{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,24]],"date-time":"2026-06-24T16:44:56Z","timestamp":1782319496776,"version":"3.54.5"},"reference-count":56,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2023,1,25]],"date-time":"2023-01-25T00:00:00Z","timestamp":1674604800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"German Federal Ministry of Education and Research","award":["01KI2010D"],"award-info":[{"award-number":["01KI2010D"]}]},{"name":"German Federal Ministry of Education and Research","award":["01KI2010A"],"award-info":[{"award-number":["01KI2010A"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Tick-borne encephalitis (TBE) is Eurasia\u2019s most important tick-borne viral disease. Rodents play an important role as natural hosts. Longitudinal studies on the dynamics of the seroprevalence rates in wild rodents in natural foci over the year are rare, and the dynamics of the transmission cycle still need to be understood. To better understand the infection dynamics, rodents were captured in a capture-mark-release-recapture-study in two natural foci in Bavaria, Germany, monthly from March 2019 to October 2022. Overall, 651 blood and thoracic lavage samples from 478 different wild rodents (Clethrionomys glareolus and Apodemus flavicollis) were analyzed for antibodies against tick-borne encephalitis virus (TBEV) by indirect immunofluorescence assay (IIFA) and confirmed using a serum neutralization test (SNT). Furthermore, a generalized linear mixed model (GLMM) analysis was performed to investigate ecological and individual factors for the probability of infection in rodents. Clethrionomys glareolus (19.4%) had a higher seroprevalence than A. flavicollis (10.5%). Within Cl. glareolus, more males (40.4%) than females (15.6%) were affected, and more adults (25.4%) than juveniles (9.8%). The probability of infection of rodents rather depends on factors such as species, sex, and age than on the study site of a natural focus, year, and season. The high incidence rates of rodents, particularly male adult bank voles, highlight their critical role in the transmission cycle of TBEV in a natural focus and demonstrate that serologically positive rodents can be reliably detected in a natural focus regardless of season or year. In addition, these data contribute to a better understanding of the TBEV cycle and thus could improve preventive strategies for human infections.<\/jats:p>","DOI":"10.3390\/pathogens12020185","type":"journal-article","created":{"date-parts":[[2023,1,25]],"date-time":"2023-01-25T04:22:16Z","timestamp":1674620536000},"page":"185","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":16,"title":["Seroprevalence of Tick-Borne Encephalitis (TBE) Virus Antibodies in Wild Rodents from Two Natural TBE Foci in Bavaria, Germany"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4197-7550","authenticated-orcid":false,"given":"Philipp Johannes","family":"Brandenburg","sequence":"first","affiliation":[{"name":"Institute of Animal Hygiene and Veterinary Public Health, Faculty of Veterinary Medicine, University of Leipzig, An den Tierkliniken 1, 04103 Leipzig, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anna","family":"Obiegala","sequence":"additional","affiliation":[{"name":"Institute of Animal Hygiene and Veterinary Public Health, Faculty of Veterinary Medicine, University of Leipzig, An den Tierkliniken 1, 04103 Leipzig, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hannah Maureen","family":"Schmuck","sequence":"additional","affiliation":[{"name":"Institute of Animal Hygiene and Veterinary Public Health, Faculty of Veterinary Medicine, University of Leipzig, An den Tierkliniken 1, 04103 Leipzig, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7461-293X","authenticated-orcid":false,"given":"Gerhard","family":"Dobler","sequence":"additional","affiliation":[{"name":"National Consulting Laboratory for TBE, Bundeswehr Institute of Microbiology, Neuherbergstrasse 11, 80937 Munich, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lidia","family":"Chitimia-Dobler","sequence":"additional","affiliation":[{"name":"National