1887

Abstract

Both H9N2 avian influenza and 2009 pandemic H1N1 viruses (pH1N1) are able to infect humans and swine, which has raised concerns that novel reassortant H9 viruses with pH1N1 genes might be generated in these hosts by reassortment. Although previous studies have demonstrated that reassortant H9 viruses with pH1N1 genes show increased virulence in mice and transmissibility in ferrets, the virulence and transmissibility of reassortant H9 viruses in natural hosts such as chickens and swine remain unknown. This study generated two reassortant H9 viruses (H9N2/CA09 and H9N1/CA09) in the background of the pH1N1 A/California/04/2009 (CA09) virus by replacing either both the haemagglutinin (HA) and neuraminidase (NA) genes or only the HA gene with the respective genes from the A/quail/Hong Kong/G1/1997 (H9N2) virus and evaluated their replication, pathogenicity and transmission in chickens and pigs compared with the parental viruses. Chickens that were infected with the parental H9N2 and reassortant H9 viruses seroconverted. The parental H9N2 and reassortant H9N2/CA09 viruses were transmitted to sentinel chickens, but H9N1/CA09 virus was not. The parental H9N2 replicated poorly and was not transmitted in pigs, whereas both H9N2/CA09 and H9N1/CA09 viruses replicated and were transmitted efficiently in pigs, similar to the pH1N1 virus. These results demonstrated that reassortant H9 viruses with pH1N1 genes show enhanced replication and transmissibility in pigs compared with the parental H9N2 virus, indicating that they may pose a threat for humans if such reassortants arise in swine.

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2012-11-01
2019-12-12
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References

  1. Bi J. , Deng G. , Dong J. , Kong F. , Li X. , Xu Q. , Zhang M. , Zhao L. , Qiao J. . ( 2010; ). Phylogenetic and molecular characterization of H9N2 influenza isolates from chickens in Northern China from 2007–2009. . PLoS ONE 5:, e13063. [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 Microbiol 43:, 5760–5767. [CrossRef] [PubMed]
    [Google Scholar]
  3. Butt A. M. , Siddique S. , Idrees M. , Tong Y. . ( 2010; ). Avian influenza A (H9N2): computational molecular analysis and phylogenetic characterization of viral surface proteins isolated between 1997 and 2009 from the human population. . Virol J 7:, 319. [CrossRef] [PubMed]
    [Google Scholar]
  4. Cheng V. C. , Chan J. F. , Wen X. , Wu W. L. , Que T. L. , Chen H. , Chan K. H. , Yuen K. Y. . ( 2011; ). Infection of immunocompromised patients by avian H9N2 influenza A virus. . J Infect 62:, 394–399. [CrossRef] [PubMed]
    [Google Scholar]
  5. Choi Y. K. , Ozaki H. , Webby R. J. , Webster R. G. , Peiris J. S. , Poon L. , Butt C. , Leung Y. H. , Guan Y. . ( 2004; ). Continuing evolution of H9N2 influenza viruses in Southeastern China. . J Virol 78:, 8609–8614. [CrossRef] [PubMed]
    [Google Scholar]
  6. Cong Y. L. , Pu J. , Liu Q. F. , Wang S. , Zhang G. Z. , Zhang X. L. , Fan W. X. , Brown E. G. , Liu J. H. . ( 2007; ). Antigenic and genetic characterization of H9N2 swine influenza viruses in China. . J Gen Virol 88:, 2035–2041. [CrossRef] [PubMed]
