{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,3]],"date-time":"2026-06-03T12:37:37Z","timestamp":1780490257493,"version":"3.54.1"},"reference-count":52,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2014,1,23]],"date-time":"2014-01-23T00:00:00Z","timestamp":1390435200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/3.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Puumala virus (PUUV) causes mild to moderate cases of haemorrhagic fever with renal syndrome (HFRS), and is responsible for the majority of hantavirus infections of humans in Fennoscandia, Central and Western Europe. Although there are relatively many PUUV sequences available from different European countries, little is known about the presence of this virus in Poland. During population studies in 2009 a total of 45 bank voles were trapped at three sites in north-eastern Poland, namely islands on Dejguny and Dobskie Lakes and in a forest near Miko\u0142ajki. S and M segment-specific RT-PCR assays detected PUUV RNA in three animals from the Miko\u0142ajki site. The obtained partial S and M segment sequences demonstrated the highest similarity to the corresponding segments of a PUUV strain from Latvia. Analysis of chest cavity fluid samples by IgG ELISA using a yeast-expressed PUUV nucleocapsid protein resulted in the detection of two seropositive samples, both being also RT-PCR positive. Interestingly, at the trapping site in Miko\u0142ajki PUUV-positive bank voles belong to the Carpathian and Eastern genetic lineages within this species. In conclusion, we herein present the first molecular evidence for PUUV in the rodent reservoir from Poland.<\/jats:p>","DOI":"10.3390\/v6010340","type":"journal-article","created":{"date-parts":[[2014,1,23]],"date-time":"2014-01-23T05:29:55Z","timestamp":1390454995000},"page":"340-353","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":19,"title":["First Molecular Evidence for Puumala Hantavirus in Poland"],"prefix":"10.3390","volume":"6","author":[{"given":"Hanan","family":"Ali","sequence":"first","affiliation":[{"name":"Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, Institute for Novel and Emerging Infectious Diseases, S\u00fcdufer 10, Greifswald - Insel Riems D-17493, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stephan","family":"Drewes","sequence":"additional","affiliation":[{"name":"Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, Institute for Novel and Emerging Infectious Diseases, S\u00fcdufer 10, Greifswald - Insel Riems D-17493, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Edyta","family":"Sadowska","sequence":"additional","affiliation":[{"name":"Institute of Environmental Sciences, Jagiellonian University, Krak\u00f3w 30-387, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Magdalena","family":"Mikowska","sequence":"additional","affiliation":[{"name":"Institute of Environmental Sciences, Jagiellonian University, Krak\u00f3w 30-387, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Martin","family":"Groschup","sequence":"additional","affiliation":[{"name":"Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, Institute for Novel and Emerging Infectious Diseases, S\u00fcdufer 10, Greifswald - Insel Riems D-17493, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gerald","family":"Heckel","sequence":"additional","affiliation":[{"name":"Computational and Molecular Population Genetics (CMPG), Institute of Ecology and Evolution, University of Bern, Bern CH-3012, Switzerland"},{"name":"Swiss Institute of Bioinformatics, Genopode, Lausanne CH-1015, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pawel","family":"Koteja","sequence":"additional","affiliation":[{"name":"Institute of Environmental Sciences, Jagiellonian University, Krak\u00f3w 30-387, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rainer","family":"Ulrich","sequence":"additional","affiliation":[{"name":"Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, Institute for Novel and Emerging Infectious Diseases, S\u00fcdufer 10, Greifswald - Insel Riems D-17493, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2014,1,23]]},"reference":[{"key":"ref_1","unstructured":"King, A.M.Q., Adams, M.J., Carstens, E.B., and Lefkowitz, E.J. (2011). Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses, Elsevier Inc."},{"key":"ref_2","unstructured":"Johnson, N. (2014). Role of Animals in Emerging Viral Diseases, Academic Press."