Orthohantaviruses in Reservoir and Atypical Hosts in the Czech Republic: Spillover Infection and Indication of Virus-Specific Tissue Tropism

. 2022 Oct 26 ; 10 (5) : e0130622. [epub] 20220928

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid36169417

Orthohantaviruses (genus Orthohantavirus) are a diverse group of viruses that are closely associated with their natural hosts (rodents, shrews, and moles). Several orthohantaviruses cause severe disease in humans. Central and western Europe are areas with emerging orthohantavirus occurrences. In our study, several orthohantaviruses, including the pathogenic Kurkino virus (KURV), were detected in their natural hosts trapped at several study sites in the Czech Republic. KURV was detected mainly in its typical host, the striped field mouse (Apodemus agrarius). Nevertheless, spillover infections were also detected in wood mice (Apodemus sylvaticus) and common voles (Microtus arvalis). Similarly, Tula virus (TULV) was found primarily in common voles, and events of spillover to rodents of other host species, including Apodemus spp., were recorded. In addition, unlike most previous studies, different tissues were sampled and compared to assess their suitability for orthohantavirus screening and possible tissue tropism. Our data suggest possible virus-specific tissue tropism in rodent hosts. TULV was most commonly detected in the lung tissue, whereas KURV was more common in the liver, spleen, and brain. Moreover, Seewis and Asikkala viruses were detected in randomly found common shrews (Sorex araneus). In conclusion, we have demonstrated the presence of human-pathogenic KURV and the potentially pathogenic TULV in their typical hosts as well as their spillover to atypical host species belonging to another family. Furthermore, we suggest the possibility of virus-specific tissue tropism of orthohantaviruses in their natural hosts. IMPORTANCE Orthohantaviruses (genus Orthohantavirus, family Hantaviridae) are a diverse group of globally distributed viruses that are closely associated with their natural hosts. Some orthohantaviruses are capable of infecting humans and causing severe disease. Orthohantaviruses are considered emerging pathogens due to their ever-increasing diversity and increasing numbers of disease cases. We report the detection of four different orthohantaviruses in rodents and shrews in the Czech Republic. Most viruses were found in their typical hosts, Kurkino virus (KURV) in striped field mice (Apodemus agrarius), Tula virus (TULV) in common voles (Microtus arvalis), and Seewis virus in common shrews (Sorex araneus). Nevertheless, spillover infections of atypical host species were also recorded for KURV, TULV, and another shrew-borne orthohantavirus, Asikkala virus. In addition, indications of virus-specific patterns of tissue tropism were observed. Our results highlight the circulation of several orthohantaviruses, including KURV, which is pathogenic to humans, among rodents and shrews in the Czech Republic.

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Laenen L, Vergote V, Calisher CH, Klempa B, Klingström J, Kuhn JH, Maes P. 2019. Hantaviridae: current classification and future perspectives. Viruses 11:788. doi:10.3390/v11090788. PubMed DOI PMC

Kuhn JH, Adkins S, Agwanda BR, Al Kubrusli R, Alkhovsky SV, Amarasinghe GK, Avšič-Županc T, Ayllón MA, Bahl J, Balkema-Buschmann A, Ballinger MJ, Basler CF, Bavari S, Beer M, Bejerman N, Bennett AJ, Bente DA, Bergeron É, Bird BH, Blair CD, Blasdell KR, Blystad D-R, Bojko J, Borth WB, Bradfute S, Breyta R, Briese T, Brown PA, Brown JK, Buchholz UJ, Buchmeier MJ, Bukreyev A, Burt F, Büttner C, Calisher CH, Cao M, Casas I, Chandran K, Charrel RN, Cheng Q, Chiaki Y, Chiapello M, Choi I-R, Ciuffo M, Clegg JCS, Crozier I, Dal Bó E, de la Torre JC, de Lamballerie X, de Swart RL, et al. . 2021. 2021 taxonomic update of phylum Negarnaviricota (Riboviria: Orthornavirae), including the large orders Bunyavirales and Mononegavirales. Arch Virol 166:3513–3566. doi:10.1007/s00705-021-05143-6. PubMed DOI PMC