Consulting Laboratory for TBE, Bundeswehr Institute of Microbiology, Neuherbergstrasse 11, 80937 Munich, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2457-8224","authenticated-orcid":false,"given":"Martin","family":"Pfeffer","sequence":"additional","affiliation":[{"name":"Institute of Animal Hygiene and Veterinary Public Health, Faculty of Veterinary Medicine, University of Leipzig, An den Tierkliniken 1, 04103 Leipzig, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,1,25]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1861","DOI":"10.1016\/S0140-6736(08)60800-4","article-title":"Tick-borne encephalitis","volume":"371","author":"Lindquist","year":"2008","journal-title":"Lancet"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1781","DOI":"10.1099\/vir.0.011437-0","article-title":"Tick-borne encephalitis virus\u2014A review of an emerging zoonosis","volume":"90","author":"Mansfield","year":"2009","journal-title":"J. Gen. Virol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"230","DOI":"10.1007\/s10354-012-0100-5","article-title":"Epidemiology and distribution of tick-borne encephalitis","volume":"162","author":"Dobler","year":"2012","journal-title":"Wien. Med. Wochenschr."},{"key":"ref_4","first-page":"20299","article-title":"Tick-borne encephalitis joins the diseases under surveillance in the European Union","volume":"17","author":"Zeller","year":"2012","journal-title":"Eurosurveillance"},{"key":"ref_5","unstructured":"European Centre for Disease Prevention and Control (2022, November 03). Tick-borne encephalitis\u2014Annual Epidemiological Report for 2020, Available online: https:\/\/www.ecdc.europa.eu\/en\/publications-data\/tick-borne-encephalitis-annual-epidemiological-report-2020."},{"key":"ref_6","unstructured":"Robert Koch-Institut (2022). Epidemiologisches Bulletin."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Deviatkin, A.A., Karganova, G.G., Vakulenko, Y.A., and Lukashev, A.N. (2020). TBEV Subtyping in Terms of Genetic Distance. Viruses, 12.","DOI":"10.3390\/v12111240"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.virol.2008.11.023","article-title":"CD8+ T-cells mediate immunopathology in tick-borne encephalitis","volume":"384","author":"Ruzek","year":"2009","journal-title":"Virology"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"453","DOI":"10.20506\/rst.34.2.2371","article-title":"Tick-borne encephalitis","volume":"34","author":"Valarcher","year":"2015","journal-title":"Rev. Sci. Tech."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"430","DOI":"10.12998\/wjcc.v3.i5.430","article-title":"Tick-borne encephalitis: A review of epidemiology, clinical characteristics, and management","volume":"3","author":"Bogovic","year":"2015","journal-title":"WJCC"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Borde, J.P., Glaser, R., Braun, K., Riach, N., Hologa, R., Kaier, K., Chitimia-Dobler, L., and Dobler, G. (2022). Decoding the Geography of Natural TBEV Microfoci in Germany: A Geostatistical Approach Based on Land-Use Patterns and Climatological Conditions. Int. J. Environ. Res. Public Health, 19.","DOI":"10.3390\/ijerph191811830"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1016\/S0934-8840(99)80005-X","article-title":"Survival strategy of tick-borne encephalitis virus: Cellular basis and environmental determinants","volume":"289","author":"Labuda","year":"1999","journal-title":"Zent. F\u00fcr Bakteriol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1016\/j.ttbdis.2011.07.004","article-title":"Transmission of tick-borne pathogens between co-feeding ticks: Milan Labuda\u2019s enduring paradigm","volume":"2","author":"Randolph","year":"2011","journal-title":"Ticks Tick-Borne Dis."},{"key":"ref_14","first-page":"3","article-title":"The role of particular tick developmental stages in the circulation of tick-borne pathogens affecting humans in Central Europe. 2. Tick-borne encephalitis virus","volume":"62","author":"Karbowiak","year":"2016","journal-title":"Ann. Parasitol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"72","DOI":"10.3201\/eid1701.100051","article-title":"Tick-borne encephalitis virus in wild rodents in winter, Finland, 2008\u20132009","volume":"17","author":"Tonteri","year":"2011","journal-title":"Emerg. Infect. Dis."