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Occurrence and diversity of arthropod-transmitted pathogens in red foxes (Vulpes vulpes) in western Austria, and possible vertical (transplacental) transmission of Hepatozoon canis

Published online by Cambridge University Press:  24 August 2017

ADNAN HODŽIĆ ,
NAIKE MROWIETZ ,
RITA CÉZANNE ,
PIA BRUCKSCHWAIGER ,
SYLVIA PUNZ ,
VERENA ELISABETH HABLER ,
VALENTINA TOMSIK ,
JUDIT LAZAR ,
GEORG G. DUSCHER  and
WALTER GLAWISCHNIG
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ADNAN HODŽIĆ
Affiliation:
Department of Pathobiology, Institute of Parasitology, University of Veterinary Medicine Vienna, Veterinaerplatz 1, 1210 Vienna, Austria
NAIKE MROWIETZ
Affiliation:
Department of Pathobiology, Institute of Parasitology, University of Veterinary Medicine Vienna, Veterinaerplatz 1, 1210 Vienna, Austria
RITA CÉZANNE
Affiliation:
Department of Pathobiology, Institute of Parasitology, University of Veterinary Medicine Vienna, Veterinaerplatz 1, 1210 Vienna, Austria
PIA BRUCKSCHWAIGER
Affiliation:
Department of Pathobiology, Institute of Parasitology, University of Veterinary Medicine Vienna, Veterinaerplatz 1, 1210 Vienna, Austria
SYLVIA PUNZ
Affiliation:
Department of Pathobiology, Institute of Parasitology, University of Veterinary Medicine Vienna, Veterinaerplatz 1, 1210 Vienna, Austria
VERENA ELISABETH HABLER
Affiliation:
Department of Pathobiology, Institute of Parasitology, University of Veterinary Medicine Vienna, Veterinaerplatz 1, 1210 Vienna, Austria
VALENTINA TOMSIK
Affiliation:
Department of Pathobiology, Institute of Parasitology, University of Veterinary Medicine Vienna, Veterinaerplatz 1, 1210 Vienna, Austria
JUDIT LAZAR
Affiliation:
Institute for Veterinary Disease Control, Austrian Agency for Health and Food Safety, Technikerstraße 70, 6020 Innsbruck, Austria
GEORG G. DUSCHER
Affiliation:
Department of Pathobiology, Institute of Parasitology, University of Veterinary Medicine Vienna, Veterinaerplatz 1, 1210 Vienna, Austria
WALTER GLAWISCHNIG
Affiliation:
Institute for Veterinary Disease Control, Austrian Agency for Health and Food Safety, Technikerstraße 70, 6020 Innsbruck, Austria
HANS-PETER FUEHRER*
Affiliation:
Department of Pathobiology, Institute of Parasitology, University of Veterinary Medicine Vienna, Veterinaerplatz 1, 1210 Vienna, Austria
*
*Corresponding author: Department of Pathobiology, Institute of Parasitology, University of Veterinary Medicine Vienna, Veterinaerplatz 1, 1210 Vienna, Austria. Email: Hans-Peter.Fuehrer@vetmeduni.ac.at
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Summary

Red fox (Vulpes vulpes) is the most abundant wild canid species in Austria, and it is a well-known carrier of many pathogens of medical and veterinary concern. The main aim of the present study was to investigate the occurrence and diversity of protozoan, bacterial and filarial parasites transmitted by blood-feeding arthropods in a red fox population in western Austria. Blood (n = 351) and spleen (n = 506) samples from foxes were examined by PCR and sequencing and the following pathogens were identified: Babesia canis, Babesia cf. microti (syn. Theileria annae), Hepatozoon canis, Anaplasma phagocytophilum, Candidatus Neoehrlichia sp. and Bartonella rochalimae. Blood was shown to be more suitable for detection of Babesia cf. microti, whilst the spleen tissue was better for detection of H. canis than blood. Moreover, extremely low genetic variability of H. canis and its relatively low prevalence rate observed in this study may suggest that the parasite has only recently been introduced in the sampled area. Furthermore, the data presented here demonstrates, for the first time, the possible vertical transmission of H. canis from an infected vixen to the offspring, and this could explain the very high prevalence in areas considered free of its main tick vector(s).