Krüger DH, Schönrich G, Klempa B. 2011. Human pathogenic hantaviruses and prevention of infection. Hum Vaccin 7:685–693. doi:10.4161/hv.7.6.15197. PubMed DOI PMC

Sibold C, Ulrich R, Labuda M, Lundkvist Å, Martens H, Schütt M, Gerke P, Leitmeyer K, Meisel H, Krüger DH. 2001. Dobrava hantavirus causes hemorrhagic fever with renal syndrome in central Europe and is carried by two different Apodemus mice species. J Med Virol 63:158–167. PubMed

Avšič-Županc T, Saksida A, Korva M. 2019. Hantavirus infections. Clin Microbiol Infect 21S:e6–e16. doi:10.1111/1469-0691.12291. PubMed DOI

Jonsson CB, Figueiredo LTM, Vapalahti O. 2010. A global perspective on hantavirus ecology, epidemiology, and disease. Clin Microbiol Rev 23:412–441. doi:10.1128/CMR.00062-09. PubMed DOI PMC

Klempa B, Avsic-Zupanc T, Clement J, Dzagurova TK, Henttonen H, Heyman P, Jakab F, Kruger DH, Maes P, Papa A, Tkachenko EA, Ulrich RG, Vapalahti O, Vaheri A. 2013. Complex evolution and epidemiology of Dobrava-Belgrade hantavirus: definition of genotypes and their characteristics. Arch Virol 158:521–529. doi:10.1007/s00705-012-1514-5. PubMed DOI PMC

Klempa B, Radosa L, Kruger DH. 2013. The broad spectrum of hantaviruses and their hosts in central Europe. Acta Virol 57:130–137. doi:10.4149/av_2013_02_130. PubMed DOI

Plyusnin A, Morzunov SP. 2001. Virus evolution and genetic diversity of hantaviruses and their rodent hosts. Curr Top Microbiol Immunol 256:47–75. doi:10.1007/978-3-642-56753-7_4. PubMed DOI

Yanagihara R, Gu SH, Arai S, Kang HJ, Song J-W. 2014. Hantaviruses: rediscovery and new beginnings. Virus Res 187:6–14. doi:10.1016/j.virusres.2013.12.038. PubMed DOI PMC

Zhang Y-Z. 2014. Discovery of hantaviruses in bats and insectivores and the evolution of the genus Hantavirus. Virus Res 187:15–21. doi:10.1016/j.virusres.2013.12.035. PubMed DOI

Watson DC, Sargianou M, Papa A, Chra P, Starakis I, Panos G. 2014. Epidemiology of hantavirus infections in humans: a comprehensive, global overview. Crit Rev Microbiol 40:261–272. doi:10.3109/1040841X.2013.783555. PubMed DOI

Guo W-P, Lin X-D, Wang W, Tian J-H, Cong M-L, Zhang H-L, Wang M-R, Zhou R-H, Wang J-B, Li M-H, Xu J, Holmes EC, Zhang Y-Z. 2013. Phylogeny and origins of hantaviruses harbored by bats, insectivores, and rodents. PLoS Pathog 9:e1003159. doi:10.1371/journal.ppat.1003159. PubMed DOI PMC

Heyman P, Plyusnina A, Berny P, Cochez C, Artois M, Zizi M, Pirnay JP, Plyusnin A. 2004. Seoul hantavirus in Europe: first demonstration of the virus genome in wild Rattus norvegicus captured in France. Eur J Clin Microbiol Infect Dis 23:711–717. doi:10.1007/s10096-004-1196-3. PubMed DOI

