1887

Abstract

The avian-like swine influenza viruses emerged in 1979 in Belgium and Germany. Thereafter, they spread through many European swine-producing countries, replaced the circulating classical swine H1N1 influenza viruses, and became endemic. Serological and subsequent molecular data indicated an avian source, but details remained obscure due to a lack of relevant avian influenza virus sequence data. Here, the origin of the European avian-like swine influenza viruses was analysed using a collection of 16 European swine H1N1 influenza viruses sampled in 1979–1981 in Germany, the Netherlands, Belgium, Italy and France, as well as several contemporaneous avian influenza viruses of various serotypes. The phylogenetic trees suggested a triple reassortant with a unique genotype constellation. Time-resolved maximum clade credibility trees indicated times to the most recent common ancestors of 34–46 years (before 2008) depending on the RNA segment and the method of tree inference.

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2014-11-01
2019-11-18
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References

  1. Brown I. H., Harris P. A., McCauley J. W., Alexander D. J.. ( 1998;). Multiple genetic reassortment of avian and human influenza A viruses in European pigs, resulting in the emergence of an H1N2 virus of novel genotype. . J Gen Virol 79:, 2947–2955.[PubMed]
    [Google Scholar]
  2. Campitelli L., Donatelli I., Foni E., Castrucci M. R., Fabiani C., Kawaoka Y., Krauss S., Webster R. G.. ( 1997;). Continued evolution of H1N1 and H3N2 influenza viruses in pigs in Italy. . Virology 232:, 310–318. [CrossRef][PubMed]
    [Google Scholar]
  3. Castrucci M. R., Donatelli I., Sidoli L., Barigazzi G., Kawaoka Y., Webster R. G.. ( 1993;). Genetic reassortment between avian and human influenza A viruses in Italian pigs. . Virology 193:, 503–506. [CrossRef][PubMed]
    [Google Scholar]
  4. Drummond A. J., Suchard M. A., Xie D., Rambaut A.. ( 2012;). Bayesian phylogenetics with BEAUti and the beast 1.7. . Mol Biol Evol 29:, 1969–1973. [CrossRef][PubMed]
    [Google Scholar]
  5. Jagger B. W., Wise H. M., Kash J. C., Walters K. A., Wills N. M., Xiao Y. L., Dunfee R. L., Schwartzman L. M., Ozinsky A.. & other authors ( 2012;). An overlapping protein-coding region in influenza A virus segment 3 modulates the host response. . Science 337:, 199–204. [CrossRef][PubMed]
    [Google Scholar]
  6. Jhung M. A., Epperson S., Biggerstaff M., Allen D., Balish A., Barnes N., Beaudoin A., Berman L., Bidol S.. & other authors ( 2013;). Outbreak of variant influenza A(H3N2) virus in the United States. . Clin Infect Dis 57:, 1703–1712. [CrossRef][PubMed]
    [Google Scholar]
  7. Krumbholz A., Philipps A., Oehring H., Schwarzer K., Eitner A., Wutzler P., Zell R.. ( 2011;). Current knowledge on PB1-F2 of influenza A viruses. . Med Microbiol Immunol (Berl) 200:, 69–75. [CrossRef][PubMed]
    [Google Scholar]
  8. Lange J., Groth M., Schlegel M., Krumbholz A., Wieczorek K., Ulrich R., Köppen S., Schulz K., Appl D.. & other authors ( 2013;). Reassortants of the pandemic (H1N1) 2009 virus and establishment of a novel porcine H1N2 influenza virus, lineage in Germany. . Vet Microbiol 167:, 345–356. [CrossRef][PubMed]
    [Google Scholar]
  9. Lange J., Groth M., Kanrai P., Pleschka S., Scholtissek C., Dürrwald R., Platzer M., Sauerbrei A., Zell R.. ( 2014;). Circulation of classical swine influenza virus in Europe between the wars?. Arch Virol 159:, 1467–1473. [CrossRef][PubMed]
    [Google Scholar]
  10. Lu G., Rowley T., Garten R., Donis R. O.. ( 2007;). FluGenome: a web tool for genotyping influenza A virus. . Nucleic Acids Res 35: (Web Server issue), W275–W279. [CrossRef][PubMed]
    [Google Scholar]
  11. Mayr E.. ( 1954;). Change of genetic environment and evolution. . In Evolution as a Process, pp. 156–180. Edited by Huxley J. S., Hardy A. C., Ford E. B... London:: Allen & Unwin;.
    [Google Scholar]
  12. McCauley J. W., Hongo S., Kaverin N. V., Kochs G., Lamb R. A., Matrosovich M. N., Perez D. R., Palese P., Presti R. M.. & other authors ( 2012;). Family Orthomyxoviridae. . In: Virus Taxonomy, Ninth Report of the International Committee on Taxonomy of Viruses, pp. 749–761. Edited by King A. M. Q., Adams M. J., Carstens E. B., Lefkowitz E. J... Amsterdam:: Elsevier;.
