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Abstract

During the 2020/21 winter season, 29 and 10 H5N8 high pathogenicity avian influenza viruses (HPAIVs) were isolated from environmental water and wild birds, respectively, in Kagoshima prefecture, Japan. Furthermore, seven subtypes of low pathogenicity avian influenza viruses (LPAIVs) were also isolated; H1N1, H2N9, H3N2, H3N6, H3N8, H4N6, and H6N6 subtypes. While the H5 hemagglutinin (HA) genes of the G1 cluster were isolated throughout the winter season, those of the G2 cluster were also detected in late winter, suggesting that H5 HPAIVs possessing H5 HA genes from the two different clusters were individually introduced into Kagoshima prefecture. Intriguingly, genetic constellations revealed that the H5N8 HPAIVs could be classified into six genotypes, including four previously reported genotypes (E1, E2, E3, and E7), and two new genotypes (tentatively named E8 and E9). The PB1 and PA gene segments of genotypes E8 and E9 shared high similarity with those of LPAIVs, whereas the remaining gene segments were close to those of genotype E1. Furthermore, LPAIVs whose PA gene segment was close to that of genotype E9 were isolated from the environmental water. Overall, we revealed that various HPAIV genotypes circulated in Kagoshima prefecture during the 2020/21 winter season. This study highlights the importance of monitoring both HPAIV and LPAIV to better understand AIV ecology in migratory waterfowl populations.

Funding
This study was supported by the:
  • Ministry of Agriculture, Forestry and Fisheries (Award JPJ008617.18065101)
    • Principle Award Recipient: MakotoOzawa
  • Japan Society for the Promotion of Science (Award 21K20610)
    • Principle Award Recipient: KosukeOkuya
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/content/journal/jgv/10.1099/jgv.0.001870
2023-06-23
2024-04-30
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References

