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Molecular Survey of Zoonotic Agents in Rodents and Other Small Mammals in Croatia

Ante TadinUniversity Hospital for Infectious Diseases “Dr. Fran Mihaljević,” Zagreb, Croatia; Center for Infection and Immunity, Mailman School of Public Health, Columbia University, New York, New York; Faculty of Forestry, University of Zagreb, Zagreb, Croatia; Faculty of Veterinary Medicine, University of Zagreb, Zagreb, Croatia

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Rafal TokarzUniversity Hospital for Infectious Diseases “Dr. Fran Mihaljević,” Zagreb, Croatia; Center for Infection and Immunity, Mailman School of Public Health, Columbia University, New York, New York; Faculty of Forestry, University of Zagreb, Zagreb, Croatia; Faculty of Veterinary Medicine, University of Zagreb, Zagreb, Croatia

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Alemka MarkotićUniversity Hospital for Infectious Diseases “Dr. Fran Mihaljević,” Zagreb, Croatia; Center for Infection and Immunity, Mailman School of Public Health, Columbia University, New York, New York; Faculty of Forestry, University of Zagreb, Zagreb, Croatia; Faculty of Veterinary Medicine, University of Zagreb, Zagreb, Croatia

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Josip MargaletićUniversity Hospital for Infectious Diseases “Dr. Fran Mihaljević,” Zagreb, Croatia; Center for Infection and Immunity, Mailman School of Public Health, Columbia University, New York, New York; Faculty of Forestry, University of Zagreb, Zagreb, Croatia; Faculty of Veterinary Medicine, University of Zagreb, Zagreb, Croatia

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Nenad TurkUniversity Hospital for Infectious Diseases “Dr. Fran Mihaljević,” Zagreb, Croatia; Center for Infection and Immunity, Mailman School of Public Health, Columbia University, New York, New York; Faculty of Forestry, University of Zagreb, Zagreb, Croatia; Faculty of Veterinary Medicine, University of Zagreb, Zagreb, Croatia

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Josipa HabušUniversity Hospital for Infectious Diseases “Dr. Fran Mihaljević,” Zagreb, Croatia; Center for Infection and Immunity, Mailman School of Public Health, Columbia University, New York, New York; Faculty of Forestry, University of Zagreb, Zagreb, Croatia; Faculty of Veterinary Medicine, University of Zagreb, Zagreb, Croatia

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Petra SvobodaUniversity Hospital for Infectious Diseases “Dr. Fran Mihaljević,” Zagreb, Croatia; Center for Infection and Immunity, Mailman School of Public Health, Columbia University, New York, New York; Faculty of Forestry, University of Zagreb, Zagreb, Croatia; Faculty of Veterinary Medicine, University of Zagreb, Zagreb, Croatia

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Marko VuceljaUniversity Hospital for Infectious Diseases “Dr. Fran Mihaljević,” Zagreb, Croatia; Center for Infection and Immunity, Mailman School of Public Health, Columbia University, New York, New York; Faculty of Forestry, University of Zagreb, Zagreb, Croatia; Faculty of Veterinary Medicine, University of Zagreb, Zagreb, Croatia

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Aaloki DesaiUniversity Hospital for Infectious Diseases “Dr. Fran Mihaljević,” Zagreb, Croatia; Center for Infection and Immunity, Mailman School of Public Health, Columbia University, New York, New York; Faculty of Forestry, University of Zagreb, Zagreb, Croatia; Faculty of Veterinary Medicine, University of Zagreb, Zagreb, Croatia

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Komal JainUniversity Hospital for Infectious Diseases “Dr. Fran Mihaljević,” Zagreb, Croatia; Center for Infection and Immunity, Mailman School of Public Health, Columbia University, New York, New York; Faculty of Forestry, University of Zagreb, Zagreb, Croatia; Faculty of Veterinary Medicine, University of Zagreb, Zagreb, Croatia

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W. Ian LipkinUniversity Hospital for Infectious Diseases “Dr. Fran Mihaljević,” Zagreb, Croatia; Center for Infection and Immunity, Mailman School of Public Health, Columbia University, New York, New York; Faculty of Forestry, University of Zagreb, Zagreb, Croatia; Faculty of Veterinary Medicine, University of Zagreb, Zagreb, Croatia

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Croatia is a focus for many rodent-borne zoonosis. Here, we report a survey of 242 rodents and small mammals, including 43 Myodes glareolus, 131 Apodemus flavicollis, 53 Apodemus agrarius, three Apodemus sylvaticus, six Sorex araneus, four Microtus arvalis, one Microtus agrestis, and one Muscardinus avellanarius, collected at eight sites in Croatia over an 8-year period. Multiplex MassTag polymerase chain reaction (PCR) was used for detection of Borrelia, Rickettsia, Bartonella, Babesia, Ehrlichia, Anaplasma, Francisella tularensis, and Coxiella burnetii. Individual PCR assays were used for detection of Leptospira, lymphocytic choriomeningitis virus, orthopoxviruses, flaviviruses, hantaviruses, and Toxoplasma gondii. Of the rodents, 52 (21.5%) were infected with Leptospira, 9 (3.7%) with Borrelia miyamotoi, 5 (2%) with Borrelia afzelii, 29 (12.0%) with Bartonella, 8 (3.3%) with Babesia microti, 2 (0.8%) with Ehrlichia, 4 (1.7%) with Anaplasma, 2 (0.8%) with F. tularensis, 43 (17.8%) with hantaviruses, and 1 (0.4%) with an orthopoxvirus. Other agents were not detected. Multiple infections were found in 32 rodents (13.2%): dual infections in 26 rodents (10.7%), triple infections in four rodents (2.9%), and quadruple infections in two rodents (0.8%). Our findings indicate that rodents in Croatia harbor a wide range of bacteria and viruses that are pathogenic to humans.

Author Notes

* Address correspondence to Rafal Tokarz, Center for Infection and Immunity, Mailman School of Public Health, Columbia University, 722 West 168th Street, New York, NY 10032. E-mail: rt2249@cumc.columbia.edu
† These authors contributed equally to this work.

Financial support: Work reported here was supported by awards from the NIH (AI057158, Northeast Biodefense Center-Lipkin), USAID-PREDICT, DTRA, and by the grants 143-1430115-0103, 068-1430115-2119, 053-1430115-2116 from the Ministry of Science, Education and Sports of Republic Croatia and the project “The role of biotic agents on vitality of narrow-leafed ash in Croatian floodplain forests” from Croatian Science Foundation.

Authors' addresses: Ante Tadin, Alemka Markotić, and Petra Svoboda, University Hospital for Infectious Diseases “Dr. Fran Mihaljević,” Zagreb, Croatia, E-mails: ante.tadin@yahoo.com, alemka.markotic@gmail.com, and petra.petrasvoboda@gmail.com. Rafal Tokarz, Aaloki Desai, Komal Jain, and W. Ian Lipkin, Center for Infection and Immunity, Mailman School of Public Health, Columbia University, New York, NY, E-mails: rt2249@cumc.columbia.edu, as3745@cumc.columbia.edu, kj2230@cumc.columbia.edu, and wil2001@cumc.columbia.edu. Josip Margaletić and Marko Vucelja, Faculty of Forestry, University of Zagreb, Zagreb, Croatia, E-mails: josip.margaletic@sumfak.hr and vucelja.marko@gmail.com. Nenad Turk and Josipa Habuš, Faculty of Veterinary Medicine, University of Zagreb, Zagreb, Croatia, E-mails: turk@vef.hr and jhabus@vef.hr.

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