Madai M, Horváth G, Herczeg R, Somogyi B, Zana B, Földes F, Kemenesi G, Kurucz K, Papp H, Zeghbib S, Jakab F. 2021. Effectiveness regarding hantavirus detection in rodent tissue samples and urine. Viruses 13:570. doi:10.3390/v13040570. PubMed DOI PMC

Papa A, Zelená H, Barnetová D, Petroušová L. 2010. Genetic detection of Dobrava/Belgrade virus in a Czech patient with haemorrhagic fever with renal syndrome. Clin Microbiol Infect 16:1187–1190. doi:10.1111/j.1469-0691.2009.03075.x. PubMed DOI

Verner-Carlsson J, Lõhmus M, Sundström K, Strand TM, Verkerk M, Reusken C, Yoshimatsu K, Arikawa J, van de Goot F, Lundkvist Å. 2015. First evidence of Seoul hantavirus in the wild rat population in the Netherlands. Infect Ecol Epidemiol 5:27215. doi:10.3402/iee.v5.27215. PubMed DOI PMC

Radosa L, Schlegel M, Gebauer P, Ansorge H, Heroldová M, Jánová E, Stanko M, Mošanský L, Fričová J, Pejčoch M, Suchomel J, Purchart L, Groschup MH, Krüger DH, Ulrich RG, Klempa B. 2013. Detection of shrew-borne hantavirus in Eurasian pygmy shrew (Sorex minutus) in central Europe. Infect Genet Evol 19:403–410. doi:10.1016/j.meegid.2013.04.008. PubMed DOI

Schlegel M, Radosa L, Rosenfeld UM, Schmidt S, Triebenbacher C, Löhr P-W, Fuchs D, Heroldová M, Jánová E, Stanko M, Mošanský L, Fričová J, Pejčoch M, Suchomel J, Purchart L, Groschup MH, Krüger DH, Klempa B, Ulrich RG. 2012. Broad geographical distribution and high genetic diversity of shrew-borne Seewis hantavirus in central Europe. Virus Genes 45:48–55. doi:10.1007/s11262-012-0736-7. PubMed DOI

Heyman P, Vaheri A, ENIVD Members . 2008. Situation of hantavirus infections and haemorrhagic fever with renal syndrome in European countries as of December 2006. Euro Surveill 13:18925. doi:10.2807/ese.13.28.18925-en. PubMed DOI

Klempa B, Stanko M, Labuda M, Ulrich R, Meisel H, Krüger DH. 2005. Central European Dobrava hantavirus isolate from a striped field mouse (Apodemus agrarius). J Clin Microbiol 43:2756–2763. doi:10.1128/JCM.43.6.2756-2763.2005. PubMed DOI PMC

Vapalahti O, Mustonen J, Lundkvist A, Henttonen H, Plyusnin A, Vaheri A. 2003. Hantavirus infections in Europe. Lancet Infect Dis 3:653–661. doi:10.1016/s1473-3099(03)00774-6. PubMed DOI

Lee S-H, No JS, Kim W-K, Gajda E, Perec-Matysiak A, Kim J-A, Hildebrand J, Yanagihara R, Song J-W. 2020. Molecular epidemiology and genetic diversity of orthohantaviruses in small mammals in western Poland. Am J Trop Med Hyg 103:193–199. doi:10.4269/ajtmh.19-0802. PubMed DOI PMC

Nemirov K, Vapalahti O, Lundkvist A, Vasilenko V, Golovljova I, Plyusnina A, Niemimaa J, Laakkonen J, Henttonen H, Vaheri A, Plyusnin A. 1999. Isolation and characterization of Dobrava hantavirus carried by the striped field mouse (Apodemus agrarius) in Estonia. J Gen Virol 80:371–379. doi:10.1099/0022-1317-80-2-371. PubMed DOI

