1887

Abstract

We report the genetic characterization of H6 avian influenza (AI) viruses isolated from domestic ducks and wild birds in Korea between April 2008 and April 2009. A phylogenetic analysis showed that the H6N1 viruses of wild birds and domestic ducks were of the same genotype (K-1) and were similar to the H6N1 virus isolated from a live poultry market in 2003, as six of the eight gene segments of those viruses had a common source. However, the H6N2 viruses of domestic poultry were separated into four genotypes (K-2a, K-2b, K-2c and K-2d) by at least a triple reassortment between influenza viruses of low pathogenicity from Korean poultry (H9N2 and H3N2) and viruses from aquatic birds. In an experimental infection of animals, certain H6 AI viruses replicated well in chickens and mice without pre-adaptation, indicating that H6 virus pathogenicity has the potential to be altered due to multiple reassortments, and that these reassortments could result in interspecies transmission to mammals.

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2010-01-01
2019-11-21
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References

  1. Abolnik, C., Bisschop, S., Gerdes, T., Olivier, A. & Horner, R. ( 2007; ). Outbreaks of avian influenza H6N2 viruses in chickens arose by a reassortment of H6N8 and H9N2 ostrich viruses. Virus Genes 34, 37–45.[CrossRef]
    [Google Scholar]
  2. Alexander, D. J. & Brown, I. H. ( 2000; ). Recent zoonoses caused by influenza A viruses. Rev Sci Tech 19, 197–225.
    [Google Scholar]
  3. Beare, A. S. & Webster, R. G. ( 1991; ). Replication of avian influenza viruses in humans. Arch Virol 119, 37–42.[CrossRef]
    [Google Scholar]
  4. Belshe, R. B., Smith, M. H., Hall, C. B., Betts, R. & Hay, A. J. ( 1988; ). Genetic basis of resistance to rimantadine emerging during treatment of influenza virus infection. J Virol 62, 1508–1512.
    [Google Scholar]
  5. Brown, J. D., Stallknecht, D. E., Beck, J. R., Suarez, D. L. & Swayne, D. E. ( 2006; ). Susceptibility of North American ducks and gulls to H5N1 highly pathogenic avian influenza viruses. Emerg Infect Dis 12, 1663–1670.[CrossRef]
    [Google Scholar]
  6. Cheung, C. L., Vijaykrishna, D., Smith, G. J. D., Fan, X. H., Zhang, J. X., Bahl, J., Duan, L., Huang, K., Tai, H. & other authors ( 2007; ). Establishment of influenza A virus (H6N1) in minor poultry species in Southern China. J Virol 81, 10402–10412.[CrossRef]
    [Google Scholar]
  7. Choi, Y. K., Seo, S. H., Kim, J. A., Webby, R. J. & Webster, R. G. ( 2005; ). Avian influenza viruses in Korean live poultry markets and their pathogenic potential. Virology 332, 529–537.[CrossRef]
    [Google Scholar]
  8. Fereidouni, S. R., Starick, E., Grund, C., Globig, A., Mettenleiter, T. C., Beer, M. & Harder, T. ( 2009; ). Rapid molecular subtyping by reverse transcription polymerase chain reaction of the neuraminidase gene of avian influenza A viruses. Vet Microbiol 135, 253–260.[CrossRef]
    [Google Scholar]
  9. Fouchier, R. A. M., Bestebroer, T. M., Herfst, S., Van Der Kemp, L., Rimmelzwaan, G. F. & Osterhaus, A. D. M. E. ( 2000; ). Detection of influenza A viruses from different species by PCR amplification of conserved sequences in the matrix gene. J Clin Microbiol 38, 4096–4101.
    [Google Scholar]
