Volume 94, Issue 2
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



Croatia is a focus for many rodent-borne zoonosis. Here, we report a survey of 242 rodents and small mammals, including 43 , 131 , 53 , three , six , four , one , and one , collected at eight sites in Croatia over an 8-year period. Multiplex MassTag polymerase chain reaction (PCR) was used for detection of , , , , , , , and . Individual PCR assays were used for detection of , lymphocytic choriomeningitis virus, orthopoxviruses, flaviviruses, hantaviruses, and . Of the rodents, 52 (21.5%) were infected with , 9 (3.7%) with , 5 (2%) with , 29 (12.0%) with , 8 (3.3%) with , 2 (0.8%) with , 4 (1.7%) with , 2 (0.8%) with , 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.


Article metrics loading...

The graphs shown below represent data from March 2017
Loading full text...

Full text loading...



  1. Topic MB, Habus J, Milas Z, Tosev EC, Stritof Z, Turk N, , 2010. Human leptospirosis in Croatia: current status of epidemiology and clinical characteristics. Trans R Soc Trop Med Hyg 104: 202206.[Crossref] [Google Scholar]
  2. Mulic R, Antonijevic S, Klismanic Z, Ropac D, Lucev O, , 2006. Epidemiological characteristics and clinical manifestations of Lyme borreliosis in Croatia. Mil Med 171: 11051109.[Crossref] [Google Scholar]
  3. Milotic I, Miletic B, Morovic M, , 2001. Clinical, epidemiological and epizootic features of Q fever in the northern coastal part of Croatia from 1989 to 1998. Acta Med Croatica 55: 5357. [Google Scholar]
  4. Arricau-Bouvery N, Rodolakis A, , 2005. Is Q fever an emerging or re-emerging zoonosis? Vet Res 36: 327349.[Crossref] [Google Scholar]
  5. Schex S, Dobler G, Riehm J, Muller J, Essbauer S, , 2011. Rickettsia spp. in wild small mammals in Lower Bavaria, south-eastern Germany. Vector Borne Zoonotic Dis 11: 493502.[Crossref] [Google Scholar]
  6. Punda-Polic V, Luksic B, Capkun V, , 2008. Epidemiological features of Mediterranean spotted fever, murine typhus, and Q fever in Split-Dalmatia County (Croatia), 1982–2002. Epidemiol Infect 136: 972979.[Crossref] [Google Scholar]
  7. Misic-Majerus L, Bujic N, Madaric V, Avsic-Zupanc T, Milinkovic S, , 2006. Human anaplasmosis (ehrlichiosis) [in Croatian]. Acta Med Croatica 60: 411419. [Google Scholar]
  8. Borcic B, Hrabar A, Dulic B, Tvrtkovic N, Bilic V, Mikacic D, , 1976. Ecological features of the tularemia natural focus in central Posavina (Croatia). Folia Parasitol (Praha) 23: 257265. [Google Scholar]
  9. Kosoy M, Hayman DT, Chan KS, , 2012. Bartonella bacteria in nature: where does population variability end and a species start? Infect Genet Evol 12: 894904.[Crossref] [Google Scholar]
  10. Markotic A, Kuzman I, Babic K, Gagro A, Nichol S, Ksiazek TG, Rabatic S, Dekaris D, , 2002. Double trouble: hemorrhagic fever with renal syndrome and leptospirosis. Scand J Infect Dis 34: 221224.[Crossref] [Google Scholar]
  11. Markotic A, Nichol ST, Kuzman I, Sanchez AJ, Ksiazek TG, Gagro A, Rabatic S, Zgorelec R, Avsic-Zupanc T, Beus I, Dekaris D, , 2002. Characteristics of Puumala and Dobrava infections in Croatia. J Med Virol 66: 542551.[Crossref] [Google Scholar]