Tkachenko EA, Okulova NM, Iunicheva IV, Morzunov SP, Khaĭbulina SF, Riabova TE, Vasilenko LE, Bashkirtsev VN, Dzagurova TK, Gorbachkova EA, Sedova NS, Balakirev AE, Dekonenko AE, Drozdov SG. 2005. The epizootological and virological characteristics of a natural hantavirus infection focus in the subtropic zone of the Krasnodarsk Territory. Vopr Virusol 50:14–19. (In Russian.) PubMed

Kariwa H, Tkachenko EA, Morozov VG, Seto T, Tanikawa Y, Kolominov SI, Belov SN, Nakamura I, Hashimoto N, Balakiev AE, Dzagurnova TK, Daud NHBA, Miyashita D, Medvedkina OA, Nakauchi M, Ishizuka M, Yoshii K, Yoshimatsu K, Arikawa J, Takashima I. 2009. Epidemiological study of hantavirus infection in the Samara Region of European Russia. J Vet Med Sci 71:1569–1578. doi:10.1292/jvms.001569. PubMed DOI

Avšič Županc T, Korva M, Markotić A. 2014. HFRS and hantaviruses in the Balkans/south-east Europe. Virus Res 187:27–33. doi:10.1016/j.virusres.2013.12.042. PubMed DOI

Plyusnina A, Heyman P, Baert K, Stuyck J, Cochez C, Plyusnin A. 2012. Genetic characterization of Seoul hantavirus originated from Norway rats (Rattus norvegicus) captured in Belgium. J Med Virol 84:1298–1303. doi:10.1002/jmv.23321. PubMed DOI

Heroldová M, Pejcoch M, Bryja J, Jánová E, Suchomel J, Tkadlec E. 2010. Tula virus in populations of small terrestrial mammals in a rural landscape. Vector Borne Zoonotic Dis 10:599–603. doi:10.1089/vbz.2009.0211. PubMed DOI

Plyusnin A, Vapalahti O, Lankinen H, Lehväslaiho H, Apekina N, Myasnikov Y, Kallio-Kokko H, Henttonen H, Lundkvist A, Brummer-Korvenkontio M. 1994. Tula virus: a newly detected hantavirus carried by European common voles. J Virol 68:7833–7839. doi:10.1128/JVI.68.12.7833-7839.1994. PubMed DOI PMC

Schlegel M, Kindler E, Essbauer SS, Wolf R, Thiel J, Groschup MH, Heckel G, Oehme RM, Ulrich RG. 2012. Tula virus infections in the Eurasian water vole in central Europe. Vector Borne Zoonotic Dis 12:503–513. doi:10.1089/vbz.2011.0784. PubMed DOI

Klempa B, Meisel H, Räth S, Bartel J, Ulrich R, Krüger DH. 2003. Occurrence of renal and pulmonary syndrome in a region of northeast Germany where Tula hantavirus circulates. J Clin Microbiol 41:4894–4897. doi:10.1128/JCM.41.10.4894-4897.2003. PubMed DOI PMC

Zelená H, Mrázek J, Kuhn T. 2013. Tula hantavirus infection in immunocompromised host, Czech Republic. Emerg Infect Dis 19:1873–1876. doi:10.3201/eid1911.130421. PubMed DOI PMC

Song J-W, Gu SH, Bennett SN, Arai S, Puorger M, Hilbe M, Yanagihara R. 2007. Seewis virus, a genetically distinct hantavirus in the Eurasian common shrew (Sorex araneus). Virol J 4:114. doi:10.1186/1743-422X-4-114. PubMed DOI PMC

Zelená H, Straková P, Heroldová M, Mrázek J, Kastl T, Zakovska A, Ruzek D, Smetana J, Rudolf I. 2019. Molecular epidemiology of hantaviruses in the Czech Republic. Emerg Infect Dis 25:2133–2135. doi:10.3201/eid2511.190449. PubMed DOI PMC

Sironen T, Voutilainen L, Isoviita V-M, Niemimaa J, Vaheri A, Vapalahti O, Henttonen H. 2010. Isolation and characterization of novel insectivore-borne hantaviruses from Finland, VIII. International Conference on HFRS, HPS & Hantaviruses, Beijing, China.