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1089\/vbz.2006.6.32","article-title":"Natural tick-borne encephalitis virus infection among wild small mammals in the southeastern part of western Siberia, Russia","volume":"6","author":"Bakhvalova","year":"2006","journal-title":"Vector Borne Zoonotic Dis."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1060","DOI":"10.3201\/eid2805.212457","article-title":"Breast Milk as Route of Tick-Borne Encephalitis Virus Transmission from Mother to Infant","volume":"28","author":"Kerlik","year":"2022","journal-title":"Emerg. Infect. Dis."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"641","DOI":"10.1089\/vbz.2010.0236","article-title":"Rodents as sentinels for the prevalence of tick-borne encephalitis virus","volume":"11","author":"Achazi","year":"2011","journal-title":"Vector Borne Zoonotic Dis."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"896","DOI":"10.1093\/infdis\/jix040","article-title":"A Cluster of Fatal Tick-borne Encephalitis Virus Infection in Organ Transplant Setting","volume":"215","author":"Lipowski","year":"2017","journal-title":"J. Infect. Dis."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1089\/vbz.2006.6.379","article-title":"Tick-borne encephalitis virus in Clethrionomys glareolus in the Czech Republic","volume":"6","author":"Weidmann","year":"2006","journal-title":"Vector Borne Zoonotic Dis."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"236","DOI":"10.1089\/vbz.2011.0728","article-title":"Patterns of tick-borne encephalitis virus infection in rodents in Slovenia","volume":"12","author":"Knap","year":"2012","journal-title":"Vector Borne Zoonotic Dis."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"178","DOI":"10.3109\/00365548.2014.975743","article-title":"Bank voles show high seropositivity rates in a natural TBEV focus in Hungary","volume":"47","author":"Papp","year":"2015","journal-title":"Infect. Dis."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"101693","DOI":"10.1016\/j.ttbdis.2021.101693","article-title":"Long-term presence of tick-borne encephalitis virus in experimentally infected bank voles (Myodes glareolus)","volume":"12","author":"Michelitsch","year":"2021","journal-title":"Ticks Tick-Borne Dis."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Michelitsch, A., Tews, B.A., Klaus, C., Bestehorn-Willmann, M., Dobler, G., Beer, M., and Wernike, K. (2019). In Vivo Characterization of Tick-Borne Encephalitis Virus in Bank Voles (Myodes glareolus). Viruses, 11.","DOI":"10.3390\/v11111069"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1038\/s41426-018-0149-3","article-title":"Seroprevalence of TBEV in bank voles from Poland-a long-term approach","volume":"7","author":"Grzybek","year":"2018","journal-title":"Emerg. Microbes Infect."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Bournez, L., Umhang, G., Moinet, M., Richomme, C., Demerson, J.-M., Caillot, C., Devillers, E., Boucher, J.-M., Hansmann, Y., and Bou\u00e9, F. (2020). Tick-Borne Encephalitis Virus: Seasonal and Annual Variation of Epidemiological Parameters Related to Nymph-to-Larva Transmission and Exposure of Small Mammals. Pathogens, 9.","DOI":"10.3390\/pathogens9070518"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Borde, J.P., Kaier, K., Hehn, P., Matzarakis, A., Frey, S., Bestehorn, M., Dobler, G., and Chitimia-Dobler, L. (2021). The complex interplay of climate, TBEV vector dynamics and TBEV infection rates in ticks-Monitoring a natural TBEV focus in Germany, 2009\u20132018. PLoS ONE, 16.","DOI":"10.1371\/journal.pone.0244668"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"2129","DOI":"10.1099\/vir.0.054478-0","article-title":"Molecular phylogeography of tick-borne encephalitis virus in central Europe","volume":"94","author":"Weidmann","year":"2013","journal-title":"J. Gen. Virol."},{"key":"ref_29","unstructured":"Robert Koch-Institut (2022, November 04). SurvStat@RKI 2.0, Available online: https:\/\/survstat.rki.de\/Content\/Query\/Create.aspx."