Wild small mammals and ticks play an important role in maintaining and spreading zoonoses in nature, as well as in captive animals. The aim of this study was to monitor selected agents with zoonotic potential in their reservoirs and vectors in a zoo, and to draw attention to the risk of possible contact with these pathogens. In total, 117 wild small mammals (rodents) and 166 ticks were collected in the area of Brno Zoo. Antibodies to the bacteria Coxiella burnetii, Francisella tularensis, and Borrelia burgdorferi s.l. were detected by a modified enzyme-linked immunosorbent assay in 19% (19/99), 4% (4/99), and 15% (15/99) of rodents, respectively. Antibodies to Leptospira spp. bacteria were detected by the microscopic agglutination test in 6% (4/63) of rodents. Coinfection (antibodies to more than two agents) were proved in 14.5% (15/97) of animals. The prevalence of C. burnetii statistically differed according to the years of trapping (p = 0.0241). The DNAs of B. burgdorferi s.l., Rickettsia sp., and Anaplasma phagocytophilum were detected by PCR in 16%, 6%, and 1% of ticks, respectively, without coinfection and without effect of life stage and sex of ticks on positivity. Sequencing showed homology with R. helvetica and A. phagocytophilum in four and one positive samples, respectively. The results of our study show that wild small mammals and ticks in a zoo could serve as reservoirs and vectors of infectious agents with zoonotic potential and thus present a risk of infection to zoo animals and also to keepers and visitors to a zoo.

Department of Animal Physiology and Immunology Faculty of Science Masaryk University Poříčí 7 9 63900 Brno Czech Republic

Department of Biology and Wildlife Diseases Faculty of Veterinary Hygiene and Ecology University of Veterinary Sciences Brno Palackého tř 1946 1 61242 Brno Czech Republic

Department of Biology Faculty of Education Masaryk University Poříčí 7 9 63900 Brno Czech Republic

Department of Infection Disease and Microbiology Faculty of Veterinary Medicine University of Veterinary Sciences Brno Palackého tř 1946 1 61242 Brno Czech Republic

Department of Kinesiology Faculty of Sports Studies Masaryk University Kamenice 753 5 62500 Brno Czech Republic

Department of Mathematics and Statistics Faculty of Science Masaryk University Kotlářská 2 61137 Brno Czech Republic

Department of Virology and Serology State Veterinary Institute Prague Sídlištní 136 24 16503 Prague Czech Republic

Zobrazit více v PubMed

Gürtler L., Bauerfeind U., Blümel J., Burger R., Drosten C., Gröner A., Heiden M., Hildebrandt M., Jansen B., Offergeld R., et al. Coxiella burnetiid—pathogenic agent of Q (Query) fever. Transfus. Med. Hemoth. 2014;41:60–72. PubMed PMC

Maurin M., Raoult D. Q fever. Clin. Microbiol. Rev. 1999;12:518–553. doi: 10.1128/CMR.12.4.518. PubMed DOI PMC

Hennebique A., Boisset S., Maurin M. Tularemia as a waterborne disease: A review. Emerg. Microbes Infect. 2019;8:1027–1042. doi: 10.1080/22221751.2019.1638734. PubMed DOI PMC

Britannica, The Editors of Encyclopaedia Tularemia. Encyclopedia Britannica, 6 August 2020. [(accessed on 3 June 2021)]; Available online: https://www.britannica.com/science/tularemia.

Bertasio C., Papetti A., Scaltriti E., Tagliabue S., D’Incau M., Boniotti M.B. Serological survey and molecular typing reveal new Leptospira serogroup pomona strains among pigs of Northern Italy. Pathogens. 2020;9:332. doi: 10.3390/pathogens9050332. PubMed DOI PMC

Bharti A.R., Nally J.E., Ricaldi J.N., Matthias M.A., Diaz M.M., Lovett M.A., Levett P.N., Gilman R.H., Willig M.R., Gotuzzo E., et al. Peru-United States Leptospirosis Consortium. Leptospirosis: A zoonotic disease of global importance. Lancet Infect. Dis. 2003;3:757–771. doi: 10.1016/S1473-3099(03)00830-2. PubMed DOI

Grennan D. Leptospirosis. JAMA. 2019;321:812. doi: 10.1001/jama.2019.0697. PubMed DOI