Holmes EC, Zhang Y-Z. 2015. The evolution and emergence of hantaviruses. Curr Opin Virol 10:27–33. doi:10.1016/j.coviro.2014.12.007. PubMed DOI

Jiang F, Wang L, Wang S, Zhu L, Dong L, Zhang Z, Hao B, Yang F, Liu W, Deng Y, Zhang Y, Ma Y, Pan B, Han Y, Ren H, Cao G. 2017. Meteorological factors affect the epidemiology of hemorrhagic fever with renal syndrome via altering the breeding and hantavirus-carrying states of rodents and mites: a 9 years’ longitudinal study. Emerg Microbes Infect 6:e104. doi:10.1038/emi.2017.92. PubMed DOI PMC

Klempa B. 2018. Reassortment events in the evolution of hantaviruses. Virus Genes 54:638–646. doi:10.1007/s11262-018-1590-z. PubMed DOI PMC

National Institute of Public Health. 2021. Incidence of selected infectious diseases in the Czech Republic: incidence rates per 100,000 population in the years 2012-2021. National Institute of Public Health, Prague, Czech Republic.

Krüger DH, Figueiredo LTM, Song J-W, Klempa B. 2015. Hantaviruses—globally emerging pathogens. J Clin Virol 64:128–136. doi:10.1016/j.jcv.2014.08.033. PubMed DOI

Heyman P, Ceianu CS, Christova I, Tordo N, Beersma M, Alves MJ, Lundkvist Å, Hukic M, Papa A, Tenorio A, Zelená H, Eßbauer S, Visontai I, Golovljova I, Connell J, Nicoletti L, Esbroeck MV, Dudman SG, Aberle SW, Avšić-Županc T, Korukluoglu G, Nowakowska A, Klempa B, Ulrich RG, Bino S, Engler O, Opp M, Vaheri A. 2011. A five-year perspective on the situation of haemorrhagic fever with renal syndrome and status of the hantavirus reservoirs in Europe, 2005-2010. Euro Surveill 16:19961. doi:10.2807/ese.16.36.19961-en. PubMed DOI

Faber M, Krüger DH, Auste B, Stark K, Hofmann J, Weiss S. 2019. Molecular and epidemiological characteristics of human Puumala and Dobrava-Belgrade hantavirus infections, Germany, 2001 to 2017. Euro Surveill 24:1800675. doi:10.2807/1560-7917.ES.2019.24.32.1800675. PubMed DOI PMC

Vaheri A, Henttonen H, Voutilainen L, Mustonen J, Sironen T, Vapalahti O. 2013. Hantavirus infections in Europe and their impact on public health. Rev Med Virol 23:35–49. doi:10.1002/rmv.1722. PubMed DOI

European Centre for Disease Prevention and Control. 2021. Hantavirus infection: annual epidemiological report for 2019. European Centre for Disease Prevention and Control, Stockholm, Sweden.

Camp JV, Schmon E, Krause R, Sixl W, Schmid D, Aberle SW. 2021. Genetic diversity of Puumala orthohantavirus in rodents and human patients in Austria, 2012-2019. Viruses 13:640. doi:10.3390/v13040640. PubMed DOI PMC

Hofmann J, Meier M, Enders M, Führer A, Ettinger J, Klempa B, Schmidt S, Ulrich RG, Kruger DH. 2014. Hantavirus disease in Germany due to infection with Dobrava-Belgrade virus genotype Kurkino. Clin Microbiol Infect 20:O648–O655. doi:10.1111/1469-0691.12543. PubMed DOI

Dusek J, Pejcoch M, Kolsky A, Seeman T, Nemec V, Stejskal J, Vondrak K, Janda J. 2006. Mild course of Puumala nephropathy in children in an area with sporadic occurrence hantavirus infection. Pediatr Nephrol 21:1889–1892. doi:10.1007/s00467-006-0250-z. PubMed DOI

