1887

Abstract

The wide circulation of novel avian influenza viruses (AIVs) highlights the risk of pandemic influenza emergence in China. To investigate the prevalence and genetic diversity of AIVs in different ecological contexts, we surveyed AIVs in live poultry markets (LPMs), free-range poultry and the wetland habitats of wild birds in Zhejiang and Hubei provinces. Notably, LPMs contained the highest frequency of AIV infection, and the greatest number of subtypes ( = 9) and subtype co-infections ( = 14), as well as frequent reassortment, suggesting that they play an active role in fuelling AIV transmission. AIV-positive samples were also identified in wild birds in both provinces and free-range poultry in one sampling site close to a wetland region in Hubei. H9N2, H7N9 and H5N1 were the most commonly sampled subtypes in the LPMs from Zhejiang, whilst H5N6 and H9N2 were the dominant subtypes in the LPMs from Hubei. Phylogenetic analyses of the whole-genome sequences of 43 AIVs revealed that three reassortant H5 subtypes were circulating in LMPs in both geographical regions. Notably, the viruses sampled from the wetland regions and free-range poultry contained complex reassortants, for which the origins of some segments were unclear. Overall, our study highlights the extent of AIV genetic diversity in two highly populated parts of central and south-eastern China, particularly in LPMs, and emphasizes the need for continual surveillance.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000399
2016-04-01
2019-12-11
Loading full text...

Full text loading...

/deliver/fulltext/jgv/97/4/844.html?itemId=/content/journal/jgv/10.1099/jgv.0.000399&mimeType=html&fmt=ahah

