google Scholar

Dantas-Torres F. 2008a. Canine vector-borne diseases in Brazil. Parasites & Vectors, 1, 25. 10.1186/1756-3305-1-25Search in Google Scholar PubMed PubMed Central

Dantas-Torres F. 2008b. The brown dog tick, Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae): from taxonomy to control. Veterinary Parasitology, 152, 173–185. 10.1016/j.vetpar.2007.12.030Search in Google Scholar PubMed

Dantas-Torres F., Figueredo L.A. 2006. Canine babesiosis: a Brazilian perspective. Veterinary Parasitology, 141, 197–20310.1016/j.vetpar.2006.07.030Search in Google Scholar PubMed

Dantas-Torres F., Otranto D. 2016. Best Practices for Preventing Vector-Borne Diseases in Dogs and Humans. Trends in Parasitology, 32, 43–55. 10.1016/ in Google Scholar PubMed

Dong J., Olano J.P., McBride J.W., Walker D.H. 2008. Emerging pathogens: challenges and successes of molecular diagnostics. The Journal of Molecular Diagnostics, 10, 185–197. 10.2353/jmoldx.2008.070063Search in Google Scholar PubMed PubMed Central

Gökçe E., Kirmizigül A.H., Taşci G.T., Uzlu E., Gündüz N., Vatansever Z. 2013. The first time clinical and parasitological determination of Babesia canis in dogs in Turkey. The Journal of the Faculty of Veterinary Medicine, University of Kafkas, 19, 717–720Search in Google Scholar

Gulanber A., Gorenflot A., Schetters T.P., Carcy B. 2006. First molecular diagnosis of Babesia vogeli in domestic dogs from Turkey. Veterinary Parasitology, 139, 224–23010.1016/j.vetpar.2006.02.035Search in Google Scholar PubMed

Hii S.F., Traub R.J., Thompson M.F., Henning J., O’Leary C.A., Burleigh A., et al. 2015. Canine tick-borne pathogens and associated risk factors in dogs presenting with and without clinical signs consistent with tick-borne diseases in northern Australia. Australian Veterinary Journal, 93, 58–66. 10.1111/avj.12293Search in Google Scholar

Hornok S., Tánczos B., Fernández de Mera I.G., de la Fuente J., Hofmann-Lehmann R., Farkas R., 2013. High prevalence of Hepatozoon-infection among shepherd dogs in a region considered to be free of Rhipicephalus sanguineus. Veterinary Parasitology, 196, 189–193. 10.1016/j.vetpar.2013.02.009Search in Google Scholar

Inokuma H., Brouqui P., Drancourt M., Raoult D. 2001. Citrate synthase gene sequence: a new tool for phylogenetic analysis and identification of Ehrlichia. Journal of Clinical Microbiology, 39, 3031–303910.1128/JCM.39.9.3031-3039.2001Search in Google Scholar

Inokuma H., Fujii K., Okuda M., Onishi T., Beaufils J.P., Raoult D., Brouqui P. 2002a. Determination of the nucleotide sequence of heat shock operon groESL and the citrate synthase gene (gltA) of Anaplasma (Ehrlichia) platys for phylogenetic and diagnostic studies. Clinical and Diagnostic Laboratory Immunology, 9, 1132–113610.1128/CDLI.9.5.1132-1136.2002Search in Google Scholar

Inokuma H., Okuda M., Ohno K., Shimoda K., Onishi T. 2002b. Analysis of the 18S rRNA gene sequence of a Hepatozoon detected in two Japanese dogs. Veterinary Parasitology, 106, 265–27110.1016/S0304-4017(02)00065-1Search in Google Scholar

Irwin P.J. 2009. Canine babesiosis: from molecular taxonomy to control. Parasites & Vectors, 2, S4. 10.1186/1756-3305-2-S1-S4Search in Google Scholar PubMed PubMed Central

Kenny M.J., Shaw S.E., Beugnet F., Tasker S. 2004. Demonstration of two distinct hemotropic Mycoplasmas in French dogs. Journal of Clinical Microbiology, 42, 5397–539910.1128/JCM.42.11.5397-5399.2004Search in Google Scholar PubMed PubMed Central

Koc S., Aydin L., Cetin H. 2015. Tick species (Acari: Ixodida) in Antalya City, Turkey: species diversity and seasonal activity. Parasitology Research, 114, 2581–2586. 10.1007/s00436-015-4462-7Search in Google Scholar PubMed

Kordick S.K., Breitschwerdt E.B., Hegarty B.C., Southwick K.L., Colitz C.M., Hancock S.I., Bradley J.M., et al. 1999. Coinfection with multiple tick-borne pathogens in a Walker Hound kennel in North Carolina. Journal of Clinical Microbiology, 37, 2631–263810.1128/JCM.37.8.2631-2638.1999Search in Google Scholar PubMed PubMed Central

Little S.E., Allen K.E., Johnson E.M., Panciera R.J., Reichard M.V., Ewing S.A. 2009. New developments in canine hepatozoonosis in North America: a review. Parasites & Vectors, 2 (Suppl. 1), S5. 10.1186/1756-3305-2-S1-S5Search in Google Scholar PubMed PubMed Central

Liu M., Ruttayaporn N., Saechan V., Jirapattharasate C., Vudriko P., Moumouni P.F., et al. 2016. Molecular survey of canine vector-borne diseases in stray dogs in Thailand. Parasitology International, 65, 357–361. 10.1016/j.parint.2016.04.011Search in Google Scholar PubMed

Lobetti R.G. 1998. Hyperreninaemic hypoaldosteronism in a dog. Journal of the South African Veterinary Association, 69, 33–3510.4102/jsava.v69i1.808Search in Google Scholar PubMed

