Bats may carry various viruses and bacteria which can be harmful to humans, but little is known about their role as a parasitic source with zoonotic potential. The aim of this study was to test wild bats for the presence of selected parasites: Toxoplasma gondii, Neospora caninum and microsporidia Encephalitozoon spp. In total, brain and small intestine tissues of 100 bats (52 Myotis myotis, 43 Nyctalus noctula and 5 Vespertilio murinus) were used for the DNA isolation and PCR detection of the abovementioned agents. Toxoplasma gondii DNA was detected by real-time PCR in 1% of bats (in one male of M. myotis), while all bats were negative for N. caninum DNA. Encephalitozoon spp. DNA was detected by nested PCR in 25% of bats, including three species (twenty-two M. myotis, two N. noctula and one V. murinus). Positive samples were sequenced and showed homology with the genotypes Encephalitozoon cuniculi II and Encephalitozoon hellem 2C. This is the first study on wild vespertilionid bats from Central Europe and worldwide, with a relatively high positivity of Encephalitozoon spp. detected in bats.

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 Ecology and Diseases of Game Fish and Bees Faculty of Veterinary Hygiene and Ecology University of Veterinary Sciences Brno Palackého tř 1946 1 61242 Brno Czech Republic

Department of Epizootology Parasitology and Protection of One Health University of Veterinary Medicine and Pharmacy in Košice Komenského 73 04181 Košice Slovakia

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Frank R., Kuhn T., Werblow A., Liston A., Kochmann J., Klimpel S. Parasite diversity of European Myotis species with special emphasis on Myotis myotis (Microchiroptera, Vespertilionidae) from a typical nursery roost. Parasites Vectors. 2015;8:101. doi: 10.1186/s13071-015-0707-7. PubMed DOI PMC

Hutson A.M., Mickleburgh S.P., Racey P.A. Microchiropteran Bats: Global Status Survey and Conservation Action Plan. IUCN; Gland, Switzerland: Cambridge, UK: 2001.

Racey P.A., Hutson A.M., Lina P.H.C. Bat rabies, public health and European Bat conservation. Zoonoses Public Health. 2012;60:58–68. doi: 10.1111/j.1863-2378.2012.01533.x. PubMed DOI

Scheneeberger K., Voigt C.C. Zoonotic viruses and conservation of bats. In: Voigt C.C., Kingston T., editors. Bats in the Anthropocene: Conservation of Bats in a Changing World. Springer; Cham, Switzerland: 2016. pp. 263–292.

Fagre A.C., Rebekah C., Kading R.C. Can bats serve as reservoirs for Arboviruses? Viruses. 2019;11:215. doi: 10.3390/v11030215. PubMed DOI PMC

Chen L., Liu B., Yang J., Jin Q. DBatVir: The database of bat-associated viruses. Database. 2014;2014:bau021. doi: 10.1093/database/bau021. PubMed DOI PMC

Szentiványi T., Markotter W., Dietrich M., Clément L., Ançay L., Brun L., Genzoni E., Kearney T., Seamark E., Estók P., et al. Host conservation through their parasites: Molecular surveillance of vector-borne microorganisms in bats using ectoparasitic bat flies. Parasite. 2020;27:72. doi: 10.1051/parasite/2020069. PubMed DOI PMC

Uhrin M., Kanuch P., Kristofik J., Paule L. Phenotypic plasticity in the greater mouse-eared bat in extremely different roost conditions. Acta Theriol. 2020;55:153–164. doi: 10.4098/j.at.0001-7051.073.2009. DOI

Mihalca A.D., Dumitrache M.O., Magdaş C., Gherman C.M., Domşa C., Mircean V., Ghira I.V., Pocora V., Ionescu D.T., Sikó Barabási S., et al. Synopsis of the hard ticks (Acari: Ixodidae) of Romania with update on host associations and geographical distribution. Exp. Appl. Acarol. 2012;58:183–206. doi: 10.1007/s10493-012-9566-5. PubMed DOI

Haelewater D., Hiller T., Dick C.W. Bats, bat flies, and fungi: A case of hyperparasitism. Trends Parasitol. 2018;34:794–799. doi: 10.1016/j.pt.2018.06.006. PubMed DOI

Cabral A.D., Gama A.R., Sodré M.M., Savani E.S.M.M., Galvão-Dias M.A., Jordão L.R., Maeda M.M., Yai L.E.O., Gennari S.M., Pena H.F.D.J. First isolation and genotyping of Toxoplasma gondii from bats (Mammalia: Chiroptera) Vet. Parasitol. 2013;193:100–104. doi: 10.1016/j.vetpar.2012.11.015. PubMed DOI