Keywords

vector-borne pathogensHepatozoon canistransplacental transmissionfoxVulpes vulpesAustria
Type
Research Article
Information
Parasitology , Volume 145 , Issue 3 , March 2018 , pp. 335 - 344
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Copyright
Copyright © Cambridge University Press 2017 

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References

REFERENCES

Aguirre, A. A. (2009). Wild canids as sentinels of ecological health: a conservation medicine perspective. Parasites and Vectors 2(Suppl. 1), S7.CrossRefGoogle Scholar
Alvarado-Rybak, M., Solano-Gallego, L. and Millán, J. (2016). A review of piroplasmid infections in wild carnivores worldwide: importance for domestic animal health and wildlife conservation. Parasites and Vectors 9, 538.Google Scholar
Baneth, G. (2011). Perspectives on canine and feline hepatozoonosis. Veterinary Parasitology 181, 3–11.CrossRefGoogle ScholarPubMed
Barandika, J. F., Espí, A., Oporto, B., Del Cerro, A., Barral, M., Povedano, I., García-Pérez, A. L. and Hurtato, A. (2016). Occurrence and genetic diversity of piroplasms and other apicomplexa in wild carnivores. Parasitology 2, 1–7.Google Scholar
Brown, G. K., Martin, A. R., Roberts, T. K. and Aitken, R. J. (2001). Detection of Ehrlichia platys in dogs in Australia. Australian Veterinary Journal 79, 554–558.CrossRefGoogle ScholarPubMed
Camacho, A. T. (2006). Piroplasma infection in dogs in northern Spain. Veterinary Parasitology 138, 97–102.Google Scholar
Camacho, A. T., Pallas, E., Gestal, J. J., Guitián, F. J., Olmeda, A. S., Telford, S. R. and Spielman, A. (2003). Ixodes hexagonus is the main candidate as vector of Theileria annae in northwest Spain. Veterinary Parasitology 112, 157–163.Google Scholar
Cardoso, L., Cortes, H. C. E., Reis, A., Rodrigues, P., Simões, M., Lopes, A. P., Vila-Viçosac, M. J., Talmi-Frankd, D., Eyald, O., Solano-Gallegoe, L. and Baneth, G. (2013). Prevalence of Babesia microti-like infection in red foxes (Vulpes vulpes) from Portugal. Veterinary Parasitology 196, 90–95.CrossRefGoogle ScholarPubMed
Cardoso, L., Cortes, H. C. E., Eyal, O., Reis, A., Lopes, A. P., Vila-Viçosa, M. J., Rodrigues, P. A. and Baneth, G. (2014). Molecular and histopathological detection of Hepatozoon canis in red foxes (Vulpes vulpes) from Portugal. Parasites and Vectors 7, 113.CrossRefGoogle ScholarPubMed
Cardoso, L., Gilad, M., Cortes, H. C. E., Nachum-Biala, Y., Lopes, A. P., Vila-Viçosa, M. J., Simões, M., Rodrigues, P. A. and Baneth, G. (2015). First report of Anaplasma platys infection in red foxes (Vulpes vulpes) and molecular detection of Ehrlichia canis and Leishmania infantum in foxes from Portugal. Parasites and Vectors 8, 144.Google Scholar
Diniz, P. P., Maggi, R. G., Schwartz, D. S., Cadenas, M. B., Bradley, J. M., Hegarty, B. and Breitschwerdt, E. B. (2007). Canine bartonellosis: serological and molecular prevalence in Brazil and evidence of co-infection with Bartonella henselae and Bartonella vinsonii subsp. berkhoffii . Veterinary Research 38, 697–710.Google Scholar
Dumitrache, M. O., Matei, I. A., Ionică, A. M., Kalmár, Z., D'Amico, G., Sikó-Barabási, S., Ionescu, D. T., Gherman, C. M. and Mihalca, A. D. (2015). Molecular detection of Anaplasma phagocytophilum and Borrelia burgdorferi sensu lato genospecies in red foxes (Vulpes vulpes) from Romania. Parasites and Vectors 8, 514.CrossRefGoogle ScholarPubMed
Duscher, G. G., Kübber-Heiss, A., Richter, B. and Suchentrunk, F. (2013). A golden jackal (Canis aureus) from Austria bearing Hepatozoon canis – import due to immigration into a non-endemic area? Ticks and Tick Borne Diseases 4, 133–137.Google Scholar