References

  1. Bi Y., Mei K., Shi W., Liu D., Yu X., Gao Z., Zhao L., Gao G. F., Chen J., Chen Q.. 2015; Two novel reassortants of avian influenza A (H5N6) virus in China. J Gen Virol96:975–981 [CrossRef][PubMed]
    [Google Scholar]
  2. Butt K. M., Smith G. J., Chen H., Zhang L. J., Leung Y. H., Xu K. M., Lim W., Webster R. G., Yuen K. Y., other authors. 2005; Human infection with an avian H9N2 influenza A virus in Hong Kong in 2003. J Clin Microbiol43:5760–5767 [CrossRef][PubMed]
    [Google Scholar]
  3. Chen H., Yuan H., Gao R., Zhang J., Wang D., Xiong Y., Fan G., Yang F., Li X., other authors. 2014; Clinical and epidemiological characteristics of a fatal case of avian influenza A H10N8 virus infection: a descriptive study. Lancet383:714–721 [CrossRef][PubMed]
    [Google Scholar]
  4. Claas E. C., Osterhaus A. D., van Beek R., De Jong J. C., Rimmelzwaan G. F., Senne D. A., Krauss S., Shortridge K. F., Webster R. G.. 1998; Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. Lancet351:472–477 [CrossRef][PubMed]
    [Google Scholar]
  5. Gao R., Cao B., Hu Y., Feng Z., Wang D., Hu W., Chen J., Jie Z., Qiu H., other authors. 2013; Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med368:1888–1897 [CrossRef][PubMed]
    [Google Scholar]
  6. Guan Y., Smith G. J.. 2013; The emergence and diversification of panzootic H5N1 influenza viruses. Virus Res178:35–43 [CrossRef][PubMed]
    [Google Scholar]
  7. Guan Y., Shortridge K. F., Krauss S., Webster R. G.. 1999; Molecular characterization of H9N2 influenza viruses: were they the donors of the ‘internal’ genes of H5N1 viruses in Hong Kong?. Proc Natl Acad Sci U S A96:9363–9367 [CrossRef][PubMed]
    [Google Scholar]
  8. 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 Biol59:307–321 [CrossRef][PubMed]
    [Google Scholar]
  9. Hall T. A.. 1999; BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp41:95–98
    [Google Scholar]
  10. Hoffmann E., Stech J., Guan Y., Webster R. G., Perez D. R.. 2001; Universal primer set for the full-length amplification of all influenza A viruses. Arch Virol146:2275–2289 [CrossRef][PubMed]
    [Google Scholar]
  11. Kuiken T., Holmes E. C., McCauley J., Rimmelzwaan G. F., Williams C. S., Grenfell B. T.. 2006; Host species barriers to influenza virus infections. Science312:394–397 [CrossRef][PubMed]
    [Google Scholar]
  12. Lam T. T., Wang J., Shen Y., Zhou B., Duan L., Cheung C. L., Ma C., Lycett S. J., Leung C. Y., other authors. 2013; The genesis and source of the H7N9 influenza viruses causing human infections in China. Nature502:241–244 [CrossRef][PubMed]
    [Google Scholar]
  13. Lam T. T., Zhou B., Wang J., Chai Y., Shen Y., Chen X., Ma C., Hong W., Chen Y., other authors. 2015; Dissemination, divergence and establishment of H7N9 influenza viruses in China. Nature522:102–105 [CrossRef][PubMed]
    [Google Scholar]
  14. Li C., Chen H.. 2014; Enhancement of influenza virus transmission by gene reassortment. Curr Top Microbiol Immunol385:185–204[PubMed]
    [Google Scholar]
  15. Li K. S., Guan Y., Wang J., Smith G. J., Xu K. M., Duan L., Rahardjo A. P., Puthavathana P., Buranathai C., other authors. 2004; Genesis of a highly pathogenic and potentially pandemic H5N1 influenza virus in eastern Asia. Nature430:209–213 [CrossRef][PubMed]
    [Google Scholar]
  16. Liu M., He S., Walker D., Zhou N., Perez D. R., Mo B., Li F., Huang X., Webster R. G., Webby R. J.. 2003; The influenza virus gene pool in a poultry market in south central China. Virology305:267–275 [CrossRef][PubMed]
    [Google Scholar]
  17. Ma C., Lam T. T., Chai Y., Wang J., Fan X., Hong W., Zhang Y., Li L., Liu Y., other authors. 2015; Emergence and evolution of H10 subtype influenza viruses in poultry in China. J Virol89:3534–3541 [CrossRef][PubMed]
    [Google Scholar]
  18. Madsen J. M., Zimmermann N. G., Timmons J., Tablante N. L.. 2013; Avian influenza seroprevalence and biosecurity risk factors in Maryland backyard poultry: a cross-sectional study. PLoS One8:e56851 [CrossRef][PubMed]
    [Google Scholar]
  19. Marinova-Petkova A., Feeroz M. M., Rabiul Alam S. M., Kamrul Hasan M., Akhtar S., Jones-Engel L., Walker D., McClenaghan L., Rubrum A., other authors. 2014; Multiple introductions of highly pathogenic avian influenza H5N1 viruses into Bangladesh. Emerg Microbes Infect3:e11 [CrossRef][PubMed]
    [Google Scholar]
  20. Matsuoka Y., Swayne D. E., Thomas C., Rameix-Welti M. A., Naffakh N., Warnes C., Altholtz M., Donis R., Subbarao K.. 2009; Neuraminidase stalk length and additional glycosylation of the hemagglutinin influence the virulence of influenza H5N1 viruses for mice. J Virol83:4704–4708 [CrossRef][PubMed]