  10. Fouchier, R. A. M., Schneeberger, P. M., Rozendaal, F. W., Broekman, J. M., Kemink, S. A. G., Munster, V., Kuiken, T., Rimmelzwaan, G. F., Schutten, M. & other authors ( 2004; ). Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proc Natl Acad Sci U S A 101, 1356–1361.[CrossRef]
    [Google Scholar]
  11. Gillim-Ross, L., Santos, C., Chen, Z., Aspelund, A., Yang, C., Ye, D., Jin, H., Kemble, G. & Subbarao, K. ( 2008; ). Avian influenza H6 viruses productively infect and cause illness in mice and ferrets. J Virol 82, 10854–10863.[CrossRef]
    [Google Scholar]
  12. Ha, Y., Stevens, D., Skehel, J. & Wiley, D. ( 2001; ). X-ray structures of H5 avian and H9 swine influenza virus hemagglutinins bound to avian and human receptor analogs. Proc Natl Acad Sci U S A 98, 11181–11186.[CrossRef]
    [Google Scholar]
  13. Hatchette, T. F., Walker, D., Johnson, C., Baker, A., Pryor, S. P. & Webster, R. G. ( 2004; ). Influenza A viruses in feral Canadian ducks: extensive reassortment in nature. J Gen Virol 85, 2327–2337.[CrossRef]
    [Google Scholar]
  14. Hatta, M., Gao, P., Halfmann, P. & Kawaoka, Y. ( 2001; ). Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 293, 1840–1842.[CrossRef]
    [Google Scholar]
  15. Hinshaw, V. S., Webster, R. G. & Turner, B. ( 1980; ). The perpetuation of orthomyxoviruses and paramyxoviruses in Canadian waterfowl. Can J Microbiol 26, 622–629.[CrossRef]
    [Google Scholar]
  16. Hoffmann, E., Stech, J., Leneva, I., Krauss, S., Scholtissek, C., Chin, P., Peiris, M., Shortridge, K. & Webster, R. ( 2000; ). Characterization of the Influenza A virus gene pool in avian species in Southern China: was H6N1 a derivative or a precursor of H5N1? J Virol 74, 6309–6315.[CrossRef]
    [Google Scholar]
  17. Hulse-Post, D. J., Sturm-Ramirez, K. M., Humberd, J., Seiler, P., Govorkova, E. A., Krauss, S., Scholtissek, C., Puthavathana, P., Buranathai, C. & other authors ( 2005; ). Role of domestic ducks in the propagation and biological evolution of highly pathogenic H5N1 influenza viruses in Asia. Proc Natl Acad Sci U S A 102, 10682–10687.[CrossRef]
    [Google Scholar]
  18. Kawaoka, Y., Gorman, O., Ito, T., Wells, K., Donis, R., Castrucci, M., Donatelli, I. & Webster, R. ( 1998; ). Influence of host species on the evolution of the nonstructural (NS) gene of influenza A viruses. Virus Res 55, 143–156.[CrossRef]
    [Google Scholar]
  19. Kayali, G., Ortiz, E., Chorazy, M. & Gray, G. ( 2009; ). Evidence of previous avian influenza infection among US turkey workers. Zoonoses Public Health (in press). doi:10.1111/j.1863-2378.2009.01231.x.
    [Google Scholar]
  20. Lee, M.-S., Chang, P.-C., Shien, J.-H., Cheng, M.-C. & Shieh, H. K. ( 2001; ). Identification and subtyping of avian influenza viruses by reverse transcription-PCR. J Virol Methods 97, 13–22.[CrossRef]
    [Google Scholar]
  21. Lee, C.-W., Suarez, D. L., Tumpey, T. M., Sung, H.-W., Kwon, Y.-K., Lee, Y.-J., Choi, J.-G., Joh, S.-J., Kim, M.-C. & other authors ( 2005; ). Characterization of highly pathogenic H5N1 avian influenza A viruses isolated from South Korea. J Virol 79, 3692–3702.[CrossRef]
    [Google Scholar]
  22. Lee, M.-S., Chang, P.-C., Shien, J.-H., Cheng, M.-C., Chen, C. L. & Shieh, H. K. ( 2006; ). Genetic and pathogenic characterization of H6N1 avian influenza viruses isolated in Taiwan between 1972 and 2005. Avian Dis 50, 561–571.[CrossRef]