Duscher, G. G., Fuehrer, H-P. and Kübber-Heiss, A. (2014). Fox on the run – molecular surveillance of fox blood and tissue for the occurrence of tick-borne pathogens in Austria. Parasites and Vectors 7, 521.Google Scholar
Duscher, G. G., Leschnik, M., Fuehrer, H-P. and Joachim, A. (2015). Wildlife reservoirs for vector-borne canine, feline and zoonotic infections in Austria. International Journal for Parasitology: Parasites and Wildlife 4, 89–96.Google Scholar
Ebani, V. V., Verin, R., Fratini, F., Poli, A. and Cerri, D. (2011). Molecular survey of Anaplasma phagocytophilum and Ehrlichia canis in red foxes (Vulpes vulpes) from central Italy. Journal of Wildlife Diseases 47, 699–703.CrossRefGoogle ScholarPubMed
Eremeeva, M. E., Gerns, H. L., Lydy, S. L., Goo, J. S., Ryan, E. T., Mathew, S. S., Ferraro, M. J., Holden, J. M., Nicholson, W. L., Dasch, G. A. and Koehler, J. E. (2007). Bacteremia, fever, and splenomegaly caused by a newly recognized Bartonella species. The New England Journal of Medicine 356, 2381–2387.Google Scholar
Falkenö, U., Tasker, S., Osterman-Lind, E. and Tvedten, H. W. (2013). Theileria annae in a young Swedish dog. Acta Veterinaria Scandinavica 55, 50.CrossRefGoogle Scholar
Fuehrer, H.-P., Starzengruber, P., Swoboda, P., Ali Khan, W., Matt, J., Ley, B., Thriemer, K., Haque, R., Yunus, E. B., Hossain, S. M., Walochnik, J. and Noedl, H. (2010). Indigenous Plasmodium ovale malaria in Bangladesh. The American Journal of Tropical Medicine and Hygiene 83, 75–78.CrossRefGoogle ScholarPubMed
Fuehrer, H.-P., Auer, H., Leschnik, M., Silbermayr, K., Duscher, G. G. and Joachim, A. (2016). Dirofilaria in humans, dogs, and vectors in Austria (1978–2014) – from imported pathogens to the endemicity of Dirofilaria repens . PLOS Neglected Tropical Diseases 10, e0004547.CrossRefGoogle Scholar
Giannelli, A., Lia, R. P., Annoscia, G., Buonavoglia, C., Lorusso, E., Dantas-Torres, F., Baneth, G. and Otranto, D. (2017). Rhipicephalus turanicus, a new vector of Hepatozoon canis . Parasitology 144, 730–737.CrossRefGoogle ScholarPubMed
Hall, T. A. (1999). Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Harris, J. D. (2016). Naming no names: comments on the taxonomy of small piroplasmids in canids. Parasites and Vectors 9, 289.CrossRefGoogle ScholarPubMed
Härtwig, V., von Loewenich, F. D., Schultze, C., Straubinger, R. K., Daugschies, A. and Dyachenko, V. (2014). Detection of Anaplasma phagocytophilum in red foxes (Vulpes vulpes) and raccoon dogs (Nyctereutes procynoides) from Brandenburg, Germany. Ticks and Tick-borne Diseases 5, 277–280.Google Scholar
Henn, J. B., Chomel, B. B., Boulouis, H-J., Kasten, R. W., Murray, W. J., Bar-Gal, G. K., King, R., Courreau, J. F. and Baneth, G. (2009). Bartonella rochalimae in raccoons, coyotes, and red foxes. Emerging and Infectious Diseases 5, 1984–1987.CrossRefGoogle Scholar
Hodžić, A., Alić, A., Fuehrer, H. P., Harl, J., Wille-Piazzai, W. and Duscher, G. G. (2015). A molecular survey of vector-borne pathogens in red foxes (Vulpes vulpes) from Bosnia and Herzegovina. Parasites and Vectors 8, 88.CrossRefGoogle ScholarPubMed
Hodžić, A., Cézanne, R., Duscher, G. G., Harl, J., Glawischnig, W. and Fuehrer, H-P. (2015a) Candidatus Neoehrlichia sp. in an Austrian fox is distinct from Candidatus Neoehrlichia mikurensis, but closer related to Candidatus Neoehrlichia lotoris. Parasites and Vectors 8, 539.CrossRefGoogle Scholar
Hodžić, A., Zörer, J. and Duscher, G. G. (2017). Dermacentor reticulatus, a putative vector of Babesia cf. microti (syn. Theileria annae) piroplasm. Parasitology Research 116, 1075–1077.CrossRefGoogle ScholarPubMed