    [Google Scholar]
  21. Pantin-Jackwood M. J., Miller P. J., Spackman E., Swayne D. E., Susta L., Costa-Hurtado M., Suarez D. L.. 2014; Role of poultry in the spread of novel H7N9 influenza virus in China. J Virol88:5381–5390 [CrossRef][PubMed]
    [Google Scholar]
  22. Stegeman A., Bouma A., Elbers A. R., de Jong M. C., Nodelijk G., de Klerk F., Koch G., van Boven M.. 2004; Avian influenza A virus (H7N7) epidemic in The Netherlands in 2003: course of the epidemic and effectiveness of control measures. J Infect Dis190:2088–2095 [CrossRef][PubMed]
    [Google Scholar]
  23. Stieneke-Gröber A., Vey M., Angliker H., Shaw E.,Thomas,G., Roberts C., Klenk H. D., Garten W.. 1992; Influenza virus hemagglutinin with multibasic cleavage site is activated by furin, a subtilisin-like endoprotease. EMBO J 11, 2407–2414
    [Google Scholar]
  24. Su S., Bi Y., Wong G., Gray G. C., Gao G. F., Li S.. 2015; Epidemiology, evolution, and recent outbreaks of avian influenza virus in China. J Virol89:8671–8676 [CrossRef][PubMed]
    [Google Scholar]
  25. 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 Evol28:2731–2739 [CrossRef][PubMed]
    [Google Scholar]
  26. Tian H., Zhou S., Dong L., Van Boeckel T. P., Cui Y., Newman S. H., Takekawa J. Y., Prosser D. J., Xiao X., other authors. 2015; Avian influenza H5N1 viral and bird migration networks in Asia. Proc Natl Acad Sci U S A112:172–177 [CrossRef][PubMed]
    [Google Scholar]
  27. Tong S., Zhu X., Li Y., Shi M., Zhang J., Bourgeois M., Yang H., Chen X., Recuenco S., other authors. 2013; New world bats harbor diverse influenza A viruses. PLoS Pathog9:e1003657 [CrossRef][PubMed]
    [Google Scholar]
  28. Webster R. G., Bean W. J., Gorman O. T., Chambers T. M., Kawaoka Y.. 1992; Evolution and ecology of influenza A viruses. Microbiol Rev56:152–179[PubMed]
    [Google Scholar]
  29. Wei S. H., Yang J. R., Wu H. S., Chang M. C., Lin J. S., Lin C. Y., Liu Y. L., Lo Y. C., Yang C. H., other authors. 2013; Human infection with avian influenza A H6N1 virus: an epidemiological analysis. Lancet Respir Med1:771–778 [CrossRef][PubMed]
    [Google Scholar]
  30. WHO 2015; http://www.who.int/csr/don/15-june-2015-avian-influenza-china/en/ Influenza at the Human–Animal Interface. Summary and Assessment. Available at:. http://www.who.int/csr/don/15-june-2015-avian-influenza-china/en/.
  31. Wong F. Y., Phommachanh P., Kalpravidh W., Chanthavisouk C., Gilbert J., Bingham J., Davies K. R., Cooke J., Eagles D., other authors. 2015; Reassortant highly pathogenic influenza A(H5N6) virus in Laos. Emerg Infect Dis21:511–516 [CrossRef][PubMed]
    [Google Scholar]
  32. Wu H., Peng X., Xu L., Jin C., Cheng L., Lu X., Xie T., Yao H., Wu N.. 2014; Novel reassortant influenza A(H5N8) viruses in domestic ducks, eastern China. Emerg Infect Dis20:1315–1318 [CrossRef][PubMed]
    [Google Scholar]
  33. Wu H., Lu R., Peng X., Xu L., Cheng L., Lu X., Jin C., Xie T., Yao H., Wu N.. 2015; Novel reassortant highly pathogenic H5N6 avian influenza viruses in poultry in China. Infect Genet Evol31:64–67 [CrossRef][PubMed]
    [Google Scholar]
  34. Xu H., Meng F., Huang D., Sheng X., Wang Y., Zhang W., Chang W., Wang L., Qin Z.. 2015; Genomic and phylogenetic characterization of novel, recombinant H5N2 avian influenza virus strains isolated from vaccinated chickens with clinical symptoms in China. Viruses7:887–898 [CrossRef][PubMed]
    [Google Scholar]
  35. Yang Z. F., Mok C. K., Peiris J. S., Zhong N. S.. 2015; Human infection with a novel avian influenza A (H5N6) virus. N Engl J Med373:487–489 [CrossRef][PubMed]
    [Google Scholar]
  36. Yu Y., Wang X., Jin T., Wang H., Si W., Yang H., Wu J., Yan Y., Liu G..other authors 2015a; Newly emergent highly pathogenic H5N9 subtype avian influenza A virus. J Virol89:8806–8815 [CrossRef][PubMed]
    [Google Scholar]
  37. Yu Z., Gao X., Wang T., Li Y., Li y., Xu Y., Chu D., Sun H., Wu C.&otherauthors. 2015b; Fatal H5N6 avian influenza virus infection in a domestic cat and wild birds in China. Sci Rep5:10704 [CrossRef][PubMed]
    [Google Scholar]
  38. Zhou H., Yu Z., Hu Y., Tu J., Zou W., Peng Y., Zhu J., Li Y., Zhang A., other authors. 2009; The special neuraminidase stalk-motif responsible for increased virulence and pathogenesis of H5N1 influenza A virus. PLoS One4:e6277 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000399
Loading
/content/journal/jgv/10.1099/jgv.0.000399
Loading

Data & Media loading...

Supplements

Supplementary Data

PDF

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