Abstract
Canine vector-borne diseases (CVBDs) have increasingly become a focus of interest in recent years. Some of the CVBDs are zoonotic and may therefore also represent a risk for the human population. Different factors are in discussion to explain the expansion of vectors and pathogens into formerly unaffected areas. Knowledge of the prevalence and distribution of CVBDs in Bulgaria is scant overall and most data rely on single case descriptions. The aim of the present study was to determine the seroprevalence of important CVBDs in 167 dogs from central-southern Bulgaria (Stara Zagora), with special emphasis on hitherto uninvestigated babesiosis and angiostrongylosis, on poorly investigated Lyme borreliosis and canine granulocytic anaplasmosis, and on the potentially zoonotic dirofilariosis and leishmaniosis. Relatively high prevalence rates were documented for anti-Babesia canis antibodies, Dirofilaria immitis antigen (16.2 %; 27/167 each), anti-Ehrlichia canis (21 %; 35/167) and anti-Anaplasma phagocytophilum antibodies (30.5 – 46.1 %; 51 – 77/167), while Borrelia burgdorferi seroprevalence was low (2.4 %; 4/167). All samples were negative for Leishmania infantum antibodies and Angiostrongylus vasorum antigen and antibodies. In total, 64.7 % (108/167) of the samples indicated infection or exposure to at least one agent and a high proportion of dual infections (39.8 %; 43/108) was demonstrated. Multiple infections with up to four different organisms were also detected. Our data underline the importance of CVBDs and especially of co-infections which could influence the clinical outcome in dogs.
Article PDF
Similar content being viewed by others
References
Baneth G, Koutinas AF, Solano-Gallego L, Bourdeau P, Ferrer L (2008) Canine leishmaniosis – new concepts and insights on an expanding zoonosis: part one. Trends Parasitol 24(7):324–30
Beck R, Vojta L, Mrljak V, Marinculić A, Beck A, Zivicnjak T, Cacciò SM (2009) Diversity of Babesia and Theileria species in symptomatic and asymptomatic dogs in Croatia. Int J Parasitol 39(7):843–8
Beall MJ, Chandrashekar R, Eberts MD, Cyr KE, Diniz PP, Mainville C, Hegarty BC, Crawford JM, Breitschwerdt EB (2008) Serological and molecular prevalence of Borrelia burgdorferi, Anaplasma phagocytophilum, and Ehrlichia species in dogs from Minnesota. Vector Borne Zoonotic Dis 8:455–464
Bland JM (2000) An introduction to medical statistics. 3th edition, Oxford university press, 230
Bowman D, Little SE, Lorentzen L, Shields J, Sullivan MP, Carlin EP (2009) Prevalence and geographic distribution of Dirofilaria immitis, Borrelia burgdorferi, Ehrlichia canis, and Anaplasma phagocytophilum in dogs in the United States: results of a national clinic-based serologic survey. Vet Parasitol 160(1 – 2):138–48
Chandrashekar R, Mainville CA, Beall MJ, O’Connor T, Eberts MD, Alleman AR, Gaunt SD, Breitschwerdt EB (2010) Performance of a commercially available in-clinic ELISA for the detection of antibodies against Anaplasma phagocytophilum, Ehrlichia canis, and Borrelia burgdorferi and Dirofilaria immitis antigen in dogs. Am J Vet Res 71(12):1443–50
Davoust B, Bourry O, Gomez J, Lafay L, Casali F, Leroy E, Parzy D (2006) Surveys on seroprevalence of canine monocytic ehrlichiosis among dogs living in the Ivory Coast and Gabon and evaluation of a quick commercial test kit dot-ELISA. Ann N Y Acad Sci 1078:464–9
Diniz PP, Breitschwerdt EB (2012) Anaplasma phagocytophilum infection (canine granulocytotropic anaplasmosis). In: Infectious diseases of the dog and cat. 4th edition, edited by Greene CE., Elsevier, 244 – 254
Dyachenko V, Pantchev N, Balzer HJ, Meyersen A, Straubinger RK (2012) First case of Anaplasma platys infection in a dog from Croatia. Parasit Vectors 5:49