Krawczyk A.I., van Duijvendijk G.L.A., Swart A., Heylen D., Jaarsma R.I., Jacobs F.H.H., Fonville M., Sprong H., Takken W. Effect of rodent density on tick and tick-borne pathogen populations: Consequences for infectious disease risk. Parasites Vectors. 2020;13:34. doi: 10.1186/s13071-020-3902-0. PubMed DOI PMC

Lernout T., De Regge N., Tersago K., Fonville M., Suin V., Sprong H. Prevalence of pathogens in ticks collected from humans through citizen science in Belgium. Parasites Vectors. 2019;12:550. doi: 10.1186/s13071-019-3806-z. PubMed DOI PMC

Gross L. A new view on Lyme disease: Rodents hold the key to annual risk. PLoS Biol. 2006;4:182. doi: 10.1371/journal.pbio.0040182. PubMed DOI PMC

Steere A.C., Strle F., Wormser G.P., Hu L.T., Branda J.A., Hovius J.W.R., Li X., Mead P.S. Lyme borreliosis. Nat. Rev. Dis. Primers. 2016;2:16090. doi: 10.1038/nrdp.2016.90. PubMed DOI PMC

Borawski K., Dunaj J., Czupryna P., Pancewicz S., Świerzbińska R., Żebrowska A., Moniuszko-Malinowska A. Prevalence of spotted fever group rickettsia in North-Eastern Poland. Infect. Dis. 2019;51:810–814. doi: 10.1080/23744235.2019.1660800. PubMed DOI

Raoult D., Roux V. Rickettsioses as paradigms of new or emerging infectious diseases. Clin Microbiol Rev. 1997;10:694–719. doi: 10.1128/CMR.10.4.694. PubMed DOI PMC

Matei I.A., Estrada-Peña A., Cutler S.J., Vayssier-Taussat M., Varela-Castro L., Potkonjak A., Zeller H., Mihalca A.D. A review on the eco-epidemiology and clinical management of human granulocytic anaplasmosis and its agent in Europe. Parasites Vectors. 2019;12:599. doi: 10.1186/s13071-019-3852-6. PubMed DOI PMC

Ismail N., Bloch K.C., McBride J.W. Human ehrlichiosis and anaplasmosis. Clin. Lab. Med. 2010;30:261–292. doi: 10.1016/j.cll.2009.10.004. PubMed DOI PMC

Bártová E., Kučerová H.L., Žákovská A., Budíková M., Nejezchlebová H. Coxiella burnetii and Francisella tularensis in wild small mammals from the Czech Republic. Ticks Tick-Borne Dis. 2020;11:101350. doi: 10.1016/j.ttbdis.2019.101350. PubMed DOI

Meredith A.L., Cleaveland S.C., Denwood M.J., Brown J.K., Shaw D.J. Coxiella burnetii (Q Fever) seroprevalence in prey and predators in the United Kingdom: Evaluation of infection in wild rodents, foxes and domestic cats using a modified ELISA. Transbound. Emerg. Dis. 2015;62:639–649. doi: 10.1111/tbed.12211. PubMed DOI

Bielawska-Drózd A., Cieślik P., Żakowska D., Głowacka P., Wlizło-Skowronek B., Ziȩba P., Zdun A. Detection of Coxiella burnetii and Francisella tularensis in tissues of wild-living animals and in ticks of North-West Poland. Pol. J. Microbiol. 2018;67:529–534. doi: 10.21307/pjm-2018-059. PubMed DOI PMC

Dorko E., Rimarova K., Pilipinec E., Travnicek M. Prevalence of Coxiella burnetii antibodies in wild ruminants in Kavecany ZOO, Kosice, eastern Slovakia. Ann. Agr. Env. Med. 2009;16:321–324. PubMed

Otto P., Chaignat V., Klimpel D., Diller R., Melzer F., Muller W., Tomaso H. Serological investigation of wild boars (Sus scrofa) and red foxes (Vulpes vulpes) asindicator animals for circulation of Francisella tularensis in Germany. Vector-Borne Zoonotic Dis. 2014;14:46–51. doi: 10.1089/vbz.2013.1321. PubMed DOI PMC