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.xSearch in Google Scholar PubMed

Messick J.B. 2003. New perspectives about Hemotrophic mycoplasma (formerly, Haemobartonella and Eperythrozoon species) infections in dogs and cats. The Veterinary Clinics of North America. Small Animal, 33, 1453–146510.1016/j.cvsm.2003.08.002Search in Google Scholar PubMed

Metwally M.A., Yassin A.S., Essam T.M., Hamouda H.M., Amin M.A. 2014. Detection, characterization, and molecular typing of human Mycoplasma spp. from major hospitals in Cairo, Egypt. The Scientific World Journal, 2014, 549858. 10.1155/2014/549858Search in Google Scholar PubMed PubMed Central

Novacco M., Meli M.L., Gentilini F., Marsilio F., Ceci C., Pennisi M.G., et al. 2010. Prevalence and geographical distribution of canine hemotropic mycoplasma infection in Mediterranean countries and analysis of risk factors for infection. Veterinary Microbiology, 142, 276–284. 10.1016/j.vetmic.2009.09.069Search in Google Scholar PubMed

Ongor H., Kalin R., Karahan M., Cetinkaya B., McAuliffe L., Nicholas R.A.J. 2008. Isolation of Mycoplasma bovis from broiler chickens in Turkey. Avian Pathology: Journal of The World Veterinary Poultry Association, 37, 587–588. 10.1080/03079450802412590Search in Google Scholar PubMed

Ongor H., Kalin R., Karahan M., Çetinkaya B., Akan M. 2009. Detection of mycoplasma species in turkeys by culture and polymerase chain reaction. Revue Scientifique et Technique (International Office of Epizootics), 28, 3, 1103–110910.20506/rst.28.3.1955Search in Google Scholar PubMed

Otranto D., Dantas-Torres F., Breitschwerdt E.B. 2009. Managing canine vector-borne diseases of zoonotic concern: part two. Trends in Parasitology, 25, 228–235. 10.1016/ in Google Scholar PubMed

Pantchev N., Pluta S., Huisinga E., Nather S., Scheufelen M., Vrhovec M.G., et al. 2015. Tick-borne Diseases (Borreliosis, Anaplasmosis, Babesiosis) in German and Austrian Dogs: Status quo and Review of Distribution, Transmission, Clinical Findings, Diagnostics and Prophylaxis. Parasitology Research, 114, 19–54. 10.1007/s00436-015-4513-0Search in Google Scholar PubMed

Passos L.M., Geiger S.M., Ribeiro M.F., Pfister K., Zahler-Rinder M. 2005. First molecular detection of Babesia vogeli in dogs from Brazil. Veterinary Parasitollgy, 127, 81–8510.1016/j.vetpar.2004.07.028Search in Google Scholar

Sayin Z., Sakmanoglu A., Uçan U.S., Uslu A., Hadimli H.H., Aras Z., et al. 2016. Mycoplasma infections in dairy cattle farms in Turkey. Turkish Jounal of Veterinary and Animal Sciences- Academic Journal, 40, 1–610.3906/vet-1602-82Search in Google Scholar

Seneviratna P., Weerasinghe Ariyadasa S. 1973. Transmission of Haemobartonella canis by the dog tick, Rhipicephalus sanguineus. Research in Veterinary Science, 14, 112–11410.1016/S0034-5288(18)33950-XSearch in Google Scholar

Singla L.D., Sumbria D., Mandhotra A., Bal M.S., Kaur P. 2016. Critical analysis of vector-borne infections in dogs: Babesia vogeli, Babesia gibsoni, Ehrlichia canis and Hepatozoon canis in Punjab, India. Acta Parasitologica, 61, 697–706. 10.1515/ap-2016-0098Search in Google Scholar PubMed

Uilenberg G. 2006. Babesia – a historical overview. Veterinary Parasitology, 138, 3–1010.1016/j.vetpar.2006.01.035Search in Google Scholar PubMed

Valle Sde F., Messick J.B., Dos Santos A.P., Kreutz L.C., Duda N.C., Machado G., et al. 2014. Identification, occurrence and clinical finding of canine hemoplasmas in southern Brazil. Comparative Immunology, Microbiology and Infectious Diseases, 37, 259–265. 10.1016/j.cimid.2014.08.001Search in Google Scholar PubMed

Vojta L., Mrljak V., Curkovic S., Zivicnjak T., Marinculic A., Beck R. 2009. Molecular epizootiology of canine hepatozoonosis in Croatia. International Journal of Parasitology, 39, 1129–1136. 10.1016/j.ijpara.2009.02.007Search in Google Scholar PubMed

Wei L., Kelly P., Ackerson K., El-Mahallawy H.S., Kaltenboeck B., Wang C. 2014. Molecular detection of Dirofilaria immitis, Hepatozoon canis, Babesia spp., Anaplasma platys and Ehrlichia canis in dogs on Costa Rica. Acta Parasitologica, 60, 21–25. 10.1515/ap-2015-0003Search in Google Scholar PubMed

Wengi N., Willi B., Boretti F.S., Cattori V., Riond B., Meli M.L., et al. 2008. Real-time PCR-based prevalence study, infection follow-up and molecular characterization of canine hemotropic mycoplasmas. Veterinary Microbioloy, 126, 132–14110.1016/j.vetmic.2007.06.018Search in Google Scholar PubMed

Received: 2016-9-12
Revised: 2017-2-21
Accepted: 2017-4-5
Published Online: 2017-7-5
Published in Print: 2017-9-26

© 2017 W. Stefański Institute of Parasitology, PAS

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