  12. Scharninghausen JJ, Pfeffer M, Meyer H, Davis DS, Honeycutt RL, Faulde M, , 2002. Genetic evidence for Tula virus in Microtus arvalis and Microtus agrestis populations in Croatia. Vector Borne Zoonotic Dis 2: 1927.[Crossref] [Google Scholar]
  13. Cvetko L, Markotic A, Plyusnina A, Margaletic J, Miletic-Medved M, Turk N, Milas Z, Avsic-Zupanc T, Plyusnin A, , 2005. Puumala virus in Croatia in the 2002 HFRS outbreak. J Med Virol 77: 290294.[Crossref] [Google Scholar]
  14. Plyusnina A, Krajinovic LC, Margaletic J, Niemimaa J, Nemirov K, Lundkvist A, Markotic A, Miletic-Medved M, Avsic-Zupanc T, Henttonen H, Plyusnin A, , 2011. Genetic evidence for the presence of two distinct hantaviruses associated with Apodemus mice in Croatia and analysis of local strains. J Med Virol 83: 108114.[Crossref] [Google Scholar]
  15. McFadden G, , 2005. Poxvirus tropism. Nat Rev Microbiol 3: 201213.[Crossref] [Google Scholar]
  16. Tagliapietra V, Rosa R, Hauffe HC, Laakkonen J, Voutilainen L, Vapalahti O, Vaheri A, Henttonen H, Rizzoli A, , 2009. Spatial and temporal dynamics of lymphocytic choriomeningitis virus in wild rodents, northern Italy. Emerg Infect Dis 15: 10191025.[Crossref] [Google Scholar]
  17. Knap N, Korva M, Dolinsek V, Sekirnik M, Trilar T, Avsic-Zupanc T, , 2012. Patterns of tick-borne encephalitis virus infection in rodents in Slovenia. Vector Borne Zoonotic Dis 12: 236242.[Crossref] [Google Scholar]
  18. Niethamer J, Krapp F, , 1982. Handbuch der Saugetiere Europas: Nagetiere 2/1. Akad Verlag Wiesbaden 2: 51491. [Google Scholar]
  19. Dekonenko A, Yakimenko V, Ivanov A, Morozov V, Nikitin P, Khasanova S, Dzagurova T, Tkachenko E, Schmaljohn C, , 2003. Genetic similarity of Puumala viruses found in Finland and western Siberia and of the mitochondrial DNA of their rodent hosts suggests a common evolutionary origin. Infect Genet Evol 3: 245257.[Crossref] [Google Scholar]
  20. Essbauer S, Schmidt J, Conraths FJ, Friedrich R, Koch J, Hautmann W, Pfeffer M, Wolfel R, Finke J, Dobler G, Ulrich R, , 2006. A new Puumala hantavirus subtype in rodents associated with an outbreak of Nephropathia epidemica in south-east Germany in 2004. Epidemiol Infect 134: 13331344.[Crossref] [Google Scholar]
  21. Sikes RS, Gannon WL, , 2011. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mammal 92: 235253.[Crossref] [Google Scholar]
  22. Tokarz R, Kapoor V, Samuel JE, Bouyer DH, Briese T, Lipkin WI, , 2009. Detection of tick-borne pathogens by MassTag polymerase chain reaction. Vector Borne Zoonotic Dis 9: 147152.[Crossref] [Google Scholar]
  23. Tokarz R, Jain K, Bennett A, Briese T, Lipkin WI, , 2010. Assessment of polymicrobial infections in ticks in New York State. Vector Borne Zoonotic Dis 10: 217221.[Crossref] [Google Scholar]
  24. Bowen MD, Gelbmann W, Ksiazek TG, Nichol ST, Nowotny N, , 1997. Puumala virus and two genetic variants of Tula virus are present in Austrian rodents. J Med Virol 53: 174181.[Crossref] [Google Scholar]
  25. Chu YK, Jennings GB, Schmaljohn CS, , 1995. A vaccinia virus-vectored Hantaan virus vaccine protects hamsters from challenge with Hantaan and Seoul viruses but not Puumala virus. J Virol 69: 64176423. [Google Scholar]
