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Recent study on canine vector-borne zoonoses in southern Slovakia - serologic survey

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Abstract

Over the last decade a significant spread of Canine Vector Borne Diseases has been recorded in Central Europe. The aim of the study described here, was to collect current data on the occurrence and distribution of three major canine vector-borne pathogens in the veterinary clinical practice by a newly-developed commercial ELISA test for the detection of Dirofilaria immitis antigen as well as specific circulating antibodies to Anaplasma phagocytophilum and Borrelia burgdorferi sensu lato. Circulating D. immitis antigen was detected in five of 180 investigated sera samples. Two of D. immitis seropositive dogs revealed also microfilariae of D. repens in the blood and three of them were negative for the presence of microfilariae in the Knott´s test. From the practical point of view, the finding of D. immitis occult infections might influence existing knowledge about distribution of this species among dogs in Central European countries. In 11.7% of the tested dogs the presence of specific antibodies against A. phagocytophilum was confirmed. Antibodies against B. burgdorferi s.l. were detected in 2.8% of tested sera samples. Coinfection with A. phagocytophilum and B. burgdorferi s.l. was observed in two dogs from Košice district in south-eastern Slovakia. Our data point toward the presence of Canine Vector Borne Diseases in the studied area. Therefore, veterinarians should include these diseases in their differential diagnosis and higher awareness should be focused also on prophylactic measures to prevent the pathogens transmission by arthropod vectors.

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References

  • Anderson J. 1991. Epizootology of lyme borreliosis. Scandinavian Journal of Infectious Diseases. Suppl. 77, 23–34

    PubMed  CAS  Google Scholar 

  • Angus B.M. 1981. Periodicity exhibited by microfilariae of Dirofilaria immitis in South East Queensland. Australian Veterinary Journal, 57, 101–102

    Article  CAS  Google Scholar 

  • Beall M.J., Chandrashekar R., Eberts M.D., Cyr K.E., Diniz P.P., Mainville C., Hegarty B.C., Crawford J.M., Breitschwerdt E.B. 2008. Serological and molecular prevalence of Borrelia burgdorferi, Anaplasma phagocytophilum, and Ehrlichia species in dogs from Minnesota. Vector-Borne and Zoonotic Diseases, 8, 455–464. DOI: 10.1089/vbz.2007.0236

    Article  Google Scholar 

  • Bland J.M. 2000. An introduction to medical statistics. 3th edition, Oxford University Press, 230

    Google Scholar 

  • Carrade D.D., Foley J.E., Borjesson D.L., Sykes J.E., 2009. Canine granulocytic anaplasmosis: a review. Journal of Veterinary Internal Medicine, 23, 1129–41. DOI: 10.1111/j.1939-1676. 2009.0384.x

    Article  CAS  Google Scholar 

  • Courtney C.H., Zeng Q.Y. 2001. Comparison of heartworm antigen test kit performance in dogs having low heartworm burdens. Veterinary Parasitology, 96, 317–322

    Article  CAS  Google Scholar 

  • Derdáková M., Štefancíková A., Špitálska E., Taragelová V., Koštálová T., Hrklová G., Kybicová K., Schánilec P., Majláthová V., Várady M., Petko, B. 2011. Emergence and genetic variability of Anaplasma species in small ruminants and ticks from Central Europe. Veterinary Microbiology, 153, 293–298. DOI: 10.1016/j.vetmic.2011.05.044

    Article  Google Scholar 

  • Di Cesare A., Otranto D., Di Giulio E., Simonato G., Latrofa M.S., La Torre F., Coccia G., Traversa D. 2013. Microfilarial periodicity of Dirofilaria repens in naturally infested dogs. Parasitology Research, 112, 4273–4279. DOI: 10.1007/s00436-013-3619-5

    Article  Google Scholar 

  • EPIS. Epidemiological Informative System of Communicable Diseases of the Slovak Republic, http://www.epis.sk

  • Fók E., Kiss G., Majoros G., Jacsó O., Farkas R., Gyurkovszky M. 2007. Preliminary results of an epidemiological survey on dirofilariosis of dogs and cats in Hungary. Mappe Parassito-logiche - Dirofilaria immitis and Dirfilaria repens in dog and cat and human infection (ed.: Genchi C., Rinaldi L. and Cringoli G.), 8, 195–196. Rolando Editore, Naples 2007