    [Google Scholar]
  7. Dong G. , Luo J. , Zhang H. , Wang C. , Duan M. , Deliberto T. J. , Nolte D. L. , Ji G. , He H. . ( 2011; ). Phylogenetic diversity and genotypical complexity of H9N2 influenza A viruses revealed by genomic sequence analysis. . PLoS ONE 6:, e17212. [CrossRef] [PubMed]
    [Google Scholar]
  8. 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 A 96:, 9363–9367. [CrossRef] [PubMed]
    [Google Scholar]
  9. Guo Y. J. , Krauss S. , Senne D. A. , Mo I. P. , Lo K. S. , Xiong X. P. , Norwood M. , Shortridge K. F. , Webster R. G. , Guan Y. . ( 2000; ). Characterization of the pathogenicity of members of the newly established H9N2 influenza virus lineages in Asia. . Virology 267:, 279–288. [CrossRef] [PubMed]
    [Google Scholar]
  10. Howard W. A. , Essen S. C. , Strugnell B. W. , Russell C. , Barass L. , Reid S. M. , Brown I. H. . ( 2011; ). Reassortant pandemic (H1N1) 2009 virus in pigs, United Kingdom. . Emerg Infect Dis 17:, 1049–1052. [CrossRef] [PubMed]
    [Google Scholar]
  11. Kim S.-H. , Moon O.-K. , Lee K.-K. , Song Y.-K. , Yeo C.-I. , Bae C.-W. , Yoon H. , Lee O.-S. , Lee J.-H. , Park C.-K. . ( 2011; ). Outbreak of pandemic influenza (H1N1) 2009 in pigs in Korea. . Vet Rec 169:, 155. [CrossRef] [PubMed]
    [Google Scholar]
  12. Kimble J. B. , Sorrell E. , Shao H. , Martin P. L. , Perez D. R. . ( 2011; ). Compatibility of H9N2 avian influenza surface genes and 2009 pandemic H1N1 internal genes for transmission in the ferret model. . Proc Natl Acad Sci U S A 108:, 12084–12088. [CrossRef] [PubMed]
    [Google Scholar]
  13. Li K. S. , Xu K. M. , Peiris J. S. , Poon L. L. , Yu K. Z. , Yuen K. Y. , Shortridge K. F. , Webster R. G. , Guan Y. . ( 2003; ). Characterization of H9 subtype influenza viruses from the ducks of southern China: a candidate for the next influenza pandemic in humans?. J Virol 77:, 6988–6994. [CrossRef] [PubMed]
    [Google Scholar]
  14. Lin Y. P. , Shaw M. , Gregory V. , Cameron K. , Lim W. , Klimov A. , Subbarao K. , Guan Y. , Krauss S. . & other authors ( 2000; ). Avian-to-human transmission of H9N2 subtype influenza A viruses: relationship between H9N2 and H5N1 human isolates. . Proc Natl Acad Sci U S A 97:, 9654–9658. [CrossRef] [PubMed]
    [Google Scholar]
  15. Liu Q. , Ma J. , Liu H. , Qi W. , Anderson J. , Henry S. C. , Hesse R. A. , Richt J. A. , Ma W. . ( 2012; ). Emergence of novel reassortant H3N2 swine influenza viruses with the 2009 pandemic H1N1 genes in the United States. . Arch Virol 157:, 555–562. [CrossRef] [PubMed]
    [Google Scholar]
  16. Ma W. , Vincent A. L. , Gramer M. R. , Brockwell C. B. , Lager K. M. , Janke B. H. , Gauger P. C. , Patnayak D. P. , Webby R. J. , Richt J. A. . ( 2007; ). Identification of H2N3 influenza A viruses from swine in the United States. . Proc Natl Acad Sci U S A 104:, 20949–20954. [CrossRef] [PubMed]
    [Google Scholar]
  17. Mok C. K. , Yen H. L. , Yu M. Y. , Yuen K. M. , Sia S. F. , Chan M. C. , Qin G. , Tu W. W. , Peiris J. S. . ( 2011; ). Amino acid residues 253 and 591 of the PB2 protein of avian influenza virus A H9N2 contribute to mammalian pathogenesis. . J Virol 85:, 9641–9645. [CrossRef] [PubMed]