Rossow H., Sissonen S., Koskela K.A., Kinnunen P.M., Hemmila H., Niemimaa J., Huitu O., Kuusi M., Vapalahti O., Henttonen H., et al. Detection of Francisella tularensis in voles in Finland. Vector Borne Zoonotic Dis. 2014;14:193–198. doi: 10.1089/vbz.2012.1255. PubMed DOI PMC

Pascucci L., Di Domenico M., Dall’Acqua F., Sozio G., Cammà C. Detection of lyme disease and Q fever agents in wild rodents in central Italy. Vector-Borne Zoonotic. 2015;15:404–411. doi: 10.1089/vbz.2015.1807. PubMed DOI PMC

Schmidt S., Essbauer S.S., Mayer-Scholl A., Poppert S., Schmidt-Chanasit J., Klempa B., Henning K., Schares G., Groschup M., Spitzenberger F., et al. Multiple infections of rodents with zoonotic pathogens in Austria. Vector-Borne Zoonotic. 2014;14:467–475. doi: 10.1089/vbz.2013.1504. PubMed DOI PMC

State Health Institute Data. [(accessed on 20 April 2021)]; Available online: www.uzis.cz/en/about-us.

Vostal K., Žákovská A. Two-year study of examination of blood from wild rodents for the presence of antiborrelian antibodies. Ann. Agric. Environ. Med. 2003;10:203–206. PubMed

Kybicová K., Kurzová Z., Hulínská D. Molecular and serological evidence of Borrelia burgdorferi sensu lato in wild rodents in the Czech Republic. Vector-Borne Zoonotic. 2008;8:645–652. doi: 10.1089/vbz.2007.0249. PubMed DOI

Kučerová H.L., Žákovská A., Marková J., Bártová E. Detection of antibodies to Borrelia burgdorferi s.l. in wild small mammals and sensitivity of PCR and cultivation. Vet. Microbiol. 2019;230:241–243. doi: 10.1016/j.vetmic.2019.02.004. PubMed DOI

Štefančíková A., Bhide M., Peťko B., Stanko M., Mošanský L., Fričova J., Derdáková M., Trávniček M. Anti-Borrelia antibodies in rodents: Important hosts in ecology of Lyme disease. Ann. Agric. Environ. Med. 2004;11:209–213. PubMed

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

Širmarová J., Tichá L., Golovchenko M., Salát J., Grubhoffer L., Rudenko N., Nowotny N., Růžek D. Seroprevalence of Borrelia burgdorferi sensu lato and tick-borne encephalitis virus in zoo animal species in the Czech Republic. Ticks Tick-Borne Dis. 2014;5:523–527. doi: 10.1016/j.ttbdis.2014.03.008. PubMed DOI

Stoebel K., Schoenberg A., Streich W.J. The seroepidemiology of Lyme borreliosis in zoo animals in Germany. Epidemiol. Infect. 2003;131:975–983. doi: 10.1017/S0950268803008896. PubMed DOI PMC

Stanko M., Prokopcáková H., Fricová J., Pet’ko B. Leptospira antibodies in small mammals in Eastern Slovakia. Vet. Med. 1996;41:373–377. PubMed

Boey K., Shiokawa K., Rajeev S. Leptospira infection in rats: A literature review of global prevalence and distribution. PLoS Negl. Trop. Dis. 2019;13:e0007499. doi: 10.1371/journal.pntd.0007499. PubMed DOI PMC

Beest J.T., Cushing A., McClean M., Hsu W., Bildfell R. Disease surveillance of California Ground Squirrels (Spermophilus beecheyi) in a Drive-through Zoo in Oregon, USA. J. Wildl. Dis. 2017;53:667–670. doi: 10.7589/2016-05-119. PubMed DOI

Himsworth C.G., Jardine C.M., Parsons K.L., Feng A.Y.T., Patrick D.M. The characteristics of wild rat (Rattus spp.) populations from an inner-city neighborhood with a focus on factors critical to the understanding of rat-associated zoonoses. PLoS ONE. 2014 doi: 10.1371/journal.pone.0091654. PubMed DOI PMC