  26. Avsic-Zupanc T, Nemirov K, Petrovec M, Trilar T, Poljak M, Vaheri A, Plyusnin A, , 2000. Genetic analysis of wild-type Dobrava hantavirus in Slovenia: co-existence of two distinct genetic lineages within the same natural focus. J Gen Virol 81: 17471755.[Crossref] [Google Scholar]
  27. Merien F, Portnoi D, Bourhy P, Charavay F, Berlioz-Arthaud A, Baranton G, , 2005. A rapid and quantitative method for the detection of Leptospira species in human leptospirosis. FEMS Microbiol Lett 249: 139147.[Crossref] [Google Scholar]
  28. Victoria B, Ahmed A, Zuerner RL, Ahmed N, Bulach DM, Quinteiro J, Hartskeerl RA, , 2008. Conservation of the S10-spc-alpha locus within otherwise highly plastic genomes provides phylogenetic insight into the genus Leptospira . PLoS One 3: e2752.[Crossref] [Google Scholar]
  29. Briese T, Palacios G, Kokoris M, Jabado O, Liu Z, Renwick N, Kapoor V, Casas I, Pozo F, Limberger R, Perez-Brena P, Ju J, Lipkin WI, , 2005. Diagnostic system for rapid and sensitive differential detection of pathogens. Emerg Infect Dis 11: 310313.[Crossref] [Google Scholar]
  30. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S, , 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30: 27252729.[Crossref] [Google Scholar]
  31. Gravekamp C, Van de Kemp H, Franzen M, Carrington D, Schoone GJ, Van Eys GJ, Everard CO, Hartskeerl RA, Terpstra WJ, , 1993. Detection of seven species of pathogenic leptospires by PCR using two sets of primers. J Gen Microbiol 139: 16911700.[Crossref] [Google Scholar]
  32. Stritof Majetic Z, Galloway R, Ruzic Sabljic E, Milas Z, Mojcec Perko V, Habus J, Margaletic J, Pernar R, Turk N, , 2014. Epizootiological survey of small mammals as Leptospira spp. reservoirs in eastern Croatia. Acta Trop 131: 111116.[Crossref] [Google Scholar]
  33. Turk N, Milas Z, Margaletic J, Staresina V, Slavica A, Riquelme-Sertour N, Bellenger E, Baranton G, Postic D, , 2003. Molecular characterization of Leptospira spp. strains isolated from small rodents in Croatia. Epidemiol Infect 130: 159166.[Crossref] [Google Scholar]
  34. Turk N, Milas Z, Margaletic J, Turk R, Barbic L, Konjevic D, Peric S, Stritof Z, Staresina V, , 2008. The role of fat dromouse (Glis glis L.) as reservoir host for spirochete Borrelia burgdorferi sensu lato in the region of Gorski Kotar, Croatia. Eur J Wildl Res 54: 117121.[Crossref] [Google Scholar]
  35. Tea A, Alexiou-Daniel S, Papoutsi A, Papa A, Antoniadis A, , 2004. Bartonella species isolated from rodents, Greece. Emerg Infect Dis 10: 963964.[Crossref] [Google Scholar]
  36. La Scola B, Zeaiter Z, Khamis A, Raoult D, , 2003. Gene-sequence-based criteria for species definition in bacteriology: the Bartonella paradigm. Trends Microbiol 11: 318321.[Crossref] [Google Scholar]
  37. Buffet JP, Kosoy M, Vayssier-Taussat M, , 2013. Natural history of Bartonella-infecting rodents in light of new knowledge on genomics, diversity and evolution. Future Microbiol 8: 11171128.[Crossref] [Google Scholar]
  38. Welc-Faleciak R, Paziewska A, Bajer A, Behnke JM, Sinski E, , 2008. Bartonella spp. infection in rodents from different habitats in the Mazury Lake District, northeast Poland. Vector Borne Zoonotic Dis 8: 467474.[Crossref] [Google Scholar]