    [Google Scholar]
  18. Moreno A. , Di Trani L. , Alborali L. , Vaccari G. , Barbieri I. , Falcone E. , Sozzi E. , Puzelli S. , Ferri G. , Cordioli P. . ( 2010; ). First pandemic H1N1 outbreak from a pig farm in Italy. . Open Virol J 4:, 52–56. [CrossRef] [PubMed]
    [Google Scholar]
  19. Moreno A. , Di Trani L. , Faccini S. , Vaccari G. , Nigrelli D. , Boniotti M. B. , Falcone E. , Boni A. , Chiapponi C. . & other authors ( 2011; ). Novel H1N2 swine influenza reassortant strain in pigs derived from the pandemic H1N1/2009 virus. . Vet Microbiol 149:, 472–477. [CrossRef] [PubMed]
    [Google Scholar]
  20. Nomura N. , Sakoda Y. , Endo M. , Yoshida H. , Yamamoto N. , Okamatsu M. , Sakurai K. , Hoang N. V. , Nguyen L. V. . & other authors ( 2012; ). Characterization of avian influenza viruses isolated from domestic ducks in Vietnam in 2009 and 2010. . Arch Virol 157:, 247–257. [CrossRef] [PubMed]
    [Google Scholar]
  21. Pasma T. , Joseph T. . ( 2010; ). Pandemic (H1N1) 2009 infection in swine herds, Manitoba, Canada. . Emerg Infect Dis 16:, 706–708.[PubMed] [CrossRef]
    [Google Scholar]
  22. Peiris M. , Yuen K. Y. , Leung C. W. , Chan K. H. , Ip P. L. , Lai R. W. , Orr W. K. , Shortridge K. F. . ( 1999; ). Human infection with influenza H9N2. . Lancet 354:, 916–917. [CrossRef] [PubMed]
    [Google Scholar]
  23. Peiris J. S. , Guan Y. , Markwell D. , Ghose P. , Webster R. G. , Shortridge K. F. . ( 2001; ). Cocirculation of avian H9N2 and contemporary “human” H3N2 influenza A viruses in pigs in southeastern China: potential for genetic reassortment?. J Virol 75:, 9679–9686. [CrossRef] [PubMed]
    [Google Scholar]
  24. Reed L. J. , Muench H. . ( 1938; ). A simple method of estimating fifty percent endpoints. . Am J Hyg 27:, 493–497.
    [Google Scholar]
  25. Richt J. A. , Lager K. M. , Janke B. H. , Woods R. D. , Webster R. G. , Webby R. J. . ( 2003; ). Pathogenic and antigenic properties of phylogenetically distinct reassortant H3N2 swine influenza viruses cocirculating in the United States. . J Clin Microbiol 41:, 3198–3205. [CrossRef] [PubMed]
    [Google Scholar]
  26. Shi W. F. , Gibbs M. J. , Zhang Y. Z. , Zhang Z. , Zhao X. M. , Jin X. , Zhu C. D. , Yang M. F. , Yang N. N. . & other authors ( 2008; ). Genetic analysis of four porcine avian influenza viruses isolated from Shandong, China. . Arch Virol 153:, 211–217. [CrossRef] [PubMed]
    [Google Scholar]
  27. Sorrell E. M. , Wan H. , Araya Y. , Song H. , Perez D. R. . ( 2009; ). Minimal molecular constraints for respiratory droplet transmission of an avian–human H9N2 influenza A virus. . Proc Natl Acad Sci U S A 106:, 7565–7570. [CrossRef] [PubMed]
    [Google Scholar]
  28. Sreta D. , Tantawet S. , Na Ayudhya S. N. , Thontiravong A. , Wongphatcharachai M. , Lapkuntod J. , Bunpapong N. , Tuanudom R. , Suradhat S. . & other authors ( 2010; ). Pandemic (H1N1) 2009 virus on commercial swine farm, Thailand. . Emerg Infect Dis 16:, 1587–1590.[PubMed] [CrossRef]
    [Google Scholar]
