Wild canids as hosts for ticks and tick-borne zoonotic pathogens in Serbia

Main Article Content

Ratko Sukara
Darko Mihaljica
Gorana Veinović
Duško Ćirović
Snežana Tomanović

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

Download data is not yet available.

Article Details

How to Cite
Sukara, R., Mihaljica, D., Veinović, G., Ćirović, D., & Tomanović, S. (2020). Wild canids as hosts for ticks and tick-borne zoonotic pathogens in Serbia. Veterinarski Glasnik, 74(2), 144-153. https://doi.org/10.2298/VETGL200810017S
Section
Mini Review

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

Most read articles by the same author(s)