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"685","DOI":"10.4161\/hv.7.6.15197","article-title":"Human pathogenic hantaviruses and prevention of infection","volume":"7","author":"Klempa","year":"2011","journal-title":"Hum. Vaccin."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"3","DOI":"10.3855\/jidc.317","article-title":"Hantavirus infection: A review and global update","volume":"2","author":"Bi","year":"2008","journal-title":"J. Infect. Dev. Ctries."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"977","DOI":"10.2807\/ese.16.36.19961-en","article-title":"A five-year perspective on the situation of haemorrhagic fever with renal syndrome and status of the hantavirus reservoirs in Europe, 2005\u20132010","volume":"16","author":"Heyman","year":"2011","journal-title":"Euro Surveill."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1002\/rmv.1722","article-title":"Hantavirus infections in Europe and their impact on public health","volume":"23","author":"Vaheri","year":"2013","journal-title":"Rev. Med. Virol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1456","DOI":"10.1093\/infdis\/170.6.1456","article-title":"Genetic identification of a new Puumala virus strain causing severe hemorrhagic fever with renal syndrome in Germany","volume":"170","author":"Pilaski","year":"1994","journal-title":"J. Infect. Dis."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"515","DOI":"10.3109\/00365549509047057","article-title":"Four fatal cases of nephropathia epidemica","volume":"27","author":"Valtonen","year":"1995","journal-title":"Scand. J. Infect. Dis."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"S860","DOI":"10.1093\/clinids\/11.Supplement_4.S860","article-title":"The minor problem of hemostatic impairment in nephropathia epidemica, the mild Scandinavian form of hemorrhagic fever with renal syndrome","volume":"11","author":"Lahdevirta","year":"1989","journal-title":"Rev. Infect. Dis."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"83","DOI":"10.15298\/rusjtheriol.09.2.04","article-title":"Clethrionomys Tilesius, 1850 is the valid generic name for red-backed voles and Myodes Pallas, 1811 is a junior synonym of Lemmus Link, 1795","volume":"9","author":"Tesakov","year":"2010","journal-title":"Russ. J. Theriol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1093\/infdis\/141.2.131","article-title":"Nephropathia epidemica: Detection of antigen in bank voles and serologic diagnosis of human infection","volume":"141","author":"Vaheri","year":"1980","journal-title":"J. Infect. Dis."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"222","DOI":"10.4269\/ajtmh.1995.53.222","article-title":"Evidence for the existence of Puumula-related virus among Clethrionomys rufocanus in Hokkaido, Japan","volume":"53","author":"Kariwa","year":"1995","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"3121","DOI":"10.1099\/vir.0.83139-0","article-title":"Muju virus, a novel hantavirus harboured by the arvicolid rodent Myodes regulus in Korea","volume":"88","author":"Song","year":"2007","journal-title":"J. Gen. Virol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1007\/s100960050325","article-title":"Nephropathia epidemica and Puumala virus in Austria","volume":"18","author":"Aberle","year":"1999","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"512","DOI":"10.1080\/00365540600585040","article-title":"Genetic analysis of Puumala hantavirus strains from Austria","volume":"38","author":"Plyusnina","year":"2006","journal-title":"Scand. J. Infect. Dis."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"2045","DOI":"10.1002\/jmv.21635","article-title":"Co-circulation of three pathogenic hantaviruses: Puumala, Dobrava, and Saaremaa in Hungary","volume":"81","author":"Plyusnina","year":"2009","journal-title":"J. Med. Virol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1017\/S0950268800051542","article-title":"Prevalence of serum IgG antibodies to Puumala virus (haemorrhagic fever with renal syndrome) in northern Sweden","volume":"113","author":"Ahlm","year":"1994","journal-title":"Epidemiol. Infect."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"E15","DOI":"10.2807\/esm.12.05.00712-en","article-title":"Haemorrhagic Fever with Renal Syndrome: An analysis of the outbreaks in Belgium, France, Germany, the Netherlands and Luxembourg in 2005","volume":"12","author":"Heyman","year":"2007","journal-title":"Euro Surveill."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1017\/S0950268800058003","article-title":"Hantavirus infections in The Netherlands: Epidemiology and disease","volume":"114","author":"Groen","year":"1995","journal-title":"Epidemiol. Infect."