Wild canids as hosts for ticks and tick-borne zoonotic pathogens in Serbia
Main Article Content
Abstract
Wild canids are recognized as important reservoir hosts for several vector-borne
pathogens and are a good sentinel species for epidemiological surveillance. Identifying
the reservoir hosts for particular zoonotic pathogens in a specific area enables the
implementation of adequate measures in order to prevent the occurrence of zoonotic
diseases in humans and domestic animals. The present review aims to summarize the
role of wild canids in the epidemiology of tick-borne zoonoses in Serbia based on
previously published papers and to discuss the available data from an epidemiological
point of view. The results of previously published studies indicate that wild canids
are potential reservoir hosts for several zoonotic tick-borne pathogens in Serbia, and
hosts for several tick species which are proven competent vectors. Based on molecular
studies conducted so far, the presence of Anaplasma phagocytophilum, was confirmed in
jackals while the presence of Candidatus Neoehrlichia micurensis (FU98), Borrelia burgdorferi
sensu stricto, Borrelia garinii, and Borrelia lusitaniae was proven by PCR in analyzed red
foxes. There is a need for continuous epidemiological monitoring of diseases caused
by pathogens previously confirmed in wild canids. Also, further research is needed to
reveal the role of other wild and domestic animals in the epidemiology of tick-borne
zoonoses in Serbia.
Downloads
Article Details
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors retain copyright of the published papers and grant to the publisher the right to publish the article, to be cited as its original publisher in case of reuse, and to distribute it in all forms and media. Articles will be distributed under the Creative Commons Attribution International License (CC BY 4.0).
References
Aguirre A. A., 2009. Wild canids as sentinels of ecological health: a conservation medicine
perspective. Parasites vectors, 2, S7. https://doi.org/10.1186/1756-3305-2-S1-S7
Arsić B., Gligić A., Ristanović E., Lako B., Potkonjak A., Peruničić M., Pavlović M. 2014. A
case of human monocytic ehrlichiosis in Serbia. Srpski Arhiv za Celokupno Lekarstvo, 142,
–82. https://doi.org/10.2298/SARH1402079A
Ćakić S., Veinović G., Cerar T., Mihaljica D., Sukara R., Ružić-Sabljić E., Tomanović S. 2019.
Diversity of Lyme borreliosis spirochetes isolated from ticks in Serbia. Medical and
Veterinary Entomology, 33, 512–520. https://doi.org/10.1111/mve.12392
Cézanne R., Mrowietz N., Eigner B., Duscher G. G., Glawischnig W., Fuehrer H. P., 2017.
Molecular analysis of Anaplasma phagocytophilum and Babesia divergens in red deer
(Cervus elaphus) in Western Austria. Molecular and Cellular Probes, 31, 55–58. https://
doi.org/10.1016/j.mcp.2016.07.003
Ćirović D. 2000. Morphological variability and biogeorarphical status of the red fox populations
(Vulpes vulpes Linnaeus, 1758) in Vojvodina. Faculty of Biology University of Belgrade.
Ćirović D., Penezić A., Plećaš M. 2018. Šakal (Canis aureus) u predelima sa dominantnim
antropogenim uticajem, in: Pokorny, B., Kmetec, U. (Eds.), 10. Slovenski lovski dan, Šakal
v Sloveniji in Na Balkanu:Stanje in Upravljavski Izzivi. Lovska zveza Slovenije, Koper, 6.
oktobar 2018, pp. 13–14.
Dantas-Torres F. 2015. Climate change, biodiversity, ticks and tick-borne diseases: The butterfly
effect. International Journal for Parasitology: Parasites and Wildlife, 4, 452–461. https://
doi.org/10.1016/j.ijppaw.2015.07.001
Đokić M., Čurčić P., Nožić D., Lako B., Begović V., Rajić-Dimitrijević R., Hristović D. 2006.
Humana erlihioza. Vojnosanitetski pregled, 63, 403–408.