Sun H., Wang Y., Zhang Y., Ge W., Zhang F., He B., Li Z., Fan Q., Wang W., Tu C., et al. Prevalence and genetic characterization of Toxoplasma gondii in bats in Myanmar. Appl. Environ. Microbiol. 2013;79:3526–3528. doi: 10.1128/AEM.00410-13. PubMed DOI PMC

Dodd N.S., Lord J.S., Jehle R., Parker S., Parker F., Brooks D.R., Hide G. Toxoplasma gondii: Prevalence in species and genotypes of British bats (Pipistrellus pipistrellus and P. pygmaeus) Exper. Parasitol. 2014;139:6–11. doi: 10.1016/j.exppara.2014.02.007. PubMed DOI

De Jesus R.F., Rodrigues G.M., Silva E.M., Carneiro A.J., Franke C.R., de Magalhães Cunha R., Gondim L.F. Toxoplasmatinae parasites in bats from Bahia state, Brazil. J. Wildl. Dis. 2017;53:144–147. doi: 10.7589/2016-03-065. PubMed DOI

Wang X., Li J., Gong P., Li X., Zhang L., He B., Xu L., Yang Z., Liu Q., Zhang X. Detection of Neospora caninum DNA by polymerase chain reaction in bats from Southern China. Parasitol. Int. 2018;67:389–391. doi: 10.1016/j.parint.2018.03.002. PubMed DOI PMC

Graclik A., Wasielewski O. Diet composition of Myotis myotis (Chiroptera, Vespertilionidae) in western Poland: Results of fecal analyses. Turk. J. Zool. 2012;36:209–213. doi: 10.3906/zoo-1007-35. DOI

Cabral A.D., Su C., Soares R.M., Gennari S.M., Sperança M.A., da Rosa A.R., Pena H.F.J. Occurrence and diversity of Sarcocystidae protozoa in muscle and brain tissues of bats from Sao Paulo state, Brazil. Int. J. Parasitol. Parasites Wildl. 2021;14:91–96. doi: 10.1016/j.ijppaw.2021.01.003. PubMed DOI PMC

Yang Y., Xin S., Murata F.H.A., Cerqueira-Cézar C.K., Kwok O.C.H., Su C., Dubey J.P. Recent epidemiologic, clinical, subclinical and genetic diversity of Toxoplasma gondii infections in bats. Res. Vet. Sci. 2021;140:193–197. doi: 10.1016/j.rvsc.2021.09.006. PubMed DOI

Edvinsson B., Lappalainen M., Evengård B., ESCMID Study Group for Toxoplasmosis Real-time PCR targeting a 529-bp repeat element for diagnosis of toxoplasmosis. Clin. Microbiol. Infect. 2006;12:131–136. doi: 10.1111/j.1469-0691.2005.01332.x. PubMed DOI

Lallo M.A., Pereira A., Araújo R., Favorito S.E., Bertolla P., Bondan E.F. Occurrence of Giardia, Cryptosporidium and microsporidia in wild animals from a deforestation area in the state of São Paulo, Brazil. Ciênc Rural. 2009;39:1465–1470. doi: 10.1590/S0103-84782009005000085. DOI

Lee S.H., Oem J.K., Lee S.M., Son K., Jo S.D., Kwak D. Molecular detection of Enterocytozoon bieneusi from bats in South Korea. Med. Mycol. 2018;56:1033–1037. doi: 10.1093/mmy/myx136. PubMed DOI

Hinney B., Sak B., Joachim A., Kváč M. More than a rabbit‘s tale—Encephalitozoon spp. in wild mammals and birds. Int. J. Parasitol: Parasites Wildl. 2016;5:76–87. doi: 10.1016/j.ijppaw.2016.01.001. PubMed DOI PMC

Childs-Sanford S.E., Garner M.M., Raymondy J.T., Didier E., Kollias G.V. Disseminated microsporidiosis due to Encephalitozoon hellem in an Egyptian Fruit Bat (Rousettus aegyptiacus) J. Comp. Pathol. 2006;134:370–373. doi: 10.1016/j.jcpa.2006.01.004. PubMed DOI

Abu-Akkada S.S., El Kerdany E.D., Mady R.F., Diab R.G., Khedr G.A., Ashmawy K.I., Lotfy W.M. Encephalitozoon cuniculi infection among immunocompromised and immunocompetent humans in Egypt. Iran. J. Parasitol. 2015;10:561–570. PubMed PMC

Ma K.K., Kinde B., Doan T., Jacobs D.S., Tone S.O. Dual molecular diagnosis of microsporidia (Encephalitozoon hellem) keratoconjunctivitis in an immunocompetent adult. Cornea. 2021;40:242–244. doi: 10.1097/ICO.0000000000002466. PubMed DOI