Hodžić, A., Mitkovà, B., Modrý, D., Juránková, J., Frgelecová, L., Forejtek, P., Steinbauer, V. and Duscher, G. G. (2017a). A new case of the enigmatic Candidatus Neoehrlichia sp. (FU98) in a fox from the Czech Republic. Molecular and Cellular Probes 31, 59–60.Google Scholar
Hornok, S., Trauttwein, K., Takács, N., Hodžić, A., Duscher, G. G. and Kontschán, J. (2017). Molecular analysis of Ixodes rugicollis, Candidatus Neoehrlichia sp. (FU98) and a novel Babesia genotype from a European badger (Meles meles). Ticks and Tick-borne Diseases 8, 41–44.CrossRefGoogle Scholar
Hulínská, D., Langrová, K., Pejcoch, M. and Pavlásek, I. (2004). Detection of Anaplasma phagocytophilum in animals by real-time polymerase chain reaction. Acta Pathologica, Microbiologica, et Immunologica Scandinavica 112, 239–247.Google Scholar
Karayiannis, S., Ntais, P., Messaritakis, I., Tsirigotakis, N., Dokianakis, E. and Antoniou, M. (2015). Detection of Leishmania infantum in red foxes (Vulpes vulpes) in Central Greece. Parasitology 142, 1574–1578.Google Scholar
Karbowiak, G., Víchová, B., Majláthová, V., Hapunik, J. and Peťko, B. (2009). Anaplasma phagocytophilum infection of red foxes (Vulpes vulpes). Annals of Agricultural and Environmental Medicine 16, 299–300.Google ScholarPubMed
le Fichoux, Y., Quaranta, J. F., Aufeuvre, J. P., Lelievre, A., Marty, P., Suffia, I., Rousseau, D. and Kubar, J. (1999). Occurrence of Leishmania infantum parasitemia in asymptomatic blood donors living in an area of endemicity in southern France. Journal of Clinical Microbiology 37, 1953–1957.CrossRefGoogle Scholar
Magi, M., Calderini, P., Gabrielli, S., Dell'Omodarme, M., Macchioni, F., Prati, M. C. and Cancrini, G. (2008). Vulpes vulpes: a possible wild reservoir for zoonotic filariae. Vector Borne and Zoonotic Diseases 8, 249–252.Google Scholar
Majláthová, V., Hurníková, Z., Majláth, I. and Petko, B. (2007). Hepatozoon canis infection in Slovakia: imported or autochthonous? Vector Borne Zoonotic Diseases 7, 199–202.Google Scholar
Marié, J. L., Davoust, B., Socolovschia, C., Mediannikova, O., Roqueplo, C., Beaucournu, J. C., Raoult, D. and Parola, P. (2012). Rickettsiae in arthropods collected from red foxes (Vulpes vulpes) in France. Comparative Immunology, Microbiology and Infectious Diseases 35, 59–62.CrossRefGoogle ScholarPubMed
Markowicz, M., Schötta, A. M., Wijnveld, M. and Stanek, G. (2016). Human granulocytic anaplasmosis acquired in Connecticut, USA, diagnosed in Vienna, Austria, 2015. Diagnostic Microbiology and Infectious Disease 84, 347–349.CrossRefGoogle ScholarPubMed
Millán, J., Ferroglio, E. and Solano-Gallego, L. (2014). Role of wildlife in the epidemiology of Leishmania infantum infection in Europe. Parasitology Research 113, 2005–2014.CrossRefGoogle ScholarPubMed
Miró, G., Checa, R., Paparini, A., Ortega, N., González-Fraga, J. L., Gofton, A., Bartolomé, A., Montoya, A., Gálvez, R., Mayo, P. P. and Irwin, P. (2015). Theileria annae (syn. Babesia microti-like) infection in dogs in NW Spain detected using direct and indirect diagnostic techniques: clinical report of 75 cases. Parasites and Vectors 8, 217.CrossRefGoogle ScholarPubMed
Miterpáková, M., Komjáti-Nagyová, M., Hurníková, Z. and Víchová, B. (2017). Retrospective molecular study on canine hepatozoonosis in Slovakia – does infection risk for dogs really exist? Ticks and Tick-borne Diseases 8, 567–573.Google Scholar
Mitková, B., Hrazdilová, K., Steinbauer, V., D'Amico, G., Mihalca, A. D. and Modrý, D. (2016). Autochthonous Hepatozoon infection in hunting dogs and foxes from the Czech Republic. Parasitology Research 115, 4167–4171.Google Scholar