Dumitrache M. O., Matei I. A., Ionică A. M., Kalmár Z., D’Amico G., Sikó-Barabási S.,
Ionescu D. T., Gherman C. M., Mihalca A. D. 2015. Molecular detection of Anaplasma
phagocytophilum and Borrelia burgdorferi sensu lato genospecies in red foxes (Vulpes
vulpes) from Romania. Parasites & Vectors, 8, 514. https://doi.org/10.1186/s13071-015-
-9
Dumler J. S. 2005. Anaplasma and Ehrlichia infection. Annals of the New York Academy of
Sciences, 1063, 361–373. https://doi.org/10.1196/annals.1355.069
Ebani V. V., Verin R., Fratini F., Poli A., 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. https://doi.org/10.7589/0090-3558-47.3.699
Franke J., Hildebrandt A., Dorn W. 2013. Exploring gaps in our knowledge on Lyme borreliosis
spirochaetes - Updates on complex heterogeneity, ecology, and pathogenicity. Ticks and
Tick-borne Diseases, 4, 11–25. https://doi.org/10.1016/j.ttbdis.2012.06.007
Gern L. 2009. Life Cycle of Borrelia burgdorferi sensu lato and Transmission to Humans.
Current Problems in Dermatology, 37, 18-30. https://doi.org/10.1159/000213068
Gherman C. M., Mihalca A. D. 2017. A synoptic overview of golden jackal parasites reveals
high diversity of species. Parasites and Vectors, 10, 1–40. https://doi.org/10.1186/s13071-
-2329-8
Heidrich J., Schönberg A., Steuber S., Nöckler K., Schulze P., Voigt W. P., Schein E. 1999.
Investigation of skin samples from Red Foxes (Vulpes vulpes) in Eastern Brandenburg
(Germany) for the detection of Borrelia burgdorferi s. l. Zentralblatt für Bakteriologie, 289,
–672. https://doi.org/10.1016/S0934-8840(99)80026-7
Hildebrand J., Buńkowska-Gawlik K., Adamczyk M., Gajda E., Merta D., Popiołek M., Perec-
Matysiak A. 2018. The occurrence of Anaplasmataceae in European populations of
invasive carnivores. Ticks and Tick-borne Diseases, 9, 934–937. https://doi.org/10.1016/j.
ttbdis.2018.03.018
Hodžić A., Cézanne R., Duscher G. G., Harl J., Glawischnig W., Fuehrer H. P. H. P. 2015.
Candidatus Neoehrlichia sp. in an Austrian fox is distinct from Candidatus Neoehrlichia
mikurensis, but closer related to Candidatus Neoehrlichia lotoris. Parasites and Vectors, 8,
https://doi.org/10.1186/s13071-015-1163-0
Hodžić A., Mitkovà B., Modrý D., Juránková J., Frgelecová L., Forejtek P., Steinbauer V.,
Duscher G. G. 2017. A new case of the enigmatic Candidatus Neoehrlichia sp. (FU98)
in a fox from the Czech Republic. Molecular and Cellular Probes, 31, 59–60. https://doi.
org/10.1016/j.mcp.2016.02.005
Hornok S., Horváth G., Takács N., Farkas R., Szőke K., Kontschán J. 2018. Molecular evidence
of a badger-associated Ehrlichia sp., a Candidatus Neoehrlichia lotoris-like genotype and
Anaplasma marginale in dogs. Ticks and Tick-borne Diseases, 9, 1302–1309. https://doi.
org/10.1016/j.ttbdis.2018.05.012
Hornok S., Sándor A. D., Beck R., Farkas R., Beati L., Kontschán J., Takács N., Földvári G.,
Silaghi C., Meyer-Kayser E., Hodžić A., Tomanović S., Abdullah S., Wall R., Estrada-
Peña A., Duscher G. G., Plantard O. 2017a. Contributions to the phylogeny of Ixodes
(Pholeoixodes) canisuga, I. (Ph.) kaiseri, I. (Ph.) hexagonus and a simple pictorial key for the identification of their females. Parasites and Vectors, 10, 1–12. https://doi.org/10.1186/
s13071-017-2424-x
Hornok S., Trauttwein K., Takács N., Hodžić A., Duscher G. G., Kontschán J. 2017b. 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.
https://doi.org/10.1016/j.ttbdis.2016.09.014
Hulinska D., Langrova K., Pejcoch M., Pavlasek I. 2004. Detection of Anaplasma
phagocytophilum in animals by real-time polymerase chain reaction. Apmis, 112, 239–247.
https://doi.org/10.1111/j.1600-0463.2004.apm11204-0503.x
Karbowiak G., Víchová B., Majláthová V., Hapunik J., Pet’ko B. 2009. Anaplasma
phagocytophilum infection of red foxes (Vulpes vulpes). Annals of Agricultural and
Environmental Medicine, 16, 299–300.