Garifallou A, Hadziandoniou M, Schnur LF, Yuval B, Warburg A, Jacobson RL, Pateraki E, Patrikoussis M, Schlein Y, Sérié C (1989) Epidemiology of human and canine leishmaniasis on the island of Zakinthos. In: Hart DT (ed) Leishmaniasis. The current status and new strategies for control, vol 163, NATO ASI Series/A, Life Sciences. Plenum Press, New York, pp 1011–1015
Georgieva D, Kirkova Z, Ivanov A (2001) A study on the incidence and diagnosistics of dirofilariosis (heartworm disease) in carnivores. Bulg J Vet Med 4(4):231–236
Gaunt S, Beall M, Stillman B, Lorentzen L, Diniz P, Chandrashekar R, Breitschwerdt E (2010) Experimental infection and co-infection of dogs with Anaplasma platys and Ehrlichia canis: hematologic, serologic and molecular findings. Parasit Vectors 3(1):33
Harizanov R, Rainova I, Tzvetkova N, Kaftandjiev I, Bikov I, Mikov O (2013) Geographical distribution and epidemiological characteristics of visceral leishmaniasis in Bulgaria, 1988 to 2012. Euro Surveill 18(29):20531
Harrus S, Waner T (2011) Diagnosis of canine monocytotropic ehrlichiosis (Ehrlichia canis): an overview. Vet J 187(3):292–6
Harrus S, Waner T, Neer TM (2012) Ehrlichia canis infection. In: Infectious diseases of the dog and cat. 4th edition; edited by Greene CE. Elsevier; 227 – 238
Irwin PJ (2009) Canine babesiosis: from molecular taxonomy to control. Parasit Vectors 2(Suppl 1):S4
Ivanov IN, Mitkova N, Reye AL, Hübschen JM, Vatcheva-Dobrevska RS, Dobreva EG, Kantardjiev TV, Muller CP (2011) Detection of new Francisella-like tick endosymbionts in Hyalomma spp. and Rhipicephalus spp. (Acari: Ixodidae) from Bulgaria. Appl Environ Microbiol 77(15):5562–5
Killick-Kendrick R, Killick-Kendrick M (1999) Biology of sand fly vectors of Mediterranean canine leishmaniasis. Proceedings of the International Canine Leishmaniasis Forum, Barcelona, Spain: 26 – 31
Kirkova Z, Ivanov A, Georgieva D, Prelesov P (2008) An update on dirofilariosis in dogs and wild canines in Bulgaria. Sbornik dokladi ot nauchnata konferentsiya: Traditsii i s’vremenhost v’v veterinarnata meditsina:247 – 252, in Bulgarian
Kirkova Z, Iliev P, Vesser M, Knaus M (2013) Survey on ectoparasites of dogs (Canis familiaris) in Bulgaria. Conference Proceedings, 12th International Symposium of Ectoparasites in Pets, Munich:16
Krämer F, Schaper R, Schunack B, Połozowski A, Piekarska J, Szwedko A, Jodies R, Kowalska D, Schüpbach D, Pantchev N (2014) Serological detection of Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato and Ehrlichia canis antibodies and Dirofilaria immitis antigen in a countrywide survey in dogs in Poland. Parasitol Res 113(9):3229–39
Krupka I, Pantchev N, Weise M, Straubinger RK (2007) [Tick-transmitted, bacterial infections in dogs: Seroprevalences of Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato and Ehrlichia canis in Germany]. Durch Zecken übertragbare bakterielle Infektionen bei Hunden: Seroprävalenzen von Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato und Ehrlichia canis in Deutschland. Praktischer Tierarzt 10(88):776 – 87, in German
Léger N, Gramiccia M, Gradoni L, Madulo-Leblond G, Pesson B, Ferté H, Boulanger N, Killick-Kendrick R, Killick-Kendrick M (1988) Isolation and typing of Leishmania infantum from Phlebotomus neglectus on the island of Corfu, Greece. Trans R Soc Trop Med Hyg 82(3):419–20
Leontides LS, Saridomichelakis MN, Billinis C, Kontos V, Koutinas AF, Galatos AD, Mylonakis ME (2002) A crosssectional study of Leishmania spp. infection in clinically healthy dogs with polymerase chain reaction and serology in Greece. Vet Parasitol 109(1 – 2):19–27
Levy SA, O’Connor TP, Hanscom JL, Shields P, Lorentzen L, Dimarco AA (2008) Quantitative measurement of C6 antibody following antibiotic treatment of Borrelia burgdorferi antibody-positive nonclinical dogs. Clin Vaccine Immunol 15(1):115–9
Mettler M, Grimm F, Capelli G, Camp H, Deplazes P (2005) Evaluation of enzyme-linked immunosorbent assays, an immunofluorescent-antibody test, and two rapid tests (immunochromatographic-dipstick and gel tests) for serological diagnosis of symptomatic and asymptomatic Leishmania infections in dogs. J Clin Microbiol 43(11):5515–9