},{"key":"ref_20","first-page":"45","article-title":"An epidemiological analysis of hemorrhagic fever with renal syndrome morbidity in the Republic of Bashkortostan in 1997","volume":"6","author":"Nurgaleeva","year":"1999","journal-title":"Zhurnal Mikrobiol. Epidemiol. Immunobiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1007\/s15010-005-4058-8","article-title":"Detection of human hantavirus infections in Lithuania","volume":"33","author":"Sandmann","year":"2005","journal-title":"Infection"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1002\/jmv.10231","article-title":"Hantaviruses in Estonia","volume":"68","author":"Golovljova","year":"2002","journal-title":"J. Med. Virol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"626","DOI":"10.1007\/s10096-002-0784-3","article-title":"Hantavirus infections in Latvia","volume":"21","author":"Lundkvist","year":"2002","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1016\/0168-1702(95)00058-X","article-title":"Genetic characterization of a human isolate of Puumala hantavirus from France","volume":"38","author":"Bowen","year":"1995","journal-title":"Virus Res."},{"key":"ref_25","first-page":"355","article-title":"Grading the severity of disease in patients with Puumala or Dobrava virus infections from 1995 to 2000 in Croatia","volume":"57","author":"Cebalo","year":"2003","journal-title":"Acta Med. Croat."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1023\/A:1011840104037","article-title":"First molecular evidence for Puumala hantavirus in Slovakia","volume":"23","author":"Leitmeyer","year":"2001","journal-title":"Virus Genes"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"E358","DOI":"10.1111\/1469-0691.12218","article-title":"Viral load and immune response dynamics in patients with haemorrhagic fever with renal syndrome","volume":"19","author":"Korva","year":"2013","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1023\/A:1017987104363","article-title":"Hantavirus infections in Greece\u2014An update","volume":"17","author":"Papa","year":"2001","journal-title":"Eur. J. Epidemiol."},{"key":"ref_29","first-page":"227","article-title":"The renal failure and capillary leak during the acute stage of (Dobrava) DOB and PUU (Puumala) infection","volume":"59","author":"Hukic","year":"2005","journal-title":"Med. Arh."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"2603","DOI":"10.1099\/0022-1317-79-11-2603","article-title":"Isolation and characterization of Puumala hantavirus from Norway: Evidence for a distinct phylogenetic sublineage","volume":"79","author":"Lundkvist","year":"1998","journal-title":"J. Gen. Virol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1740","DOI":"10.1093\/ndt\/gfq122","article-title":"Beechnuts and outbreaks of nephropathia epidemica (NE): Of mast, mice and men","volume":"25","author":"Clement","year":"2010","journal-title":"Nephrol. Dial. Transplant."},{"key":"ref_32","first-page":"497","article-title":"Occurrence of human hantavirus infections in Poland","volume":"61","author":"Gut","year":"2007","journal-title":"Prz. Epidemiol."},{"key":"ref_33","unstructured":"Czarkowski, M.P., Cielebak, E., Kondej, E., and Staszewska, E. (2013). Infectious Diseases and Poisonings  in Poland in 2012, Bulletin of the National Institute of Public Health and Chief Sanitary Inspectorate."},{"key":"ref_34","first-page":"474","article-title":"A case of haemorrhagic fever with renal syndrome (HFRS)","volume":"21","author":"Knap","year":"2006","journal-title":"Pol. Merkur Lek."},{"key":"ref_35","first-page":"79","article-title":"The first established focus of hantavirus infection in Poland, 2007","volume":"16","author":"Nowakowska","year":"2009","journal-title":"Ann. Agric. Environ. Med."},{"key":"ref_36","first-page":"63","article-title":"Serological studies of haemorrhagic fever with renal syndrome (HFRS) in Poland. Preliminary report","volume":"38","author":"Panasiak","year":"1989","journal-title":"Acta Microbiol. Pol."},{"key":"ref_37","first-page":"489","article-title":"The cross and unspecific reactions in serological examination for antibodies against hantavirus Puumala","volume":"61","author":"Gut","year":"2007","journal-title":"Prz. Epidemiol."