Abstract
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.
Similar content being viewed by others
References
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. DOI: 10.1186/1756-3305-4-141
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. DOI: 10.1007/s00436-013-3403-6
Aktas M. 2014. A survey of ixodid tick species and molecular identification of tick-borne pathogens. Veterinary Parasitology, 200, 276–283. DOI: 10.1016/j.vetpar. 2013.12.008
Aktas M., Özübek S., Altay K.,İ., Utuk AE., Kırbas A., Şimsek S., Dumanlı N. 2015a. A molecular and parasitological survey of Hepatozoon canis in domestic dogs in Turkey. Veterinary Parasitology, 209, 264–267. DOI: 10.1016/j.vetpar.2015.02.015
Aktas M., Özübek S., Altay K., Ipek N.D., Balkaya İ., Utuk A.E., Kırbas A., Şimsek S., Dumanlı N. 2015b. Molecular detection of tick-borne rickettsial and protozoan pathogens in domestic dogs from Turkey. Parasites & Vectors, 14, 8, 157. DOI: 10.1186/s13071-015-0763-z
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. DOI: 10.1016/j.ttbdis.2015.03.004
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, Turkey
Aysul N., Ural K., Ulutas B., Eren H., Karagenc T. 2013. First detection and molecular identification of Babesia gibsoni in two dogs from the Aydın Province of Turkey. Turkish Journal of Veterinary & Animal Sciences, 37, 226–229
Baneth G. 2011. Perspectives on canine and feline hepatozoonosis. Veterinary Parasitology, 181, 3–11. DOI: 10.1016/j.vetpar.2011.04.015.
Boozer A.L., Macintire D.K. 2003. Canine babesiosis. Veterinary Clinics of North America: Small Animal Practice, 33, 885–904.
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. DOI: 10.1515/ap-2016-0022
Colwell D.D., Dantas-Torres F., Otranto, D. 2011. Vector-borne parasitic zoonoses: emerging scenarios and new perspectives. Veterinary Parasitology, 182, 14–21. DOI: 10.1016/j.vetpar.2011.07.012
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. DOI: 10.1016/j.cimid.2012.06.004.
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. DOI: 10.1186/s12917-015-0601-8
Cook S., Swann J.W. 2016. Canine babesiosis: autochthonous today, endemic tomorrow? The Veterinary Record, 178, 417–419. DOI: 10.1136/vr.i2168
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, 307–317
Dantas-Torres F. 2008a. Canine vector-borne diseases in Brazil. Parasites & Vectors, 1, 25. DOI: 10.1186/1756-3305-1-25
Dantas-Torres F. 2008b. The brown dog tick, Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae): from taxonomy to control. Veterinary Parasitology, 152, 173–185. DOI: 10.1016/j.vetpar.2007.12.030
Dantas-Torres F., Figueredo L.A. 2006. Canine babesiosis: a Brazilian perspective. Veterinary Parasitology, 141, 197–203
Dantas-Torres F., Otranto D. 2016. Best Practices for Preventing Vector-Borne Diseases in Dogs and Humans. Trends in Parasitology, 32, 43–55. DOI: 10.1016/j.pt.2015.09.004.
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. DOI: 10.2353/jmoldx.2008.070063
Gökçe E., Kırmızıgül A.H., Taşcı 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, 717–720
Gulanber A., Gorenflot A., Schetters T.P., Carcy B. 2006. First molecular diagnosis of Babesia vogeli in domestic dogs from Turkey. Veterinary Parasitology, 139, 224–230
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. DOI: 10.1111/avj.12293
Hornok S., Tánczos B., Fernández de Mera I.G., de la Fuente J., Hofmann-Lehmann R., Farkas R., 2013. High prevalence of Hepatozooninfection among shepherd dogs in a region considered to be free of Rhipicephalus sanguineus. Veterinary Parasitology, 196, 189–193. DOI: 10.1016/j.vetpar.2013.02.009
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, 3031–3039
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, 1132–1136
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, 265–271
Irwin P.J. 2009. Canine babesiosis: from molecular taxonomy to control. Parasites & Vectors, 2, S4. DOI: 10.1186/1756-3305-2-S1-S4
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, 5397–5399
Koc S., Aydın L., Cetin H. 2015. Tick species (Acari: Ixodida) in Antalya City, Turkey: species diversity and seasonal activity. Parasitology Research, 114, 2581–2586. DOI: 10.1007/s00436-015-4462-7
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, 2631–2638
Little S.E., Allen K.E., Johnson E.M., Panciera R.J., Reichard M.V., Ewing S.A. 2009. New developments in canine hepato-zoonosis in North America: a review. Parasites & Vectors, 2 (Suppl. 1), S5. DOI: 10.1186/1756-3305-2-S1-S5
Liu M., Ruttayaporn N., Saechan V., Jirapattharasate C., Vudriko P., Moumouni P.F., et al. 2016. Molecular survey of canine vectorborne diseases in stray dogs in Thailand. Parasitology International, 65, 357–361. DOI: 10.1016/j.parint.2016.04.011
Lobetti R.G. 1998. Hyperreninaemic hypoaldosteronism in a dog. Journal of the South African Veterinary Association, 69, 33–35
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
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, 1453–1465
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. DOI: 10.1155/2014/549858
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. DOI: 10.1016/j.vetmic.2009.09.069
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. DOI: 10.1080/03079450802412590
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, 1103–1109
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. DOI: 10.1016/j.pt.2009.02.005
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. DOI: 10.1007/s00436-015-4513-0
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, 81–85
Sayın Z., Sakmanoğlu 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, 1–6
Seneviratna P., Weerasinghe Ariyadasa S. 1973. Transmission of Haemobartonella canis by the dog tick, Rhipicephalus sanguineus. Research in Veterinary Science, 14, 112–114
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. DOI: 10.1515/ap-2016-0098
Uilenberg G. 2006. Babesia–a historical overview. Veterinary Parasitology, 138, 3–10
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. DOI: 10.1016/j.cimid.2014.08.001
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. DOI: 10.1016/j.ijpara.2009.02.007
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. DOI: 10.1515/ap-2015-0003
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, 132–141
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Guo, H., Sevinc, F., Ceylan, O. et al. A PCR survey of vector-borne pathogens in different dog populations from Turkey. Acta Parasit. 62, 533–540 (2017). https://doi.org/10.1515/ap-2017-0064
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1515/ap-2017-0064