  13. Nelli R. K., Kuchipudi S. V., White G. A., Perez B. B., Dunham S. P., Chang K. C.. ( 2010;). Comparative distribution of human and avian type sialic acid influenza receptors in the pig. . BMC Vet Res 6:, 4. [CrossRef][PubMed]
    [Google Scholar]
  14. Nelson M. I., Vincent A. L., Kitikoon P., Holmes E. C., Gramer M. R.. ( 2012;). Evolution of novel reassortant A/H3N2 influenza viruses in North American swine and humans, 2009–2011. . J Virol 86:, 8872–8878. [CrossRef][PubMed]
    [Google Scholar]
  15. Olsen B., Munster V. J., Wallensten A., Waldenström J., Osterhaus A. D. M. E., Fouchier R. A. M.. ( 2006;). Global patterns of influenza a virus in wild birds. . Science 312:, 384–388. [CrossRef][PubMed]
    [Google Scholar]
  16. Ottis K., Bachmann P. A.. ( 1980;). Occurrence of Hsw 1 N 1 subtype influenza A viruses in wild ducks in Europe. . Arch Virol 63:, 185–190. [CrossRef][PubMed]
    [Google Scholar]
  17. Pensaert M., Ottis K., Vandeputte J., Kaplan M. M., Bachmann P. A.. ( 1981;). Evidence for the natural transmission of influenza A virus from wild ducts to swine and its potential importance for man. . Bull World Health Organ 59:, 75–78.[PubMed]
    [Google Scholar]
  18. Ronquist F., Huelsenbeck J. P.. ( 2003;). MrBayes 3: Bayesian phylogenetic inference under mixed models. . Bioinformatics 19:, 1572–1574. [CrossRef][PubMed]
    [Google Scholar]
  19. Scholtissek C., Bürger H., Bachmann P. A., Hannoun C.. ( 1983;). Genetic relatedness of hemagglutinins of the H1 subtype of influenza A viruses isolated from swine and birds. . Virology 129:, 521–523. [CrossRef][PubMed]
    [Google Scholar]
  20. Scholtissek C., Bürger H., Kistner O., Shortridge K. F.. ( 1985;). The nucleoprotein as a possible major factor in determining host specificity of influenza H3N2 viruses. . Virology 147:, 287–294. [CrossRef][PubMed]
    [Google Scholar]
  21. Schultz-Cherry S., Olsen C. W., Easterday B. C.. ( 2013;). History of swine influenza. . Curr Top Microbiol Immunol 370:, 21–28.[PubMed]
    [Google Scholar]
  22. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S.. ( 2011;). mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. . Mol Biol Evol 28:, 2731–2739. [CrossRef][PubMed]
    [Google Scholar]
  23. Templeton A. R.. ( 1980;). The theory of speciation via the founder principle. . Genetics 94:, 1011–1038.[PubMed]
    [Google Scholar]
  24. Trebbien R., Larsen L. E., Viuff B. M.. ( 2011;). Distribution of sialic acid receptors and influenza A virus of avian and swine origin in experimentally infected pigs. . Virol J 8:, 434. [CrossRef][PubMed]
    [Google Scholar]
  25. Van Poucke S. G., Nicholls J. M., Nauwynck H. J., Van Reeth K.. ( 2010;). Replication of avian, human and swine influenza viruses in porcine respiratory explants and association with sialic acid distribution. . Virol J 7:, 38. [CrossRef][PubMed]
    [Google Scholar]
  26. Webster R. G., Bean W. J., Gorman O. T., Chambers T. M., Kawaoka Y.. ( 1992;). Evolution and ecology of influenza A viruses. . Microbiol Rev 56:, 152–179.[PubMed]
    [Google Scholar]
  27. Witte K. K., Nienhoff H., Ernst H., Schmidt U., Prager D.. ( 1981;). Erstmaliges Auftreten einer durch das Schweineinfluenzavirus verursachten Epizootie in Schweinebeständen der Bundesrepublik Deutschland. . Tierarztl Umsch 36:, 591–606 (in German).
    [Google Scholar]
  28. Wu Y., Wu Y., Tefsen B., Shi Y., Gao G. F.. ( 2014;). Bat-derived influenza-like viruses H17N10 and H18N11. . Trends Microbiol 22:, 183–191. [CrossRef][PubMed]
    [Google Scholar]
  29. Zell R., Bergmann S., Krumbholz A., Wutzler P., Dürrwald R.. ( 2008;). Ongoing evolution of swine influenza viruses: a novel reassortant. . Arch Virol 153:, 2085–2092. [CrossRef][PubMed]
    [Google Scholar]
  30. Zell R., Scholtissek C., Ludwig S.. ( 2013;). Genetics, evolution, and the zoonotic capacity of European swine influenza viruses. . Curr Top Microbiol Immunol 370:, 29–55.[PubMed]
    [Google Scholar]
  31. Zhou N. N., Senne D. A., Landgraf J. S., Swenson S. L., Erickson G., Rossow K., Liu L., Yoon K. J., Krauss S., Webster R. G.. ( 1999;). Genetic reassortment of avian, swine, and human influenza A viruses in American pigs. . J Virol 73:, 8851–8856.
    [Google Scholar]
  32. Zhu H., Webby R., Lam T. T. Y., Smith D. K., Peiris J. S. M., Guan Y.. ( 2013;). History of swine influenza viruses in Asia. . Curr Top Microbiol Immunol 370:, 57–68.[PubMed]
    [Google Scholar]
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