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1007\/s10393-014-0969-0","article-title":"A 4-year study of a natural tick-borne encephalitis virus focus in Hungary, 2010\u20132013","volume":"12","author":"Papp","year":"2015","journal-title":"EcoHealth"},{"key":"ref_31","unstructured":"Niethammer, J., and Krapp, F. (1982). Handbuch der S\u00e4ugetiere Europas, Akademische Verlagsgesellschaft."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1007\/BF03193120","article-title":"Habitat preferences of the bank vole Myodes glareolus in a Mediterranean mountain range","volume":"53","author":"Torre","year":"2008","journal-title":"Acta Theriol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1089\/vbz.2012.1287","article-title":"Evaluation of different serological diagnostic methods for tick-borne encephalitis virus: Enzyme-linked immunosorbent, immunofluorescence, and neutralization assay","volume":"14","author":"Litzba","year":"2014","journal-title":"Vector Borne Zoonotic Dis."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Girl, P., Haut, M., Riederer, S., Pfeffer, M., and Dobler, G. (2021). Comparison of Three Serological Methods for the Epidemiological Investigation of TBE in Dogs. Microorganisms, 9.","DOI":"10.3390\/microorganisms9020399"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1046\/j.1365-2915.2000.00236.x","article-title":"Role of small mammals in the persistence of Louping-ill virus: Field survey and tick co-feeding studies","volume":"14","author":"Gilbert","year":"2000","journal-title":"Med. Vet. Entomol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"436","DOI":"10.1603\/ME11084","article-title":"Serological evidence of tick-borne encephalitis virus infection in rodents captured at four sites in Switzerland","volume":"49","author":"Burri","year":"2012","journal-title":"J. Med. Entomol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1016\/S0147-9571(99)00015-6","article-title":"Epizootiologic background of dissimilar distribution of human cases of Lyme borreliosis and tick-borne encephalitis in a joint endemic area","volume":"22","author":"Zeman","year":"1999","journal-title":"Comp. Immunol. Microbiol. Infect. Dis."},{"key":"ref_38","first-page":"61","article-title":"The role of small rodents and hedgehogs in a natural focus of tick-borne encephalitis","volume":"36","author":"Kozuch","year":"1967","journal-title":"Bull. World Health Organ."},{"key":"ref_39","first-page":"537","article-title":"Longitudinal study of natural foci of Central European encephalitis virus in West Slovakia","volume":"34","author":"Kozuch","year":"1990","journal-title":"Acta Virol."},{"key":"ref_40","first-page":"283","article-title":"The prevalence of small terrestrial mammals infected with tick-borne encephalitis virus and leptospirae in the foothills of the southern Bavarian forest, Germany","volume":"34","author":"Kozuch","year":"1993","journal-title":"Appl. Parasitol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1111\/j.1365-3024.1995.tb00887.x","article-title":"Clethrionomys glareolus, but not Apodemus flavicollis, acquires resistance to Ixodes ricinus L., the main European vector of Borrelia burgdorferi","volume":"17","author":"Dizij","year":"1995","journal-title":"Parasite Immunol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1111\/apm.1966.66.4.489","article-title":"Experimental Infection with Tick-Borne Encephalitis Virus in Clethrionomys glareolus, Apodemus flavicollis, Apodemus sylvaticur and Mus musculus. I. Virological Studies","volume":"66","author":"Heigl","year":"1966","journal-title":"Acta Pathol. Microbiol. Scand."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1111\/apm.1966.68.2.211","article-title":"Experimental infection with tick-borne virus in Clethrionomys glareolus, Apodemus flavicollis, Apodemus sylvaticus and Mus musculus. 2. Serological studies","volume":"68","author":"Heigl","year":"1966","journal-title":"Acta Pathol. Microbiol. Scand."