  39. Birtles RJ, Raoult D, , 1996. Comparison of partial citrate synthase gene (gltA) sequences for phylogenetic analysis of Bartonella species. Int J Syst Bacteriol 46: 891897.[Crossref] [Google Scholar]
  40. Beck R, Vojta L, Curkovic S, Mrljak V, Margaletic J, Habrun B, , 2011. Molecular survey of Babesia microti in wild rodents in central Croatia. Vector Borne Zoonotic Dis 11: 8183.[Crossref] [Google Scholar]
  41. Tadin A, Turk N, Korva M, Margaletic J, Beck R, Vucelja M, Habus J, Svoboda P, Zupanc TA, Henttonen H, Markotic A, , 2012. Multiple co-infections of rodents with hantaviruses, Leptospira, and Babesia in Croatia. Vector Borne Zoonotic Dis 12: 388392.[Crossref] [Google Scholar]
  42. Cvetko L, Turk N, Markotic A, Milas Z, Margaletic J, Miletic-Medved M, Plyusnin A, Baranton G, Postic D, Avsic-Zupanc T, , 2006. Short report: dual infections with Puumala virus and Leptospira interrogans serovar Lora in a bank vole (Clethrionomys glareolus). Am J Trop Med Hyg 74: 612614. [Google Scholar]
  43. Sunil-Chandra NP, Clement J, Maes PDE, Silva H, Van Esbroeck M, Van Ranst M, , 2015. Concomitant leptospirosis-hantavirus co-infection in acute patients hospitalized in Sri Lanka: implications for a potentially worldwide underestimated problem. Epidemiol Infect 143: 20812093.[Crossref] [Google Scholar]
  44. Burri C, Schumann O, Schumann C, Gern L, , 2014. Are Apodemus spp. mice and Myodes glareolus reservoirs for Borrelia miyamotoi, Candidatus Neoehrlichia mikurensis, Rickettsia helvetica, R. monacensis and Anaplasma phagocytophilum? Ticks Tick Borne Dis 5: 245251.[Crossref] [Google Scholar]
  45. Fukunaga M, Takahashi Y, Tsuruta Y, Matsushita O, Ralph D, McClelland M, Nakao M, , 1995. Genetic and phenotypic analysis of Borrelia miyamotoi sp. nov., isolated from the ixodid tick Ixodes persulcatus, the vector for Lyme disease in Japan. Int J Syst Bacteriol 45: 804810.[Crossref] [Google Scholar]
  46. Platonov AE, Karan LS, Kolyasnikova NM, Makhneva NA, Toporkova MG, Maleev VV, Fish D, Krause PJ, , 2011. Humans infected with relapsing fever spirochete Borrelia miyamotoi, Russia. Emerg Infect Dis 17: 18161823.[Crossref] [Google Scholar]
  47. Hovius JW, de Wever B, Sohne M, Brouwer MC, Coumou J, Wagemakers A, Oei A, Knol H, Narasimhan S, Hodiamont CJ, Jahfari S, Pals ST, Horlings HM, Fikrig E, Sprong H, van Oers MH, , 2013. A case of meningoencephalitis by the relapsing fever spirochaete Borrelia miyamotoi in Europe. Lancet 382: 658.[Crossref] [Google Scholar]
  48. Gugliotta JL, Goethert HK, Berardi VP, Telford SR, 3rd, 2013. Meningoencephalitis from Borrelia miyamotoi in an immunocompromised patient. N Engl J Med 368: 240245.[Crossref] [Google Scholar]
  49. Bown KJ, Begon M, Bennett M, Woldehiwet Z, Ogden NH, , 2003. Seasonal dynamics of Anaplasma phagocytophila in a rodent-tick (Ixodes trianguliceps) system, United Kingdom. Emerg Infect Dis 9: 6370.[Crossref] [Google Scholar]

Data & Media loading...

  • Received : 10 Jul 2015
  • Accepted : 02 Nov 2015
  • Published online : 03 Feb 2016

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error