Pejčoch M, Unar J, Kříž B, Pauchová E, Rose R. 2010. Characterization of a natural focus of Puumala hantavirus infection in the Czech Republic. Cent Eur J Public Health 18:116–118. doi:10.21101/cejph.a3611. PubMed DOI

Weidmann M, Schmidt P, Vackova M, Krivanec K, Munclinger P, Hufert FT. 2005. Identification of genetic evidence for Dobrava virus spillover in rodents by nested reverse transcription (RT)-PCR and TaqMan RT-PCR. J Clin Microbiol 43:808–812. doi:10.1128/JCM.43.2.808-812.2005. PubMed DOI PMC

Pejčoch M, Kříž B. 2003. Hantaviruses in the Czech Republic. Emerg Infect Dis 9:756–757. doi:10.3201/eid0906.020772. PubMed DOI PMC

Vapalahti O, Lundkvist A, Kukkonen SK, Cheng Y, Gilljam M, Kanerva M, Manni T, Pejcoch M, Niemimaa J, Kaikusalo A, Henttonen H, Vaheri A, Plyusnin A. 1996. Isolation and characterization of Tula virus, a distinct serotype in the genus Hantavirus, family Bunyaviridae. J Gen Virol 77(Part 12):3063–3067. doi:10.1099/0022-1317-77-12-3063. PubMed DOI

Reynes JM, Carli D, Boukezia N, Debruyne M, Herti S. 2015. Tula hantavirus infection in a hospitalised patient, France, June 2015. Euro Surveill 20:30095. doi:10.2807/1560-7917.ES.2015.20.50.30095. PubMed DOI

Voutilainen L, Savola S, Kallio ER, Laakkonen J, Vaheri A, Vapalahti O, Henttonen H. 2012. Environmental change and disease dynamics: effects of intensive forest management on Puumala hantavirus infection in boreal bank vole populations. PLoS One 7:e39452. doi:10.1371/journal.pone.0039452. PubMed DOI PMC

Korva M, Knap N, Resman Rus K, Fajs L, Grubelnik G, Bremec M, Knapič T, Trilar T, Avšič Županc T. 2013. Phylogeographic diversity of pathogenic and non-pathogenic hantaviruses in Slovenia. Viruses 5:3071–3087. doi:10.3390/v5123071. PubMed DOI PMC

Schmidt-Chanasit J, Essbauer S, Petraityte R, Yoshimatsu K, Tackmann K, Conraths FJ, Sasnauskas K, Arikawa J, Thomas A, Pfeffer M, Scharninghausen JJ, Splettstoesser W, Wenk M, Heckel G, Ulrich RG. 2010. Extensive host sharing of central European Tula virus. J Virol 84:459–474. doi:10.1128/JVI.01226-09. PubMed DOI PMC

Nemirov K, Henttonen H, Vaheri A, Plyusnin A. 2002. Phylogenetic evidence for host switching in the evolution of hantaviruses carried by Apodemus mice. Virus Res 90:207–215. doi:10.1016/s0168-1702(02)00179-x. PubMed DOI

Plyusnin A, Vaheri A, Lundkvist Å. 2006. Saaremaa hantavirus should not be confused with its dangerous relative, Dobrava virus. J Clin Microbiol 44:1608–1611. doi:10.1128/JCM.44.4.1608-1611.2006. PubMed DOI PMC

Hjelle B, Yates T. 2001. Modeling hantavirus maintenance and transmission in rodent communities. Curr Top Microbiol Immunol 256:77–90. doi:10.1007/978-3-642-56753-7_5. PubMed DOI

Klingström J, Heyman P, Escutenaire S, Sjölander KB, De Jaegere F, Henttonen H, Lundkvist A. 2002. Rodent host specificity of European hantaviruses: evidence of Puumala virus interspecific spillover. J Med Virol 68:581–588. doi:10.1002/jmv.10232. PubMed DOI

