1887

Journal of General Virology header logo

Volume 96, Issue 2

H7N9 influenza A virus in turkeys in Minnesota Free

Abstract

Introductions of H7 influenza A virus (IAV) from wild birds into poultry have been documented worldwide, resulting in varying degrees of morbidity and mortality. H7 IAV infection in domestic poultry has served as a source of human infection and disease. We report the detection of H7N9 subtype IAVs in Minnesota (MN) turkey farms during 2009 and 2011. The full genome was sequenced from eight isolates as well as the haemagglutinin (HA) and neuraminidase (NA) gene segments of H7 and N9 virus subtypes for 108 isolates from North American wild birds between 1986 and 2012. Through maximum-likelihood and coalescent phylogenetic analyses, we identified the recent H7 and N9 IAV ancestors of the turkey-origin H7N9 IAVs, estimated the time and geographical origin of the ancestral viruses, and determined the relatedness between the 2009 and 2011 turkey-origin H7N9 IAVs. Analyses supported that the 2009 and 2011 viruses were distantly related genetically, suggesting that the two outbreaks arose from independent introduction events from wild birds. Our findings further supported that the 2011 MN turkey-origin H7N9 virus was closely related to H7N9 IAVs isolated in poultry in Nebraska during the same year. Although the precise origin of the wild-bird donor of the turkey-origin H7N9 IAVs could not be determined, our findings suggested that, for both the NA and HA gene segments, the MN turkey-origin H7N9 viruses were related to viruses circulating in wild birds between 2006 and 2011 in the Mississippi Flyway.

  • Received:
  • Accepted:
  • Published Online:
© 2015 The Authors
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.067504-0
2015-02-01
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/jgv/96/2/269.html?itemId=/content/journal/jgv/10.1099/vir.0.067504-0&mimeType=html&fmt=ahah