    [Google Scholar]
  23. Lee, Y.-J., Shin, J.-Y., Song, M.-S., Lee, Y.-M., Choi, J.-G., Lee, E.-K., Jeong, O.-M., Sung, H.-W., Kim, J.-H. & other authors ( 2007; ). Continuing evolution of H9 influenza viruses in Korean poultry. Virology 359, 313–323.[CrossRef]
    [Google Scholar]
  24. Lee, Y.-J., Choi, Y.-K., Kim, Y.-J., Song, M.-S., Jeong, O.-M., Lee, E.-K., Jeon, W.-J., Jeong, W., Joh, S.-J. & other authors ( 2008; ). Highly pathogenic avian influenza virus (H5N1) in domestic poultry and relationship with migratory birds, South Korea. Emerg Infect Dis 14, 487–490.[CrossRef]
    [Google Scholar]
  25. Li, K. S., Xu, K. M., Peiris, J. S. M., Poon, L. L. M., 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]
    [Google Scholar]
  26. Matrosovich, M., Zhou, N., Kawaoka, Y. & Webster, R. ( 1999; ). The surface glycoproteins of H5 influenza viruses isolated from humans, chickens, and wild aquatic birds have distinguishable properties. J Virol 73, 1146–1155.
    [Google Scholar]
  27. Munch, M., Nielsen, L., Handberg, K. & Jørgensen, P. ( 2001; ). Detection and subtyping (H5 and H7) of avian type A influenza virus by reverse transcription-PCR and PCR-ELISA. Arch Virol 146, 87–97.[CrossRef]
    [Google Scholar]
  28. Munster, V. J., Baas, C., Lexmond, P., Waldenström, J., Wallensten, A., Fransson, T., Rimmelzwaan, G. F., Beyer, W. E., Schutten, M. & other authors ( 2007; ). Spatial, temporal, and species variation in prevalence of influenza A viruses in wild migratory birds. PLoS Pathog 3, e61 [CrossRef]
    [Google Scholar]
  29. Myers, K. P., Setterquist, S. F., Capuano, A. W. & Gray, G. C. ( 2007; ). Infection due to 3 avian influenza subtypes in United States veterinarians. Clin Infect Dis 45, 4–9.[CrossRef]
    [Google Scholar]
  30. Palmer, D. F., Coleman, W. R., Dowdle, W. R. & Wchild, G. C. ( 1975; ). Advanced Laboratory Techniques for Influenza Diagnosis. Washington, DC, USA: Department of Health, Education and Welfare.
  31. Reed, L. & Muench, H. ( 1938; ). A simple method of estimating fifty percent endpoints. Am J Hyg 27, 493–497.
    [Google Scholar]
  32. Scholtissek, C. & von Hoyningen-Huene, V. ( 1980; ). Genetic relatedness of the gene which codes for the nonstructural (NS) protein of different influenza A strains. Virology 102, 13–20.[CrossRef]
    [Google Scholar]
  33. Seo, S. H., Hoffmann, E. & Webster, R. G. ( 2002; ). Lethal H5N1 influenza viruses escape host anti-viral cytokine responses. Nat Med 8, 950–954.[CrossRef]
    [Google Scholar]
  34. Song, M. S., Oh, T. K., Moon, H. J., Yoo, D. W., Lee, E. H., Lee, J. S., Kim, C. J., Yoo, G. J., Kim, H. & Choi, Y. K. ( 2008; ). Ecology of H3 avian influenza viruses in Korea and assessment of their pathogenic potentials. J Gen Virol 89, 949–957.[CrossRef]
    [Google Scholar]
  35. Spackman, E., Stallknecht, D., Slemons, R., Winker, K., Suarez, D., Scott, M. & Swayne, D. ( 2005; ). Phylogenetic analyses of type A influenza genes in natural reservoir species in North America reveals genetic variation. Virus Res 114, 89–100.[CrossRef]
    [Google Scholar]