},{"key":"ref_38","first-page":"531","article-title":"Detection of anti-hantavirus antibodies in forest workers in the north-east of Poland","volume":"62","author":"Grygorczuk","year":"2008","journal-title":"Prz. Epidemiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1023\/B:VIRU.0000036384.50102.cf","article-title":"Characterization of Tula virus from common voles (Microtus arvalis) in Poland: Evidence for geographic-specific phylogenetic clustering","volume":"29","author":"Song","year":"2004","journal-title":"Virus Genes"},{"key":"ref_40","first-page":"283","article-title":"A small-scale survey of hantavirus in mammals from eastern Poland","volume":"20","author":"Zajac","year":"2013","journal-title":"Ann. Agric. Environ. Med."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"160","DOI":"10.1186\/1743-422X-10-160","article-title":"Boginia virus, a newfound hantavirus harbored by the Eurasian water shrew (Neomys fodiens) in Poland","volume":"10","author":"Gu","year":"2013","journal-title":"Virol. J."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"314","DOI":"10.1002\/jmv.22263","article-title":"Co-circulation of two Puumala hantavirus lineages in Latvia: A Russian lineage described previously and a novel Latvian lineage","volume":"84","author":"Razzauti","year":"2012","journal-title":"J. Med. Virol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1111\/j.1469-7998.2010.00699.x","article-title":"Phylogeographic signatures of northward post-glacial colonization from high-latitude refugia: A case study of bank voles using museum specimens","volume":"281","author":"Wojcik","year":"2010","journal-title":"J. Zool."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1007\/s11262-011-0620-x","article-title":"Phylogenetic analysis of Puumala virus subtype Bavaria, characterization and diagnostic use of its recombinant nucleocapsid protein","volume":"43","author":"Mertens","year":"2011","journal-title":"Virus Genes"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1333","DOI":"10.1017\/S0950268806006170","article-title":"A new Puumala hantavirus subtype in rodents associated with an outbreak of Nephropathia epidemica in South-East Germany in 2004","volume":"134","author":"Essbauer","year":"2006","journal-title":"Epidemiol. Infect."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"440","DOI":"10.1007\/s10528-011-9487-8","article-title":"Molecular identification of small mammal species using novel cytochrome B gene-derived degenerated primers","volume":"50","author":"Schlegel","year":"2012","journal-title":"Biochem. Genet."},{"key":"ref_47","unstructured":"Basic Local Alignment Search Tool (BLAST). Available online:http:\/\/blast.ncbi.nlm.nih.gov\/Blast.cgi\/."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"2518","DOI":"10.1111\/j.1365-294X.2009.04189.x","article-title":"Transalpine colonisation and partial phylogeographic erosion by dispersal in the common vole (Microtus arvalis)","volume":"18","author":"Braaker","year":"2009","journal-title":"Mol. Ecol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1461","DOI":"10.3201\/eid1809.111447","article-title":"Multiple synchronous outbreaks of Puumala virus, Germany, 2010","volume":"18","author":"Ettinger","year":"2012","journal-title":"Emerg. Infect. Dis."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"2731","DOI":"10.1093\/molbev\/msr121","article-title":"MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods","volume":"28","author":"Tamura","year":"2011","journal-title":"Mol. Biol. Evol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1572","DOI":"10.1093\/bioinformatics\/btg180","article-title":"MrBayes 3: Bayesian phylogenetic inference under mixed models","volume":"19","author":"Ronquist","year":"2003","journal-title":"Bioinformatics"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"548","DOI":"10.1093\/sysbio\/syq042","article-title":"Genomic scans support repetitive continental colonization events during the rapid radiation of voles (Rodentia: Microtus): The utility of AFLPs versus mitochondrial and nuclear sequence markers","volume":"59","author":"Fink","year":"2010","journal-title":"Syst. Biol."}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/6\/1\/340\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T21:07:37Z","timestamp":1760216857000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/6\/1\/340"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2014,1,23]]},"references-count":52,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2014,1]]}},"alternative-id":["v6010340"],"URL":"https:\/\/doi.org\/10.3390\/v6010340","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2014,1,23]]}}}