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"802","DOI":"10.1007\/BF01923553","article-title":"Non-viraemic transmission of tick-borne encephalitis virus: A mechanism for arbovirus survival in nature","volume":"49","author":"Labuda","year":"1993","journal-title":"Experientia"},{"key":"ref_45","first-page":"281","article-title":"Investigations in a Natural Focus of Early Summer Meningoencephalitis in Lower Austria. 2. Attempt to isolate Virus from Arthropods and Small Mammals","volume":"190","author":"Radda","year":"1963","journal-title":"Zent. Fur Bakteriol. Parasitenkd. Infekt. Und Hyg."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1017\/S0031182001008599","article-title":"Testosterone increases the transmission potential of tick-borne parasites","volume":"123","author":"Hughes","year":"2001","journal-title":"Parasitology"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1722","DOI":"10.1017\/S0031182015001225","article-title":"Long-term spatiotemporal stability and dynamic changes in helminth infracommunities of bank voles (Myodes glareolus) in NE Poland","volume":"142","author":"Grzybek","year":"2015","journal-title":"Parasitology"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1006\/viro.1997.8622","article-title":"Tick-borne encephalitis virus transmission between ticks cofeeding on specific immune natural rodent hosts","volume":"235","author":"Labuda","year":"1997","journal-title":"Virology"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1007\/BF03192479","article-title":"Population dynamics of Clethrionomys glareolus and Apodemus flavicollis: Seasonal components of density dependence and density independence","volume":"47","author":"Stenseth","year":"2002","journal-title":"Acta Theriol."},{"key":"ref_50","first-page":"81","article-title":"Spatial organization and home range of Apodemus flavicollis and A. agrarius on Mt. Avala, Serbia","volume":"52","author":"Mati","year":"2006","journal-title":"Acta Zool. Acad. Sci. Hung."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1007\/BF00789934","article-title":"Social organization of the bank vole (Clethrionomys glareolus, Schreber 1780) and its demographic consequences: A model","volume":"80","author":"Bujalska","year":"1989","journal-title":"Oecologia"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1017\/S0031182002001865","article-title":"Prevalence and abundance of Cryptosporidium parvum and giardia spp. in wild rural rodents from the Mazury Lake District region of Poland","volume":"125","author":"Bajer","year":"2002","journal-title":"Parasitology"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"75","DOI":"10.20506\/rst.40.1.3209","article-title":"A review of diagnostic tests recommended by the World Organisation for Animal Health Manual of Diagnostic Tests and Vaccines for Terrestrial Animals","volume":"40","author":"Cullinane","year":"2021","journal-title":"Rev. Sci. Tech."},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Coroian, M., Mihalca, A.D., Dobler, G., Euringer, K., Girl, P., Bor\u0219an, S.-D., Kalm\u00e1r, Z., Tincu\u021ba Briciu, V., Flonta, M., and Topan, A. (2022). Seroprevalence Rates against West Nile, Usutu, and Tick-Borne Encephalitis Viruses in Blood-Donors from North-Western Romania. Int. J. Environ. Res. Public Health, 19.","DOI":"10.3390\/ijerph19138182"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1","DOI":"10.18637\/jss.v067.i01","article-title":"Fitting linear mixed-effects models using lme4","volume":"67","author":"Bates","year":"2015","journal-title":"J. Stat. Soft."},{"key":"ref_56","first-page":"3","article-title":"Emmeans: Estimated marginal means, aka least-squares means","volume":"1","author":"Length","year":"2018","journal-title":"R Package Version"}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/12\/2\/185\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:15:09Z","timestamp":1760120109000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/12\/2\/185"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,1,25]]},"references-count":56,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2023,2]]}},"alternative-id":["pathogens12020185"],"URL":"https:\/\/doi.org\/10.3390\/pathogens12020185","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,1,25]]}}}