Derdáková M., Beati L., Pet’ko B., Stanko M., Fish D. Genetic variability within Borrelia burgdorferi sensu lato genospecies established by PCR-single-strand conformation polymorphism analysis of the rrfA-rrlB intergenic spacer in Ixodes ricinus ticks from the Czech Republic. Appl. Environ. Microb. 2003;69:509–516. doi: 10.1128/AEM.69.1.509-516.2003. PubMed DOI PMC

Hönig V., Svec P., Halas P., Vavruskova Z., Tykalova H., Kilian P., Vetiskova V., Dornakova V., Sterbova J., Simonova Z., et al. Ticks and tick-borne pathogens in South Bohemia (Czech Republic)—Spatial variability in Ixodes ricinus abundance, Borrelia burgdorferi and tick-borne encephalitis virus prevalence. Ticks Tick-Borne Dis. 2015;6:559–567. doi: 10.1016/j.ttbdis.2015.04.010. PubMed DOI

Žákovská A., Nejezchlebová H., Bartoňková N., Rašovská T., Kučerová H.L., Norek A., Ovesná P. Activity of the tick Ixodes ricinus monitored in a suburban park in Brno, Czech Republic, in association with the evaluation of selected repellents. J. Vector. Ecol. 2013;38:295–300. doi: 10.1111/j.1948-7134.2013.12043.x. PubMed DOI

Venclikova K., Rudolf I., Mendel J., Betasova L., Hubalek Z. Rickettsiae in questing Ixodes ricinus ticks in the Czech Republic. Ticks Tick-Borne Dis. 2014;5:135–138. doi: 10.1016/j.ttbdis.2013.09.008. PubMed DOI

Hönig V., Carolan H.E., Vavruskova Z., Massire C., Mosel M.R., Crowder C.D., Rounds M.A., Ecker D.J., Ruzek D., Grubhoffer L., et al. Broad-range survey of vector-borne pathogens and tick host identification of Ixodes ricinus from Southern Czech Republic. FEMS Microbiol. Ecol. 2017;93:fix129. doi: 10.1093/femsec/fix129. PubMed DOI PMC

Svitálková Z., Haruštiaková D., Mahríková L., Berthová L., Slovák M., Kocianová E., Kazimírová M. Anaplasma phagocytophilum prevalence in ticks and rodents in an urban and natural habitat in South-Western Slovakia. Parasites Vectors. 2015;8 doi: 10.1186/s13071-015-0880-8. PubMed DOI PMC

Žákovská A., Rusňáková H., Vostal K. Host response to Borrelia afzelii in BALB/c mice tested by immunoblotting. Ann. Agric. Environ. Med. 2013;20:823–825. PubMed

Shropshire S.B., Veir J.K., Morris A.K., Lappin M.R. Evaluation of Leptospira species microscopic agglutination test in experimentally vaccinated cats and Leptospira species seropositivity in aged azotemic client-owned cats. J. Feline Med. Surg. 2016;18:768–772. doi: 10.1177/1098612X15593902. PubMed DOI PMC

O’Rourke M., Traweger A., Lusa L., Stupica D., Maraspin V., Barrett P.N., Strle F., Livey I. Quantitative detection of Borrelia burgdorferi sensu lato in erythema migrans skin lesions using internally controlled duplex real time PCR. PLoS ONE. 2013;8:e63968. doi: 10.1371/journal.pone.0063968. PubMed DOI PMC

Labruna M.B., Whitworth T., Horta M.C., Bouyer D.H., McBride J.W., Pinter A., Popov V., Gennari S.M., Walker D.H. Rickettsia species infecting Amblyomma cooperi ticks from an area in the state of São Paulo, Brazil, where Brazilian spotted fever is endemic. J. Clin. Microbiol. 2004;42:90–98. doi: 10.1128/JCM.42.1.90-98.2004. PubMed DOI PMC

Massung R.F., Slater K., Owens J.H., Nicholson W.L., Mather T.N., Solberg V.B., Olson J.G. Nested PCR assay for detection of granulocytic Ehrlichiae. J. Clin. Microbiol. 1998;36:1090–1095. doi: 10.1128/JCM.36.4.1090-1095.1998. PubMed DOI PMC

STATISTICA (Data Analysis Software System), Version 12; Statsoft Inc.: Tulsa, OK, USA, 2013. [(accessed on 6 June 2000)]; Available online: www.statsoft.com.