  1. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol Rev 1992; 56:152–179 [View Article] [PubMed]
    [Google Scholar]
  2. Lindstrom SE, Cox NJ, Klimov A. Genetic analysis of human H2N2 and early H3N2 influenza viruses, 1957-1972: evidence for genetic divergence and multiple reassortment events. Virology 2004; 328:101–119 [View Article] [PubMed]
    [Google Scholar]
  3. Nelson MI, Simonsen L, Viboud C, Miller MA, Taylor J et al. Stochastic processes are key determinants of short-term evolution in influenza A virus. PLoS Pathog 2006; 2:e125 [View Article] [PubMed]
    [Google Scholar]
  4. Kandeil A, El-Shesheny R, Maatouq A, Moatasim Y, Cai Z et al. Novel reassortant H9N2 viruses in pigeons and evidence for antigenic diversity of H9N2 viruses isolated from quails in Egypt. J Gen Virol 2017; 98:548–562 [View Article] [PubMed]
    [Google Scholar]
  5. Nguyen DT, Jang Y, Nguyen TD, Jones J, Shepard SS et al. Shifting clade distribution, reassortment, and emergence of new subtypes of highly pathogenic avian influenza A(H5) viruses collected from vietnamese poultry from 2012 to 2015. J Virol 2017; 91:e01708-16 [View Article] [PubMed]
    [Google Scholar]
  6. Stieneke-Gröber A, Vey M, Angliker H, Shaw E, Thomas G et al. Influenza virus hemagglutinin with multibasic cleavage site is activated by furin, a subtilisin-like endoprotease. EMBO J 1992; 11:2407–2414 [View Article] [PubMed]
    [Google Scholar]
  7. Banks J, Speidel ES, Moore E, Plowright L, Piccirillo A et al. Changes in the haemagglutinin and the neuraminidase genes prior to the emergence of highly pathogenic H7N1 avian influenza viruses in Italy. Arch Virol 2001; 146:963–973 [View Article] [PubMed]
    [Google Scholar]
  8. Horimoto T, Rivera E, Pearson J, Senne D, Krauss S et al. Origin and molecular changes associated with emergence of a highly pathogenic H5N2 influenza virus in Mexico. Virology 1995; 213:223–230 [View Article] [PubMed]
    [Google Scholar]
  9. Webster RG, Kawaoka Y, Bean WJ. Molecular changes in A/Chicken/Pennsylvania/83 (H5N2) influenza virus associated with acquisition of virulence. Virology 1986; 149:165–173 [View Article] [PubMed]
    [Google Scholar]
  10. Ito T, Goto H, Yamamoto E, Tanaka H, Takeuchi M et al. Generation of a highly pathogenic avian influenza A virus from an avirulent field isolate by passaging in chickens. J Virol 2001; 75:4439–4443 [View Article] [PubMed]
    [Google Scholar]
  11. Lee C-W, Lee Y-J, Senne DA, Suarez DL. Pathogenic potential of North American H7N2 avian influenza virus: a mutagenesis study using reverse genetics. Virology 2006; 353:388–395 [View Article] [PubMed]
    [Google Scholar]
  12. Olsen B, Munster VJ, Wallensten A, Waldenström J, Osterhaus A et al. Global patterns of influenza A virus in wild birds. Science 2006; 312:384–388 [View Article] [PubMed]
    [Google Scholar]
  13. Ozawa M, Matsuu A, Tokorozaki K, Horie M, Masatani T et al. Genetic diversity of highly pathogenic H5N8 avian influenza viruses at a single overwintering site of migratory birds in Japan, 2014/15. Euro Surveill 2015; 20:21132 [View Article] [PubMed]
    [Google Scholar]
  14. Okuya K, Kawabata T, Nagano K, Tsukiyama-Kohara K, Kusumoto I et al. Isolation and characterization of influenza A viruses from environmental water at an overwintering site of migratory birds in Japan. Arch Virol 2015; 160:3037–3052 [View Article] [PubMed]
    [Google Scholar]
  15. Okamatsu M, Ozawa M, Soda K, Takakuwa H, Haga A et al. Characterization of highly pathogenic avian influenza virus A(H5N6), Japan, November 2016. Emerg Infect Dis 2017; 23:691–695 [View Article] [PubMed]
    [Google Scholar]
  16. Nakagawa H, Okuya K, Kawabata T, Matsuu A, Takase K et al. Genetic characterization of low-pathogenic avian influenza viruses isolated on the Izumi plain in Japan: possible association of dynamic movements of wild birds with AIV evolution. Arch Virol 2018; 163:911–923 [View Article] [PubMed]
    [Google Scholar]
  17. Khalil AM, Fujimoto Y, Kojima I, Esaki M, Ri K et al. Genetic characterization of H5N8 highly pathogenic avian influenza viruses isolated from falcated ducks and environmental water in Japan in November 2020. Pathogens 2021; 10:171 [View Article] [PubMed]
    [Google Scholar]
  18. Okuya K, Khalil AM, Esaki M, Kojima I, Nishi N et al. Genetic characterization of avian influenza viruses isolated from the Izumi Plain, Japan in 2019/20 winter season. Pathogens 2022; 11:1013 [View Article] [PubMed]
    [Google Scholar]
  19. Baek Y-G, Lee Y-N, Lee D-H, Shin J-I, Lee J-H et al. Multiple reassortants of H5N8 Clade 2.3.4.4b highly pathogenic avian influenza viruses detected in South Korea during the winter of 2020-2021. Viruses 2021; 13:490 [View Article] [PubMed]
    [Google Scholar]
  20. Mine J, Tsunekuni R, Tanikawa T, Uchida Y, Dubovitskiy N et al. Genetics of Japanese H5N8 high pathogenicity avian influenza viruses isolated in winter 2020-2021 and their genetic relationship with avian influenza viruses in Siberia. Transbound Emerg Dis 2022; 69:e2195–e2213 [View Article] [PubMed]
    [Google Scholar]
  21. Khalil AM, Kojima I, Fukunaga W, Okajima M, Mitarai S et al. Improved method for avian influenza virus isolation from environmental water samples. Transbound Emerg Dis 2022; 69:e2889–e2897 [View Article] [PubMed]
    [Google Scholar]
  22. Khalil AM, Nishi N, Kojima I, Fukunaga W, Kuwahara M et al. Transition in genetic constellations of H3N8 and H4N6 low-pathogenic avian influenza viruses isolated from an overwintering site in Japan throughout different winter seasons. Arch Virol 2020; 165:643–659 [View Article] [PubMed]
    [Google Scholar]
  23. Ozawa M, Matsuu A, Khalil AM, Nishi N, Tokorozaki K et al. Phylogenetic variations of highly pathogenic H5N6 avian influenza viruses isolated from wild birds in the Izumi plain, Japan, during the 2016-17 winter season. Transbound Emerg Dis 2019; 66:797–806 [View Article] [PubMed]
    [Google Scholar]
  24. Tsukamoto K, Ashizawa H, Nakanishi K, Kaji N, Suzuki K et al. Subtyping of avian influenza viruses H1 to H15 on the basis of hemagglutinin genes by PCR assay and molecular determination of pathogenic potential. J Clin Microbiol 2008; 46:3048–3055 [View Article] [PubMed]
    [Google Scholar]
  25. Hoffmann E, Stech J, Guan Y, Webster RG, Perez DR. Universal primer set for the full-length amplification of all influenza A viruses. Arch Virol 2001; 146:2275–2289 [View Article] [PubMed]
    [Google Scholar]
  26. Khalil AM, Hatai H, Fujimoto Y, Kojima I, Okajima M et al. A lethal case of natural infection with the H5N8 highly pathogenic avian influenza virus of clade 2.3.4.4 in a Mandarin duck. Zoonotic Diseases 2022; 2:32–36 [View Article]
    [Google Scholar]
  27. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article] [PubMed]
    [Google Scholar]
  28. Tamura K, Peterson D, Peterson N, Stecher G, Nei M et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011; 28:2731–2739 [View Article] [PubMed]
    [Google Scholar]
  29. Okuya K, Mine J, Tokorozaki K, Kojima I, Esaki M et al. Genetically diverse highly pathogenic avian influenza A(H5N1/H5N8) Viruses among wild waterfowl and domestic poultry, Japan, 2021. Emerg Infect Dis 2022; 28:1451–1455 [View Article] [PubMed]
    [Google Scholar]
  30. Okuya K, Kanazawa N, Kanda T, Kuwahara M, Matsuu A et al. Genetic characterization of an avian H4N6 influenza virus isolated from the Izumi plain, Japan. Microbiol Immunol 2017; 61:513–518 [View Article] [PubMed]
    [Google Scholar]
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