    Google Scholar 

  • Gauthier D.T., Mansfield L.S. 1999. Western immunoblot analysis for distinguishing vaccination and infection status with Borrelia burgdorferi (Lyme disease) in dogs. Journal of Veterinary Diagnostic Investigation, 11, 259–265

    Article  CAS  Google Scholar 

  • Genchi C., Solari Basano F., Bandi C., Di Sacco B., Venco L., Vezzoni A., Cancrini G. 1995. Factors influencing the spread of heartworms in Italy: interaction between Dirofilaria immitis and Dirofilaria repens. Proceedings of Heartworm Symposium’ 95. American Heartworm Society, Batavia, Illinois, pp. 65–71

    Google Scholar 

  • Genchi C., Mortarino M., Rinaldi L., Cringoli G., Traldi G., Genchi M. 2011. Changing climate and changing vector-borne disease distribution: the example of Dirofilaria in Europe. Veterinary Parasitology, 176, 295–299

    Article  Google Scholar 

  • Goldstein R.E., Cordner A.P., Sandler J.L., Bellohusen B.A., Erb H.N. 2007. Microalbuminuria and comparison of serologic testing for exposure to Borrelia burgdorferi in nonclinical Labrador and Golden Retrievers. Journal of Veterinary Diagnostic Investigation, 19, 294–297

    Article  Google Scholar 

  • Grieve R.B., Lauria S. 1983. Periodicity of Dirofilaria immitis microfilariae in canine and murine hosts. Acta Tropica, 40, 121–127

    PubMed  CAS  Google Scholar 

  • Grieve R.B., Glickman L.T., Bater A.K. 1986. Canine Dirofilaria immitis infection in a hyperenzootic area: examination by para-sitologic finds at necropsy and by two serodiagnostic methods. American Journal of Veterinary Research, 47, 392–393

    Google Scholar 

  • Hamel D., Silaghi C., Zapadynska S., Kudrin A., Pfister K. 2013. Vector-borne pathogens in ticks and EDTA-blood samples collected from client-owned dogs, Kiev, Ukraine. Ticks and Tick-Borne Diseases, 4, 152–155. DOI:10.1016/j.ttbdis.2012.08.005

    Article  Google Scholar 

  • Iglódyová A., Miterpáková M. 2014. The survey of canine blood filarioses in Slovakia. V4 Parasitological Meeting - Parasites in the heart of Europe, Book of abstracts. 25–30 May 2014, Stará Lesná, The High Tatras, Slovakia. Slovak Society for Parasitology at SAS, Košice, pp.79–80

    Google Scholar 

  • Iglódyová A., Miterpáková M., Hurníková Z., Antolová D., Dubinský P., Letková V. 2012. Canine dirofilariosis under specific environmental conditions of the Eastern Slovak Lowland. Annals of Agricultural and Environmental Medicine, 19, 57–60

    PubMed  Google Scholar 

  • Jacsó O., Mándoki M., Majoros G., Pétsch M., Mortarino M., Genchi C., Fók É. 2009. First autochthonous Dirofilaria immitis (Leidy, 1856) infection in a dog in Hungary. Helminthologia, 46, 159–161. DOI: 10.2478/s11687-009-0030-y

    Article  Google Scholar 

  • Knott J. 1939. A method for making microfilarial survey on day blood. Transactions of the Royal Society of Tropical Medicine and Hygiene, 33, 191

    Article  Google Scholar 

  • Krämer F., Schaper R., Schunack B., Polozowski A., Piekarska J., Szwedko A., Jodies R., Kowalska D., Schüpbach D., Pantchev N. 2014. Serological detection of Anaplasma phagocy-tophilum, Borrelia burgdorferi sensu lato and Ehrlichia canis antibodies and Dirofilaria immitis antigen in a countrywide survey in dogs in Poland. Parasitological Research, 113, 3229–3239. DOI:10.1007/s00436-014-3985-7