Mikov O (2011) Distribution of mosquitoes potentially transmitting West Nile virus in Bulgaria. 9th national congress on clinical microbiology and infection, Bulgarian association of microbiologists, Plovdiv, 28 – 30 April, 2011:45 – 46, in Bulgarian
Mikov O, Harizanov R (2012) Distribution of the phlebotomine sandflies in Bulgaria and their importance as vectors of parasitic and viral diseases. 10th National Congress of Clinical Microbiology and Infections of the Bulgarian Association of Microbiologists, April 26 – 28, 2012, Plovdiv, Bulgaria. Book of abstracts:47 – 48
Miró G, Montoya A, Roura X, Gálvez R, Sainz A (2013) Seropositivity rates for agents of canine vector-borne diseases in Spain: a multicentre study. Parasit Vectors 6:117
O’Connor TP, Esty KJ, Hanscom JL, Shields P, Philipp MT (2004) Dogs vaccinated with common Lyme disease vaccines do not respond to IR6, the conserved immunodominant region of the VlsE surface protein of Borrelia burgdorferi. Clin Diagn Lab Immunol 11(3):458–62
O’Connor TP, Hanscom JL, Hegarty BC, Groat RG, Breitschwerdt EB (2006) Comparison of an indirect immunofluorescence assay, western blot analysis, and a commercially available ELISA for detection of Ehrlichia canis antibodies in canine sera. Am J Vet Res 67(2):206–10
Pantchev N, Schaper R, Limousin S, Norden N, Weise M, Lorentzen L (2009) Occurrence of Dirofilaria immitis and tick-borne infections caused by Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato and Ehrlichia canis in domestic dogs in France: results of a countrywide serologic survey. Parasitol Res 105(Suppl 1):S101–14
Pantchev N, Etzold M, Daugschies A, Dyachenko V (2011) Diagnosis of imported canine filarial infections in Germany 2008–2010. Parasitol Res 109(Suppl 1):S61–76
Pantchev N, Pluta S, Huisinga E, Natter S, Scheufelen M, Globokar Vrhovec M, Schweinitz A, Hampel H, Straubinger RK (2015) Tick-borne diseases (borreliosis, anaplasmosis, babesiosis) in German and Austrian Dogs: status quo and review of distribution, transmission, clinical findings, diagnostics and prophylaxis. Parasitol Res 114(Suppl 1):S13–48
Papazahariadou M, Founta A, Papadopoulos E, Chliounakis S, Antoniadou-Sotiriadou K, Theodorides Y (2007) Gastrointestinal parasites of shepherd and hunting dogs in the Serres Prefecture, Northern Greece. Vet Parasitol 148:170–173
Popova T, Kamenov S (1998) Erythematous form of Lyme in dog. Veterinary Medicine 3–4:244–246
Schnyder M, Tanner I, Webster P, Barutzki D, Deplazes P (2011) An ELISA for sensitive and specific detection of circulating antigen of Angiostrongylus vasorum in serum samples of naturally and experimentally infected dogs. Vet Parasitol 179:152–158
Schnyder M, Deplazes P (2012) Cross-reactions of sera from dogs infected with Angiostrongylus vasorum in commercially available Dirofilaria immitis test kits. Parasit Vectors 5:258
Schnyder M, Schaper R, Bilbrough G, Morgan ER, Deplazes P (2013a) Seroepidemiological survey for canine angiostrongylosis in dogs from Germany and the UK using combined detection of Angiostrongylus vasorum antigen and specific antibodies. Parasitology 140(11):1442–50
Schnyder M, Schaper R, Pantchev N, Kowalska D, Szwedko A, Deplazes P (2013b) Serological detection of circulating Angiostrongylus vasorum antigen- and parasite-specific antibodies in dogs from Poland. Parasitol Res 112(Suppl 1):109–17
Schucan A, Schnyder M, Tanner I, Barutzki D, Traversa D, Deplazes P (2012) Detection of specific antibodies in dogs infected with Angiostrongylus vasorum. Vet Parasitol 185:216–224
Stillman BA, Monn M, Liu J, Thatcher B, Foster P, Andrews B, Little S, Eberts M, Breitschwerdt EB, Beall MJ, Chandrashekar R (2014) Performance of a commercially available in-clinic ELISA for detection of antibodies against Anaplasma phagocytophilum, Anaplasma platys, Borrelia burgdorferi, Ehrlichia canis, and Ehrlichia ewingii and Dirofilaria immitis antigen in dogs. J Am Vet Med Assoc 245(1):80–6