Kovačević Filipović M. M., Beletić A. D., Ilić Božović A. V., Milanović Z., Tyrrell P., Buch J.,
Breitschwerdt E. B., Birkenheuer A. J., Chandrashekar R. 2018. Molecular and Serological
Prevalence of Anaplasma phagocytophilum, A. platys, Ehrlichia canis, E. chaffeensis,
E. ewingii, Borrelia burgdorferi, Babesia canis, B. gibsoni and B. vogeli among Clinically
Healthy Outdoor Dogs in Serbia. Veterinary Parasitology: Regional Studies and Reports,
, 117–122. https://doi.org/10.1016/j.vprsr.2018.10.001
Leschnik M., Kirtz G., Virányi Z., Wille-Piazzai W., Duscher G. 2012. Acute granulocytic
anaplasmosis in a captive timber wolf (Canis lupus occidentalis). Journal of Zoo and
Wildlife Medicine, 43, 645–648. doi:10.1638/2011-0224R.1
Liebisch G., Dimpfl B., Finkbeiner-Weber B., Liebisch A., Frosch M. 1995. The red fox (Vulpes
vulpes) a reservoir competent host for Borrelia burgdorferi sensu lato, in: Int. Conf. Tick-
Host-Pathogen Interactions. Kruger National Park, South Africa, p. 238.
Medlock J. M., Hansford K. M., Bormane A., Derdakova M., Estrada-peña A., George J.,
Golovljova I., Jaenson T. G. T., Jensen J., Jensen P. M., Kazimirova M., Oteo J. A., Papa A.,
Pfister K., Plantard O., Randolph S. E. 2013. Driving forces for changes in geographical
distribution of Ixodes ricinus ticks in Europe. Parasites & Vectors, 6:1. https://doi.
org/10.1186/1756-3305-6-1
Milutinović M., Masuzawa T., Tomanović S., Radulović Ž., Fukui T., Okamoto Y. 2008.
Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum, Francisella tularensis and
their co-infections in host-seeking Ixodes ricinus ticks collected in Serbia. Experimental
and Applied Acarology, 45, 171–183. https://doi.org/10.1007/s10493-008-9166-6
Milutinovic M., Petrovic Z., Bobic B., Pavlovic I. 1996. Ecological notes on ticks (Acari:
Ixodidae) collected in West Serbia, Yugoslavia. Parasitologia Hungarica, 29–30, 67–74.
Negev M., Paz S., Clermont A., Pri-Or N. G., Shalom U., Yeger T., Green M. S. 2015. Impacts
of climate change on vector borne diseases in the Mediterranean basin — implications for
preparedness and adaptation policy. International Journal of Environmental Research and
Public Health, 12, 6745–6770. https://doi.org/10.3390/ijerph120606745
Obrenović S., Ristanović E., Čekanac R., Radulović Ž., Ilić V. 2015. Seroprevalence of IgG
antibodies against Borrelia burgdorferi in dogs in Belgrade area, Serbia. Acta Veterinaria,
, 99–110. https://doi.org/10.1515/acve-2015-0008
Pavlović I., Milutinović M., Radulović Ž. 2001. Fauna artropoda ektoparazita lisica (Vulpes
vulpes L.) u Srbiji, in: Zbornik Rezimea Skupa Entomologa Srbije. Goč, p. 45.
Potkonjak A., Gutiérrez R., Savić S., Vračar V., Nachum-Biala Y., Jurišić A., Kleinerman G.,
Rojas A., Petrović A., Baneth G., Harrus S. 2016. Molecular detection of emerging tick borne pathogens in Vojvodina, Serbia. Ticks and Tick-borne Diseases, 7, 199–203. https://
doi.org/10.1016/j.ttbdis.2015.10.007
Potkonjak A., Savić S., Vračar V., Rnjak D., Tikvički M., Obrenović S., Lako B. 2013. Prevalence
of G class antibodies to antigens of Lyme disease causes in dogs in Vojvodina, Serbia.