    Article  Google Scholar 

  • Krupka I., Pantchev N., Lorentzen L., Weise M., Straubinger R.K. 2007. Tick-transmitted bacterial infections in dogs: Sero-prevalences of Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato and Ehrlichia canis in Germany. (in German). Praktische Tierarzt, 88, 776–788

    Google Scholar 

  • Labarthe N., Almosny N., Guerrero J., Duque-Araújo A.M. 1997. Description of the occurrence of canine dirofilariasis in the State of Rio de Janeiro Brazil. Memórias do Instituto Oswaldo Cruz, 92, 47–51

    Article  CAS  Google Scholar 

  • Landscape Atlas of the Slovak Republic - digital version. 2002. Ministry of Environment of the Slovak Republic, Slovak Environmental Agency, Esprit Ed., Banská Štiavnica, Slovak Republic

  • Latrofa M.S., Dantas-Torres F., Annoscia G., Genchi M., Traversa D., Otranto D. 2012. A duplex real-time polymerase chain reaction assay for the detection of and differentiation between Dirofilaria immitis and Dirofilaria repens in dogs and mosquitoes. Veterinary Parasitology, 185, 181–185. DOI: 10.1016/j.vetpar.2011.10.038

    Article  CAS  Google Scholar 

  • Levy S.A., O’Connor T.P., Hanscom J.L., Shields P., Lorentzen L., Dimarco A.A. 2008. Quantitative measurement of C6 antibody following antibiotic treatment of Borrelia burgdorferi antibody-positive nonclinical dogs. Clinical and Vaccine Immunology, 15, 115–119. DOI: 10.1128/CVI.00340-07.

    Article  CAS  Google Scholar 

  • Liang F.T., Aberer E., Cinco M., Gern L., Hu C.M., Lobet Y.N., Ruscio M., Voet P.E. Jr, Weynants V.E., Philipp M.T. 2000. Antigenic conservation of an immunodominant invariable region of the VlsE lipoprotein among European pathogenic genospecies of Borrelia burgdorferi SL. Journal of Infectious Diseases, 182, 1455–1462. DOI: 10.1086/315862

    Article  CAS  Google Scholar 

  • Littman M.P. 2013. Lyme nephritis. Journal of Veterinary Emergency and Critical Care, 23, 163–173. DOI: 10.1111/vec.12026

    Article  Google Scholar 

  • Littman M.P., Goldstein R.E., Labato M.A., Lappin M.R., Moore G.E. 2006. ACVIM small animal consensus statement on Lyme disease in dogs: diagnosis, treatment, and prevention. Journal of Veterinary Internal Medicine, 20, 422–434

    Article  Google Scholar 

  • Matola Y.G. 1991. Periodicity of Dirofilaria immitis microfilariae in a dog from Muheza district, Tanzania. Journal of Helminthology, 65, 76–78

    Article  CAS  Google Scholar 

  • Mihalca A.D., Sándor A.D. 2013. The role of rodents in the ecology of Ixodes ricinus and associated pathogens in Central and Eastern Europe. Frontiers in Cellular and Infection Microbiology, 3, Article 66. DOI:10.3389/fcimb.2013.00056

    Article  Google Scholar 

  • Miterpáková M., Antolová D., Hurníková Z., Dubinský P. 2008. Dirofilariosis in Slovakia - a new endemic area in Central Europe. Helminthologia, 45, 20–23. DOI: 10.2478/s11687-008-0003-6

    Article  Google Scholar 

  • Miterpáková M., Antolová D., Hurníková Z., Dubinský P., Pavlacka A., Németh J. 2010. Dirofilaria infections in working dogs in Slovakia. Helminthologia, 84, 173–176. DOI: 10.1017/S00221 49X09990496

    Article  Google Scholar 

  • Nelson C.T., McCall J.W., Rubin S.B., Buzhardt L.F., Dorion D.W., Graham W., Longhofer S.L., Guerrero J., Robertson-Plouch C., Paul A. 2005. Guidelines for the diagnosis, prevention and management of heartworm (Dirofilaria immitis) infection in dogs. Veterinary Parasitology, 133, 255–266

    Article  Google Scholar 

  • Nováková M., Víchová B., Majláthová V., Lesnáková A., Pochybová M., Petko B. 2010. First case of human granulocytic anaplasmosis (HGA) from Slovakia. Annals of Agricultural and Environmental Medicine, 17, 173–175