Schmidt S, Saxenhofer M, Drewes S, Schlegel M, Wanka KM, Frank R, Klimpel S, von Blanckenhagen F, Maaz D, Herden C, Freise J, Wolf R, Stubbe M, Borkenhagen P, Ansorge H, Eccard JA, Lang J, Jourdain E, Jacob J, Marianneau P, Heckel G, Ulrich RG. 2016. High genetic structuring of Tula hantavirus. Arch Virol 161:1135–1149. doi:10.1007/s00705-016-2762-6. PubMed DOI

Schlegel M, Klempa B, Auste B, Bemmann M, Schmidt-Chanasit J, Büchner T, Groschup MH, Meier M, Balkema-Buschmann A, Zoller H, Krüger DH, Ulrich RG. 2009. Dobrava-Belgrade virus spillover infections, Germany. Emerg Infect Dis 15:2017–2020. doi:10.3201/eid1512.090923. PubMed DOI PMC

Avšič Županc 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 81:1747–1755. doi:10.1099/0022-1317-81-7-1747. PubMed DOI

Dervović E, Hukić M. 2016. Detection of Puumala virus in the tissue of infected naturally rodent hosts in the area of central Dinarides. J Virol Methods 230:24–27. doi:10.1016/j.jviromet.2016.01.007. PubMed DOI

Maas M, van Heteren M, de Vries A, Kuiken T, Hoornweg T, Veldhuis Kroeze E, Rockx B. 2019. Seoul virus tropism and pathology in naturally infected feeder rats. Viruses 11:531. doi:10.3390/v11060531. PubMed DOI PMC

Resman K, Korva M, Fajs L, Zidarič T, Trilar T, Županc TA. 2013. Molecular evidence and high genetic diversity of shrew-borne Seewis virus in Slovenia. Virus Res 177:113–117. doi:10.1016/j.virusres.2013.07.011. PubMed DOI

Ling J, Smura T, Tamarit D, Huitu O, Voutilainen L, Henttonen H, Vaheri A, Vapalahti O, Sironen T. 2018. Evolution and postglacial colonization of Seewis hantavirus with Sorex araneus in Finland. Infect Genet Evol 57:88–97. doi:10.1016/j.meegid.2017.11.010. PubMed DOI

Bellinvia E. 2004. A phylogenetic study of the genus Apodemus by sequencing the mitochondrial DNA control region. J Zool Syst Ecol Res 42:289–297. doi:10.1111/j.1439-0469.2004.00270.x. DOI

Schlegel M, Ali HS, Stieger N, Groschup MH, Wolf R, Ulrich RG. 2012. Molecular identification of small mammal species using novel cytochrome b gene-derived degenerated primers. Biochem Genet 50:440–447. doi:10.1007/s10528-011-9487-8. PubMed DOI

Klempa B, Fichet-Calvet E, Lecompte E, Auste B, Aniskin V, Meisel H, Denys C, Koivogui L, ter Meulen J, Krüger DH. 2006. Hantavirus in African wood mouse, Guinea. Emerg Infect Dis 12:838–840. doi:10.3201/eid1205.051487. PubMed DOI PMC

Hall T. 1999. Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT.

Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. doi:10.1093/nar/22.22.4673. PubMed DOI PMC

Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. doi:10.1093/bioinformatics/btg180. PubMed DOI

Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704. doi:10.1080/10635150390235520. PubMed DOI

Posada D. 2008. jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256. doi:10.1093/molbev/msn083. PubMed DOI

Posada D. 2009. Selection of models of DNA evolution with jModelTest. Methods Mol Biol 537:93–112. doi:10.1007/978-1-59745-251-9_5. PubMed DOI

Page RD. 1996. TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358. doi:10.1093/bioinformatics/12.4.357. PubMed DOI

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