Modrý, D., Beck, R., Hrazdilová, K. and Baneth, G. (2017). A review of methods for detection of Hepatozoon infection in carnivores and arthropod vectors. Vector-Borne and Zoonotic Diseases 17, 66–72.CrossRefGoogle ScholarPubMed
Murata, T., Inoue, M., Tateyama, S., Taura, Y. and Nakama, S. (1993). Vertical transmission of Hepatozoon canis in dogs. The Journal of Veterinary Medical Science 55, 867–868.Google Scholar
Obwaller, A. G., Karakus, M., Poeppl, W., Töz, S., Özbel, Y., Aspöck, H. and Walochnik, J. (2016). Could Phlebotomus mascittii play a role as a natural vector for Leishmania infantum? New data. Parasites and Vectors 9, 458.Google Scholar
Otranto, D., Cantacessi, C., Pfeffer, M., Dantas-Torres, F., Brianti, E., Deplazes, P., Genchi, C., Guberti, V. and Capelli, G. (2015). The role of wild canids and felids in spreading parasites to dogs and cats in Europe: Part I: protozoa and tick-borne agents. Veterinary Parasitology 213, 12–23.CrossRefGoogle ScholarPubMed
Penezić, A., Selaković, S., Pavlović, I. and Ćirović, D. (2014). First findings and prevalence of adult heartworms (Dirofilaria immitis) in wild carnivores from Serbia. Parasitology Research 9, 3281–3285.Google Scholar
Petrovec, M., Sumner, J. W., Nicholson, W. L., Childs, J. E., Strle, F., Barlic, J., Lotric-Furlan, S. and Avsic Zupanc, T. (1999). Identity of ehrlichial DNA sequences derived from Ixodes ricinus ticks with those obtained from patients with human granulocytic ehrlichiosis in Slovenia. Journal of Clinical Microbiology 37, 209–210.CrossRefGoogle ScholarPubMed
Silbermayr, K., Eigner, B., Joachim, A., Duscher, G. G., Seidel, B., Allerberger, F., Indra, A., Hufnagl, P. and Fuehrer, H-P. (2014). Autochthonous Dirofilaria repens in Austria. Parasites and Vectors 7, 226.CrossRefGoogle ScholarPubMed
Tolnai, Z., Széll, Z., Sproch, Á., Szeredi, L. and Sréter, T. (2014). Dirofilaria immitis: an emerging parasite in dogs, red foxes and golden jackals in Hungary. Veterinary Parasitology 203, 339–342.Google Scholar
Tolnai, Z., Sréter-Lancz, Z. and Sréter, T. (2015). Spatial distribution of Anaplasma phagocytophilum and Hepatozoon canis in red foxes (Vulpes vulpes) in Hungary. Ticks and Tick Borne Diseases 6, 645–648.Google Scholar
Torina, A., Blanda, V., Antoci, F., Scimeca, S., D'Agostino, R., Scariano, E., Piazza, A., Galluzzo, P., Giudice, E. and Caracappa, S. (2013). A molecular survey of Anaplasma spp., Rickettsia spp., Ehrlichia canis and Babesia microti in foxes and fleas from Sicily. Transboundering and Emerging Diseases 60, 125–130.Google Scholar
Vitorino, L., Zé-zé, L., Sousa, A., Bacellar, F. and Tenreiro, R. (2003). rRNA intergenic spacer regions for phylogenetic analysis of Rickettsia species. Annals of the New York Academy of Sciences 990, 726–733.Google Scholar
Zahler, M., Rinder, H., Schein, E. and Gothe, R. (2000). Detection of a new pathogenic Babesia microti-like species in dogs. Veterinary Parasitology 89, 241–248.Google Scholar
Zanet, S., Trisciuoglio, A., Bottero, E., de Mera, I. G. F., Gortazar, C., Carpignano, M. G. and Forroglio, E. (2014). Piroplasmosis in wildlife: Babesia and Theileria affecting free-ranging ungulates and carnivores in the Italian Alps. Parasites and Vectors 7, 70.Google Scholar
Zemtsova, G. E., Montgomery, M. and Levin, M. L. (2015). Relative sensitivity of conventional and real-time PCR assays for detection of SFG Rickettsia in blood and tissue samples from laboratory animals. PLoS ONE 21, e0116658.Google Scholar
Zintl, A., Finnerty, E. J., Murphy, T. M., de Waal, T. and Gray, J. S. (2011). Babesias of red deer (Cervus elaphus) in Ireland. Veterinary Research 42, 7.Google Scholar