    PubMed  Google Scholar 

  • O’Connor T.P., Esty K.J., Hanscom J.L., Shields P., Philipp M.T. 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. Clinical and Diagnostic Laboratory Immunology, 11, 458–462

    PubMed  PubMed Central  Google Scholar 

  • Pangrácová L., Derdáková M., Pekárik L., Hvišcová I., Víchová B., Stanko M., Hlavatá H., Petko B. 2013. Ixodes ricinus abundance and its infection with the tick-borne pathogens in urban and suburban areas of Eastern Slovakia. Parasites and Vectors, 6, 238. DOI:10.1186/1756-3305-6-238

    Article  Google Scholar 

  • Pantchev N., Etzold M., Daugschies A., Dyachenko V. 2011. Diagnosis of imported canine filarial infections in Germany 2008–2010. Parasitology Research, 109, S61–S76. DOI:10.1007/s00436-011-2403-7

    Article  Google Scholar 

  • Rawlings C.A., Dave D.L., McCall J.W. 1982. Four types of occult Dirofilaria immitis infection in dogs. Journal of the American Veterinary Medical Association, 180, 1323–1326

    PubMed  CAS  Google Scholar 

  • Rhee J.K., Yang S.S., Kim H.C. 1998. Periodicity exhibited by Dirofilaria immitis microfilariae identified in dogs of Korea. Korean Journal of Parasitology, 36, 235–239

    Article  CAS  Google Scholar 

  • Rishniw M., Barr S.C., Simpson K.W., Frongillo M., Franz M., Dominquez Alpizar J.L. 2006. Discrimination between six species of canine microfilariae by a single polymerase chain reaction. Veterinary Parasitology, 135, 303–314

    Article  CAS  Google Scholar 

  • Scorpio D.G., Dumler J.S., Barat N.C., Cook J.A., Barat C.E., Stillman B.A., Brett A., DeBisceglie K.C. Beall M.J., Chandrashekar R., 2011. Comparative strain analysis of Anaplasma phagocytophilum infection and clinical outcomes in a canine model of granulocytic anaplasmosis. Vector-Borne and Zoonotic Diseases, 11, 223–229. DOI: 10.1089/vbz.2009.0262

    Article  Google Scholar 

  • Schnyder M., Deplazes P. 2012. Crossreactions of sera from dogs infected with Angiostrongylus vasorum in commercially available Dirofilaria immitis test kits. Parasites and Vectors, 5, 258. DOI: 10.1186/1756-3305-5-258.

    Article  Google Scholar 

  • Semenza J.C., Benne B. 2009. Climate change and infectious diseases in Europe. Lancet, 9, 365–375

    Article  Google Scholar 

  • Semenza J.C., Zeller H. 2014. Integrated surveillance for prevention and control of emerging vector-borne diseases in Europe. Eurosurveillance, 19, pii = 20757. Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId = 20757

    Article  Google Scholar 

  • Stillman B.A., Monn M., Liu J., Thatcher B., Foster P., Andrews B., Little S., Eberts M., Breitschwerdt E.B., Beall M.J., Chandrashekar R. 2014. Performance of a new commercially available inclinic ELISA for the detection of antibodies to Anaplasma phagocytophilum, Anaplasma platys, Borrelia burgdorferi, Ehrlichia canis and E. ewingii and Dirofilaria immitis antigen in dogs. Journal of the American Veterinary Medical Association, 245, 80–86. DOI: 10.2460/javma.245.1.80

    Article  Google Scholar 

  • Straubinger R.K. 2000. PCR-based quantification of Borrelia burgdorferi organisms in canine tissues over a 500-day postinfection period. Journal of Clinical Microbiology, 38, 2191–2199

    PubMed  PubMed Central  CAS  Google Scholar 

  • Straubinger R.K., Straubinger A.F., Summers B.A., Jacobson R.H. 2000. Status of Borrelia burgdorferi infection after antibiotic treatment and the effects of corticosteroids: An experimental study. Journal of Infection Diseases, 181, 1069–1081