Tsachev I (2006) Detection of antibodies reactive with Ehrlichia canis in a kennel in Bulgaria. Turk J Vet Anim Sci 30:425–426
Tsachev I, Kontos V, Zarkov I, Krastev S (2006a) Survey of antibodies reactive with Ehrlichia canis among dogs in South Bulgaria. Rev Med Vet 157(10):481–485
Tsachev I, Papadagjannakis E, Kontos V, Zarkov I, Petrov V, Pelagic V (2006b) Seroprevalence of Ehrlichia canis infection among privately-owned dogs in northern Bulgaria. J Hell Vet Med Soc 57(3):212–216
Tsachev I, Simeonov R, Petrov V (2007a) Infections with Ehrlichia canis and Borrelia burgdorferi in a dog. Veterinarski glasnik 61(3 – 4):201–210
Tsachev I, Papadajonakis M, Kontos V, Ivanov A, Chakarova B, Stojanchev K, Peshev R (2007b) Seroepidemiology of Leishmania infantum exposure among healthy dogs in Bulgaria. Turk J Vet Anim Sci 31(1):73–4
Tsachev I, Ivanov A, Dinev I, Simeonova G, Kanakov D (2008a) Clinical Ehrlichia canis and Hepatozoon canis coinfection in a dog in Bulgaria. Rev Med Vet 159(2):68–73
Tsachev I, Petrov V, Fleming K, Brown C (2008b) First detected case of Anaplasma phagocytophilum in a dog in Bulgaria. Revue de Médecine Vétérinaire 159 (11):562 – 564 Tsachev I (2009) Exotic zoonoses among dogs in Bulgaria. DSc Thesis:315, in Bulgarian
Tsachev I, Petrov V (2009) A clinical case of asymptomatic pancytopaenia in a dog. Scientific works, C series, LV (2), Veterinary Medicine, UASVM, Bucharest:29 – 33
Tsachev I, Kyriazis I, Karagouni E, Boutsini S, Dotsika E (2010) First report of canine visceral leishmaniasis in Bulgaria. Turk J Vet Anim Sci 34(5):465–469
Tsachev I, Dimov I (2012) Seroprevalence of Borrelia burgdorferi in dogs in Bulgaria. 2nd International Epizootiology Days, book of abstracts, Belgrade:175
Tsachev I, Gundasheva D, Papadagjannakis E, Kontos V, Denev S (2013) Haematological profiles in canine monocytic ehrlichiosis: a retrospective study of 31 spontaneous cases in Greece. Rev Med Vet 164(6):327–330
Villeneuve A, Goring J, Marcotte L, Overvelde S (2011) Seroprevalence of Borrelia burgdorferi, Anaplasma phagocytophilum, Ehrlichia canis, and Dirofilaria immitis among dogs in Canada. Can Vet J 52(5):527–30
Volgina NS, Romashov BV, Romashova NB, Shtannikov AV (2013) Prevalence of borreliosis, anaplasmosis, ehrlichiosis and Dirofilaria immitis in dogs and vectors in Voronezh Reserve (Russia). Comp Immunol Microbiol Infect Dis 36(6):567–74
Wagner B, Freer H, Rollins A, Garcia-Tapia D, Erb HN, Earnhart C, Marconi R, Meeus P (2012) Antibodies to Borrelia burgdorferi OspA, OspC, OspF, and C6 antigens as markers for early and late infection in dogs. Clin Vaccine Immunol 19(4):527–35
Waner T, Strenger C, Keysary A, Harrus S (1998) Kinetics of serologic cross-reactions between Ehrlichia canis and the Ehrlichia phagocytophila genogroups in experimental E. canis infection in dogs. Vet Immunol Immunopathol 66(3 – 4):237–43
Weil GJ (1987) Dirofilaria immitis: identification and partial characterization of parasite antigens in the serum of infected dogs. Exp Parasitol 64:244–251
Wolf D, Failing K, Taubert A, Pantchev N (2014) Serological diagnosis of canine leishmaniosis: comparison of three commercially available tests. Parasitol Res 113(5):1997–2002
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0), which permits use, duplication, adaptation, distribution, and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
About this article
Cite this article
Pantchev, N., Schnyder, M., Vrhovec, M.G. et al. Current Surveys of the Seroprevalence of Borrelia burgdorferi, Ehrlichia canis, Anaplasma phagocytophilum, Leishmania infantum, Babesia canis, Angiostrongylus vasorum and Dirofilaria immitis in Dogs in Bulgaria. Parasitol Res 114 (Suppl 1), 117–130 (2015). https://doi.org/10.1007/s00436-015-4518-8
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-015-4518-8