  36. Sturm-Ramirez, K. M., Hulse-Post, D. J., Govorkova, E. A., Humberd, J., Seiler, P., Puthavathana, P., Buranathai, C., Nguyen, T. D., Chaisingh, A. & other authors ( 2005; ). Are ducks contributing to the endemicity of highly pathogenic H5N1 influenza virus in Asia? J Virol 79, 11269–11279.[CrossRef]
    [Google Scholar]
  37. Swayne, D. E. & Halvorson, D. A. ( 2003; ). Influenza. In Diseases of Poultry, 11th edn, pp. 135–160. Edited by Y. M. Saif, H. J. Barnes, J. R. Glisom, A. M. Fadly, L. R. McDougald & D. E. Swayne. Ames, IA: Iowa State University Press.
  38. Tamura, K., Dudley, J., Nei, M. & Kumar, S. ( 2007; ). mega4: molecular evolutionary genetics analysis (mega) software version 4.0. Mol Biol Evol 24, 1596–1599.[CrossRef]
    [Google Scholar]
  39. Treanor, J. J., Snyder, M. H., London, W. T. & Murphy, B. R. ( 1989; ). The B allele of the NS gene of avian influenza viruses, but not the A allele, attenuates a human influenza A virus for squirrel monkeys. Virology 171, 1–9.[CrossRef]
    [Google Scholar]
  40. Tweed, S. A., Skowronski, D. M., David, S. T., Larder, A., Petric, M., Lees, W., Li, Y., Katz, J., Krajden, M. & other authors ( 2004; ). Human illness from avian influenza H7N3, British Columbia. Emerg Infect Dis 10, 2196–2199.[CrossRef]
    [Google Scholar]
  41. Webby, R. J. & Webster, R. G. ( 2003; ). Are we ready for pandemic influenza? Science 302, 1519–1522.[CrossRef]
    [Google Scholar]
  42. Webby, R. J., Woolcock, P. R., Krauss, S. L. & Webster, R. G. ( 2002; ). Reassortment and interspecies transmission of North American H6N2 influenza viruses. Virology 295, 44–53.[CrossRef]
    [Google Scholar]
  43. Webster, R. G., Yakhno, M., Hinshaw, V. S., Bean, W. J. & Murti, K. G. ( 1978; ). Intestinal influenza: replication and characterization of influenza viruses in ducks. Virology 84, 268–278.[CrossRef]
    [Google Scholar]
  44. 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.
    [Google Scholar]
  45. Winker, K., McCracken, K., Gibson, D., Pruett, C., Meier, R., Huettmann, F., Wege, M., Kulikova, I., Zhuravlev, Y. & other authors ( 2007; ). Movements of birds and avian influenza from Asia into Alaska. Emerg Infect Dis 13, 547–552.[CrossRef]
    [Google Scholar]
  46. Woolcock, P. R., Suarez, D. L. & Kuney, D. ( 2003; ). Low-pathogenicity avian influenza virus (H6N2) in chickens in California, 2000–02. Avian Dis 47, 872–881.[CrossRef]
    [Google Scholar]
  47. Yuen, K., Chan, P., Peiris, M., Tsang, D., Que, T., Shortridge, K., Cheung, P., To, W., Ho, E. & Sung, R. ( 1998; ). Clinical features and rapid viral diagnosis of human disease associated with avian influenza A H5N1 virus. Lancet 351, 467–471.[CrossRef]
    [Google Scholar]
  48. zu Dohna, H., Li, J., Cardona, C., Miller, J. & Carpenter, T. ( 2009; ). Invasions by Eurasian avian influenza virus H6 genes and replacement of the virus' North American clade. Emerg Infect Dis 15, 1040–1045.[CrossRef]
    [Google Scholar]
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vol. , part 1, pp. 208–219

Phylogenetic relationships of the representative H6 influenza viruses isolated from wild birds and poultry. (a) PB2, (b) PB1 and (c) PA genes.

Phylogenetic relationships of the representative H6 influenza viruses isolated from wild birds and poultry. (a) NP, (b) M and (c) NS genes.

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