    Article  CAS  Google Scholar 

  • Straubinger R.K., Rao T.D., Davidson E., Summerse B.A., Jacobson R.H., Frey A.B. 2002. Protection against tick-transmitted Lyme disease in dogs vaccinated with a multiantigenic vaccine. Vaccine, 20, 181–193

    Article  Google Scholar 

  • Svobodová Z., Svobodová V., Genchi C., Forejtek P. 2006. The first report of autochthonous dirofilariosis in dogs in the Czech Republic. Helminthologia, 43, 242–245. DOI: 10.2478/s11687-006-0046-5

    Article  Google Scholar 

  • Štefancíková A., Derdáková M., Škardová I., Szestáková E., Cisláková L., Kovácová D., Stanko M., Petko B. 2008. Some epidemiological and epizootiological aspects of Lyme borreliosis in Slovakia with the emphasis on the problems of serological diagnostics. Biologia, 63, 1135–1142. 10.2478/s11756-008-0177-x

    Article  Google Scholar 

  • Štefanidesová K., Kocianová E., Boldiš V., Koštanová Z., Kanka P., Némethová D., Špitalská E. 2008. Evidence of Anaplasma phagocytophilum and Rickettsia helvetica infection in free-ranging ungulates in central Slovakia. European Journal of Wildlife Research, 54, 519–524. DOI: 10.1007/s10344-007-0161-8

    Article  Google Scholar 

  • Švihrová V., Hudecková H., Jesenák M., Schwarzová K., Koštanová Z., Cižnár I. 2001. Lyme borreliosis-analysis of the trends in Slovakia. Folia Microbiologica, 56, 270–275.

    Article  CAS  Google Scholar 

  • Swiatalska A., Demiaszkiewicz A.W. 2012. First autochthonous case of Dirofilaria immitis invasion in dog in Poland. (in Polish). Zycie Weterynaryjne, 87, 685–686

    Google Scholar 

  • Víchová B., Majláthová V., Nováková M., Stanko M., Hvišcová I., Blanarová L., Chrudimský T., Curlík J., Petko B. 2014a. Anaplasma infections in ticks and reservoir host from Slovakia. Infection, Genetics and Evolution, 22, 265–272. DOI: 10.1016/j.meegid.2013.06.003

    Article  CAS  Google Scholar 

  • Víchová B., Miterpáková M., Iglódyová A. 2014b. Molecular detection of co-infections with Anaplasma phagocytophilum and/or Babesia canis canis in Dirofilaria-positive dogs from Slovakia. Veterinary Parasitology, 203, 167–172. DOI: 10.1016/j.vetpar.2014.01.022

    Article  Google Scholar 

  • Wagner B., Freer H., Rollins A., Garcia-Tapia D., Erb H.N., 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. Clinical and Vaccine Immunology, 19, 527–535. DOI: 10.1128/CVI

    Article  CAS  Google Scholar 

  • Webber W.A.F., Hawking F. 1955. Experimental maintenance of Dirofilaria repens and D. immitis in dogs. Experimental Parasitology, 4, 143–164

    Article  CAS  Google Scholar 

  • Weil G.J. 1987. Dirofilaria immitis: identification and partial characterization of parasite antigens in the serum of infected dogs. Experimental Parasitology, 64, 244–251

    Article  CAS  Google Scholar 

  • Weil G.J., Malane M.S., Powers K.G. 1984. Detection of circulating parasite antigens in canine dirofilariasis by counterimmuno-electrophoresis. American Journal of Tropical Medicine and Hygiene, 33, 425–30

    Article  CAS  Google Scholar 

  • Zittra C., Kocziha Z., Pinnyei S., Harl J., Kieser K., Laciny A., Eigner B., Silbermayr K., Duscher G.G., Fok É., Fuehrer H.P. 2015. Screening blood-fed mosquitoes for the diagnosis of filarioid helminths and avian malaria. Parasites and Vectors, 8, 16. DOI:10.1186/s13071-015-0637-4

    Article  Google Scholar 

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Čabanová, V., Pantchev, N., Hurníková, Z. et al. Recent study on canine vector-borne zoonoses in southern Slovakia - serologic survey. Acta Parasit. 60, 749–758 (2015). https://doi.org/10.1515/ap-2015-0107

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