  29. Starick E. , Lange E. , Fereidouni S. , Bunzenthal C. , Höveler R. , Kuczka A. , grosse Beilage E. , Hamann H. P. , Klingelhöfer I. . & other authors ( 2011; ). Reassorted pandemic (H1N1) 2009 influenza A virus discovered from pigs in Germany. . J Gen Virol 92:, 1184–1188. [CrossRef] [PubMed]
    [Google Scholar]
  30. Sun Y. , Qin K. , Wang J. , Pu J. , Tang Q. , Hu Y. , Bi Y. , Zhao X. , Yang H. . & other authors ( 2011; ). High genetic compatibility and increased pathogenicity of reassortants derived from avian H9N2 and pandemic H1N1/2009 influenza viruses. . Proc Natl Acad Sci U S A 108:, 4164–4169. [CrossRef] [PubMed]
    [Google Scholar]
  31. Uyeki T. M. , Chong Y.-H. , Katz J. M. , Lim W. , Ho Y.-Y. , Wang S. S. , Tsang T. H. , Au W. W. , Chan S.-C. . & other authors ( 2002; ). Lack of evidence for human-to-human transmission of avian influenza A (H9N2) viruses in Hong Kong, China 1999. . Emerg Infect Dis 8:, 154–159. [CrossRef] [PubMed]
    [Google Scholar]
  32. Vijaykrishna D. , Poon L. L. , Zhu H. C. , Ma S. K. , Li O. T. , Cheung C. L. , Smith G. J. , Peiris J. S. , Guan Y. . ( 2010; ). Reassortment of pandemic H1N1/2009 influenza A virus in swine. . Science 328:, 1529. [CrossRef] [PubMed]
    [Google Scholar]
  33. Wan H. , Perez D. R. . ( 2007; ). Amino acid 226 in the hemagglutinin of H9N2 influenza viruses determines cell tropism and replication in human airway epithelial cells. . J Virol 81:, 5181–5191. [CrossRef] [PubMed]
    [Google Scholar]
  34. Wu Z. Q. , Ji J. , Zuo K. J. , Xie Q. M. , Li H. M. , Liu J. , Chen F. , Xue C. Y. , Ma J. Y. , Bi Y. Z. . ( 2010; ). Cloning and phylogenetic analysis of hemagglutinin gene of H9N2 subtype avian influenza virus from different isolates in China during 2002 to 2009. . Poult Sci 89:, 1136–1143. [CrossRef] [PubMed]
    [Google Scholar]
  35. Yen H.-L. , Liang C.-H. , Wu C.-Y. , Forrest H. L. , Ferguson A. , Choy K.-T. , Jones J. , Wong D. D. , Cheung P. P. . & other authors ( 2011; ). Hemagglutinin–neuraminidase balance confers respiratory-droplet transmissibility of the pandemic H1N1 influenza virus in ferrets. . Proc Natl Acad Sci U S A 108:, 14264–14269. [CrossRef] [PubMed]
    [Google Scholar]
  36. Yu H. , Hua R. H. , Wei T. C. , Zhou Y. J. , Tian Z. J. , Li G. X. , Liu T. Q. , Tong G. Z. . ( 2008; ). Isolation and genetic characterization of avian origin H9N2 influenza viruses from pigs in China. . Vet Microbiol 131:, 82–92. [CrossRef] [PubMed]
    [Google Scholar]
  37. Yu H. , Zhou Y. J. , Li G. X. , Ma J. H. , Yan L. P. , Wang B. , Yang F. R. , Huang M. , Tong G. Z. . ( 2011; ). Genetic diversity of H9N2 influenza viruses from pigs in China: a potential threat to human health?. Vet Microbiol 149:, 254–261. [CrossRef] [PubMed]
    [Google Scholar]
  38. Zhang P. , Tang Y. , Liu X. , Liu W. , Zhang X. , Liu H. , Peng D. , Gao S. , Wu Y. . & other authors ( 2009; ). A novel genotype H9N2 influenza virus possessing human H5N1 internal genomes has been circulating in poultry in eastern China since 1998. . J Virol 83:, 8428–8438. [CrossRef] [PubMed]
    [Google Scholar]
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