Letko M., Seifert S.N., Olival K.J., Plowright R.K., Munster V.J. Bat-borne virus diversity, spillover and emergence. Nat. Rev. Microbiol. 2020;18:461–471. doi: 10.1038/s41579-020-0394-z. PubMed DOI PMC

Latinne A., Nga N.T.T., Long N.V., Ngoc P.T.B., Thuy H.B., PREDICT Consortium. Long N.V., Long P.T., Phuong N.T., Quang L.T.V., et al. One Health surveillance Highlights circulation of viruses with zoonotic potential in bats, pigs, and humans in Viet Nam. Viruses. 2023;15:790. doi: 10.3390/v15030790. PubMed DOI PMC

Mengistu T.S., van Wyk I., Oosthuizen M., Cohen L., Wentzel J. A One Health approach to investigate bats as a potential source of zoonotic mycoses in selected areas of Mpumalanga province, the Republic of South Africa. Ethiop. Vet. J. 2022;22:143–157. doi: 10.4314/evj.v26i2.9. DOI

Austen J.M., Barbosa A.D. Diversity and epidemiology of bat Trypanosomes: A One Health perspective. Pathogens. 2021;10:1148. doi: 10.3390/pathogens10091148. PubMed DOI PMC

Mildenstein T., Tanshi I., Racey P.A. Exploitation of bats for bushmeat and medicine. In: Voigt C., Kingston T., editors. Bats in the Anthropocene: Conservation of Bats in a Changing World. Springer; Cham, Switzerland: 2015. pp. 325–375.

Suwannarong K., Schuler S. Bats consumption in Thailand. Infect. Ecol. Epidemiol. 2016;6:29941. doi: 10.3402/iee.v6.29941. PubMed DOI PMC

Nahar N., Asaduzzaman M., Mandal U.K., Rimi N.A., Gurley E.S., Rahman M., Garcia F., Zimicki S., Sultana R., Luby S.P. Hunting bats for human consumption in Bangladesh. Ecohealth. 2020;17:139–151. doi: 10.1007/s10393-020-01468-x. PubMed DOI

Calisher C.H., Childs J.E., Field H.E., Holmes K.V., Schountz T. Bats: Important reservoir hosts of emerging viruses. Clin. Microbiol. Rev. 2006;19:531–545. doi: 10.1128/CMR.00017-06. PubMed DOI PMC

Wang L.F., Anderson D.E. Viruses in bats and potential spillover to animals and humans. Curr. Opin. Virol. 2019;34:79–89. doi: 10.1016/j.coviro.2018.12.007. PubMed DOI PMC

Zhou P., Shi Z.L. SARS-CoV-2 spillover events. Science. 2021;371:120–122. doi: 10.1126/science.abf6097. PubMed DOI

Ghaffari S., Kalantari N., Gorgani-Firouzjaee T., Bayani M., Jalali F., Daroonkola M.A. Is COVID-19 asscociated with latent toxoplasmosis? Environ. Sci. Pollut. Res. Int. 2021;28:67886–67890. doi: 10.1007/s11356-021-17126-w. PubMed DOI PMC

Roe K. The symptoms and clinical manifestations observed in COVID-19 patients/long COVID-19 symptoms that parallel Toxoplasma gondii infections. J. Neuroimmune Pharmacol. 2021;16:513–516. doi: 10.1007/s11481-021-09997-0. PubMed DOI PMC

Homan W.L., Vercammen M., De Braekeleer J., Verschueren H. Identification of a 200- to 300-fold repetitive 529 bp DNA fragment in Toxoplasma gondii, and its use for diagnostic and quantitative PCR. Int. J. Parasitol. 2000;30:69–75. doi: 10.1016/S0020-7519(99)00170-8. PubMed DOI

Ajzenberg D., Collinet F., Mercier A., Vignoles P., Dardé M.L. Genotyping of Toxoplasma gondii isolates with 15 microsatellite markers in a single multiplex PCR assay. J. Clin. Microbiol. 2010;48:4641–4645. doi: 10.1128/JCM.01152-10. PubMed DOI PMC

Muller N., Zimmermann V., Hentrich B., Gottstein B. Diagnosis of Neospora caninum and Toxoplasma gondii infection by PCR and DNA hybridisation immunoassy. J. Clin. Microbiol. 1996;34:2850–2852. doi: 10.1128/jcm.34.11.2850-2852.1996. PubMed DOI PMC

Katzwinkel-Wladarsch S., Lieb M., Heise W., Löscher T., Rinder H. Direct amplification and species determination of microsporidian DNA from stool specimens. Trop. Med. Int. Health. 1996;3:373–378. doi: 10.1046/j.1365-3156.1996.d01-51.x. PubMed DOI

Statsoft, Inc . Electronic Statistics Textbook. StatSoft; Tulsa, OK, USA: 2013.