References

  1. Bahl J., Vijaykrishna D., Holmes E. C., Smith G. J. D., Guan Y. 2009; Gene flow and competitive exclusion of avian influenza A virus in natural reservoir hosts. Virology 390:289–297 [View Article][PubMed]
     [Google Scholar]
  2. Bahl J., Krauss S., Kühnert D., Fourment M., Raven G., Pryor S. P., Niles L. J., Danner A., Walker D. et al. 2013; Influenza A virus migration and persistence in North American wild birds. PLoS Pathog 9:e1003570 [View Article][PubMed]
     [Google Scholar]
  3. Bao Y., Bolotov P., Dernovoy D., Kiryutin B., Zaslavsky L., Tatusova T., Ostell J., Lipman D. 2008; The influenza virus resource at the National Center for Biotechnology Information. J Virol 82:596–601 [View Article][PubMed]
     [Google Scholar]
  4. Chen R., Holmes E. C. 2009; Frequent inter-species transmission and geographic subdivision in avian influenza viruses from wild birds. Virology 383:156–161 [View Article][PubMed]
     [Google Scholar]
  5. Dortmans J. C. F. M., Dekkers J., Wickramasinghe I. N. A., Verheije M. H., Rottier P. J. M., van Kuppeveld F. J. M., de Vries E., de Haan C. A. M. 2013; Adaptation of novel H7N9 influenza A virus to human receptors. Sci Rep 3:3058 [View Article][PubMed]
     [Google Scholar]
  6. Drummond A. J., Rambaut A. 2007; beast: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214 [View Article][PubMed]
     [Google Scholar]
  7. Drummond A. J., Rambaut A., Shapiro B., Pybus O. G. 2005; Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192 [View Article][PubMed]
     [Google Scholar]
  8. Felsenstein J. 2005; phylip (Phylogeny Inference Package). , version 3.6. http://evolution.genetics.washington.edu/phylip.html
  9. Gao R., Cao B., Hu Y., Feng Z., Wang D., Hu W., Chen J., Jie Z., Qiu H. et al. 2013; Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med 368:1888–1897 [View Article][PubMed]
     [Google Scholar]
  10. Guindon S., Dufayard J. F., Lefort V., Anisimova M., Hordijk W., Gascuel O. 2010; New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321 [View Article][PubMed]
     [Google Scholar]
  11. Imai M., Kawaoka Y. 2012; The role of receptor binding specificity in interspecies transmission of influenza viruses. Curr Opin Virol 2:160–167 [View Article][PubMed]
     [Google Scholar]
  12. Jonges M., Meijer A., Fouchier R. A., Koch G., Li J., Pan J. C., Chen H., Shu Y. L., Koopmans M. P. 2013; Guiding outbreak management by the use of influenza A(H7Nx) virus sequence analysis. Euro Surveill 18:20460[PubMed]
     [Google Scholar]
  13. Killian M. L. 2010; National Veterinary Services Laboratories Avian Influenza and Newcastle Disease Diagnostics Report. In Proceedings of the 113 Annual Meeting of the US Animal Health Association pp. 590–593 St Joseph, MO: USAHA
    [Google Scholar]
  14. Krasnitz M., Levine A. J., Rabadan R. 2008; Anomalies in the influenza virus genome database: new biology or laboratory errors?. J Virol 82:8947–8950 [View Article][PubMed]
     [Google Scholar]
  15. Lam T. T., Ip H. S., Ghedin E., Wentworth D. E., Halpin R. A., Stockwell T. B., Spiro D. J., Dusek R. J., Bortner J. B. et al. 2012; Migratory flyway and geographical distance are barriers to the gene flow of influenza virus among North American birds. Ecol Lett 15:24–33 [View Article][PubMed]
     [Google Scholar]
  16. Lam T. T., Wang J., Shen Y., Zhou B., Duan L., Cheung C. L., Ma C., Lycett S. J., Leung C. Y. et al. 2013; The genesis and source of the H7N9 influenza viruses causing human infections in China. Nature 502:241–244 [View Article][PubMed]
     [Google Scholar]
  17. Lebarbenchon C., Stallknecht D. E. 2011; Host shifts and molecular evolution of H7 avian influenza virus hemagglutinin. Virol J 8:328 [View Article][PubMed]
     [Google Scholar]
  18. Lebarbenchon C., Brown J. D., Stallknecht D. E. 2013; Evolution of influenza A virus H7 and N9 subtypes, Eastern Asia. Emerg Infect Dis 19:1635–1638 [View Article][PubMed]
     [Google Scholar]
  19. Lemey P., Rambaut A., Drummond A. J., Suchard M. A. 2009; Bayesian phylogeography finds its roots. PLOS Comput Biol 5:e1000520 [View Article][PubMed]
     [Google Scholar]
  20. Liu D., Shi W., Shi Y., Wang D., Xiao H., Li W., Bi Y., Wu Y., Li X. et al. 2013; Origin and diversity of novel avian influenza A H7N9 viruses causing human infection: phylogenetic, structural, and coalescent analyses. Lancet 381:1926–1932 [View Article][PubMed]
     [Google Scholar]
  21. 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 [View Article][PubMed]
     [Google Scholar]
  22. Pedersen J. 2012; National Veterinary Services Laboratories Avian Influenza and Newcastle Disease Diagnostics Report. Proceedings of the 115 Annual Meeting of the US Animal Health Association pp. 446–449 St Joseph, MO: USAHA
    [Google Scholar]
  23. Ramey A. M., Poulson R. L., González-Reiche A. S., Wilcox B. R., Walther P., Link P., Carter D. L., Newsome G. M., Müller M. L. et al. 2014; Evidence for seasonal patterns in the relative abundance of avian influenza virus subtypes in Blue-winged Teal (Anas discors). J Wildl Dis 50:916–922 [View Article][PubMed]
     [Google Scholar]
  24. Reeves A. B., Pearce J. M., Ramey A. M., Meixell B. W., Runstadler J. A. 2011; Interspecies transmission and limited persistence of low pathogenic avian influenza genomes among Alaska dabbling ducks. Infect Genet Evol 11:2004–2010 [View Article][PubMed]
     [Google Scholar]
  25. Senne D. A., Suarez D. L., Pedersen J. C., Panigrahy B. 2003; Molecular and biological characteristics of H5 and H7 avian influenza viruses in live-bird markets of the northeastern United States, 1994–2001. Avian Dis 47:Suppl898–904 [View Article][PubMed]
     [Google Scholar]
  26. Shapiro B., Rambaut A., Drummond A. J. 2006; Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol Biol Evol 23:7–9 [View Article][PubMed]
     [Google Scholar]
  27. Spackman E., Senne D. A., Davison S., Suarez D. L. 2003; Sequence analysis of recent H7 avian influenza viruses associated with three different outbreaks in commercial poultry in the United States. J Virol 77:13399–13402 [View Article][PubMed]
     [Google Scholar]
  28. Wilcox B. R., Knutsen G. A., Berdeen J., Goekjian V., Poulson R., Goyal S., Sreevatsan S., Cardona C., Berghaus R. D. et al. 2011; Influenza-A viruses in ducks in northwestern Minnesota: fine scale spatial and temporal variation in prevalence and subtype diversity. PLoS ONE 6:e24010 [View Article][PubMed]
     [Google Scholar]
  29. Wu Y., Bi Y., Vavricka C. J., Sun X., Zhang Y., Gao F., Zhao M., Xiao H., Qin C. et al. 2013; Characterization of two distinct neuraminidases from avian-origin human-infecting H7N9 influenza viruses. Cell Res 23:1347–1355 [View Article][PubMed]
     [Google Scholar]
  30. Xiong X., Martin S. R., Haire L. F., Wharton S. A., Daniels R. S., Bennett M. S., McCauley J. W., Collins P. J., Walker P. A. et al. 2013; Receptor binding by an H7N9 influenza virus from humans. Nature 499:496–499 [View Article][PubMed]
     [Google Scholar]
  31. Zhang Z., Schwartz S., Wagner L., Miller W. 2000; A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.067504-0
Loading
H7N9 influenza A virus in turkeys in Minnesota
J. Gen. Virol. 96, 269 (2015); https://doi.org/10.1099/vir.0.067504-0
/content/journal/jgv/10.1099/vir.0.067504-0
/content/journal/jgv/10.1099/vir.0.067504-0
Loading

Data & Media loading...

Supplements

Supplementary Data

PDF

Most cited Most Cited RSS feed

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