Veterinarski glasnik, 67, 55–66. https://doi.org/10.2298/VETGL1302055P
Potkonjak A., Vračar V., Savić S., Lako B., Radosavljević V., Cincović M., Suvajdžić L., Jurišić
A., Petrović A. 2015. The seroprevalence of Anaplasma phagocytophilum infection in dogs
in the Autonomous Province of Vojvodina, Serbia. Veterinarski Arhiv, 85, 385–394.
Stojanov I., Pušić I., Pavlović I., Prodanov Radulović J., Miloš K., Ratajac R. 2014. Findings
of ticks in some species of wild carnivores. 3rd International Symposium on Hunting, »
Мodern aspects of sustainable management of game populations« 26–28.
Stuen S., Granquist E. G., Silaghi C. 2013. Anaplasma phagocytophilum—a widespread
multi-host pathogen with highly adaptive strategies. Frontiers in Cellular and Infection
Microbiology, 3, 1–33. https://doi.org/10.3389/fcimb.2013.00031
Sukara R., Chochlakis D., Ćirović D., Penezić A., Mihaljica D., Ćakić S., Valčić M., Tselentis
Y., Psaroulaki A., Tomanović S. 2018. Golden jackals (Canis aureus) as hosts for ticks and
tick-borne pathogens in Serbia. Ticks and Tick-borne Diseases, https://doi.org/10.1016/j.
ttbdis.2018.04.003
Sukara R., Juwaid S., Ćirović D., Penezić A., Mihaljica D., Veinović G., Radojičić S., Hodžić
A., Duscher G. G., Tomanović S. 2019. Candidatus Neoehrlichia sp. (FU98) and Borrelia
burgdorferi Sensu Lato in Red Foxes (Vulpes vulpes) from Serbia. Acta Veterinaria, 69,
–324. https://doi.org/10.2478/acve-2019-0026
Tomanović S., Chochlakis D., Radulović Ž., Milutinović M., Ćakić S., Mihaljica D., Tselentis Y.,
Psaroulaki A. 2013a. Analysis of pathogen co-occurrence in host-seeking adult hard ticks
from Serbia. Experimental and Applied Acarology, 59, 367–376. https://doi.org/10.1007/
s10493-012-9597-y
Tomanović S., Milutinović M., Fukui T., Radulović Ž., Okamoto Y., Masuzawa T. 2008.
Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum, Francisella tularensis and
their co-infections in host-seeking Ixodes ricinus ticks collected in Serbia. Experimental
and Applied Acarology, 45, 171–183. https://doi.org/10.1007/s10493-008-9166-6
Tomanović S., Radulović Ž., Ćakić S., Mihaljica D., Sukara R., Penezić A., Burazerović J.,
Ćirović D. 2013b. Tick species (acari: Ixodidae) of red foxes (Vulpes vulpes) in Serbia, in:
nd International Symposium on Hunting “modern Aspects of Sustainable Management
of Game“. University of Novi Sad, Faculty of Agriculture, Novi Sad, pp. 229–235.
Tomassone L., Berriatua E., De Sousa R., Duscher G. G., Mihalca A. D., Silaghi C., Sprong
H., Zintl A. 2018. Neglected vector-borne zoonoses in Europe: Into the wild. Veterinary
Parasitology, 251, 17–26. https://doi.org/10.1016/j.vetpar.2017.12.018
Trouwborst A., Krofel M., Linnell J. D. C. 2015. Legal implications of range expansions in a
terrestrial carnivore: the case of the golden jackal (Canis aureus) in Europe. Biodiversity
and Conservation, 24, 2593–2610. https://doi.org/10.1007/s10531-015-0948-y
Vasić A., Nieder M., Zdravković N., Bojkovski J., Bugarski D., Pavlović I., Silaghi C. 2018. Tick
infestation and occurrence of Anaplasma phagocytophilum and piroplasms in cattle in
the Republic of Serbia. Parasitology Research, 117, 1813–1818. https://doi.org/10.1007/
s00436-018-5867-x