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References

  1. Alexander, D. J. 2007. An overview of the epidemiology of avian influenza. Vaccine 25: 5637-5644.
    Pubmed CrossRef
  2. Brown, I. H. 2000. The epidemiology and evolution of influenza viruses in pigs. Vet. Microbiol. 74: 29-46.
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    Pubmed CrossRef
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    Pubmed
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    Pubmed
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    CrossRef
  7. Claas, E. C., Y. Kawaoka, J. C. de Jong, N. Masurel, and R. G. Webster. 1994. Infection of children with avian-human reassortant influenza virus from pigs in Europe. Virology 204:453-457.
    Pubmed CrossRef
  8. Fouchier, R. A., V. Munster, A. Wallensten, T. M. Bestebroer, S. Herfst, D. Smith, et al. 2005. Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J. Virol. 79: 2814-2822.
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  9. Garten, R. J., C. T. Davis, C. A. Russell, B. Shu, S. Lindstrom, A. Balish, et al. 2009. Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325: 197-201.
    Pubmed PMC CrossRef
  10. Howard, W. A., S. C. Essen, B. W. Strugnell, C. Russell, L. Barass, S. M. Reid, and I. H. Brown. 2011. Reassortant pandemic (H1N1) 2009 virus in pigs, United Kingdom. Emerg. Infect. Dis. 17: 1049-1052.
    Pubmed CrossRef
  11. Ito, T., J. N. Couceiro, S. Kelm, L. G. Baum, S. Krauss, M. R. Castrucci, et al. 1998. Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. J. Virol. 72:7367-7373.
    Pubmed PMC
  12. Jo, S. K., H. S. Kim, S. W. Cho, and S. H. Seo. 2007. Genetic and antigenic characterization of swine H1N2 influenza viruses isolated from Korean pigs. J. Microbiol. Biotechnol. 17: 868-872.
    Pubmed
  13. Jung, K. and C. Chae. 2004. Phylogenetic analysis of an H1N2 influenza A virus isolated from a pig in Korea. Brief Report. Arch. Virol. 149: 1415-1422.
  14. Jung, K. and C. Chae. 2005. First outbreak of respiratory disease associated with swine influenza H1N2 virus in pigs in Korea. J. Vet. Diagn. Invest. 17: 176-178.
    Pubmed CrossRef
  15. Kitikoon, P., D. Sreta, S. N. Na Ayudhya, M. Wongphatcharachai, J. Lapkuntod, D. Prakairungnamthip, et al. 2011. Brief report:Molecular characterization of a novel reassorted pandemic H1N1 2009 in Thai pigs. Virus Genes 43: 1-5.
    Pubmed CrossRef
  16. Lee, C. S., B. K. Kang, H. K. Kim, S. J. Park, B. K. Park, K. Jung, and D. S. Song. 2008. Phylogenetic analysis of swine influenza viruses recently isolated in Korea. Virus Genes 37:168-176.
    Pubmed CrossRef
  17. Lee, C. S., B. K. Kang, D. H. Lee, S. H. Lyou, B. K. Park, S. K. Ann, et al. 2008. One-step multiplex RT-PCR for detection and subtyping of swine influenza H1, H3, N1, N2 viruses in clinical samples using a dual priming oligonucleotide (DPO) system. J. Virol. Methods 151: 30-34.
    Pubmed CrossRef
  18. Luoh, S. M., M. W. McGregor, and V. S. Hinshaw. 1992. Hemagglutinin mutations related to antigenic variation in H1 swine influenza viruses. J. Virol. 66: 1066-1073.
    Pubmed PMC
  19. Massin, P., G. Kuntz-Simon, C. Barbezange, C. Deblanc, A. Oger, E. Marquet-Blouin, et al. 2010. Temperature sensitivity on growth and/or replication of H1N1, H1N2 and H3N2 influenza A viruses isolated from pigs and birds in mammalian cells. Vet. Microbiol. 142: 232-241.
    Pubmed CrossRef
  20. Moreno, A., L. Di Trani, S. Faccini, G. Vaccari, D. Nigrelli, M. B. Boniotti, et al. 2010. Novel H1N2 swine influenza reassortant strain in pigs derived from the pandemic H1N1/2009 virus. Vet. Microbiol. 149: 472-477.
    Pubmed CrossRef
  21. Olsen, C. W. 2002. The emergence of novel swine influenza viruses in North America. Virus Res. 85: 199-210.
    CrossRef
  22. Olsen, C. W., I. H. Brown, B. C. Easterday, and V. Reeth. 2006. In B. E. Straw, J. J. Zimmerman, S. D’Allaire, and D. J. Taylor (eds.). Disease of Swine. The Blackwell Publishing Professinal.
  23. Pascua, P. N., M. S. Song, J. H. Lee, H. W. Choi, J. H. Han, J. H. Kim, et al. 2008. Seroprevalence and genetic evolutions of swine influenza viruses under vaccination pressure in Korean swine herds. Virus Res. 138: 43-49.
    Pubmed CrossRef
  24. Pereda, A., J. Cappuccio, M. A. Quiroga, E. Baumeister, L. Insarralde, M. Ibar, et al. 2010. Pandemic (H1N1) 2009 outbreak on pig farm, Argentina. Emerg. Infect. Dis. 16: 304307.
    Pubmed
  25. Schnitzler, S. U. and P. Schnitzler. 2009. An update on swineorigin influenza virus A/H1N1: A review. Virus Genes 39:279-292.
    Pubmed CrossRef
  26. Shaw, M. W., N. H. Arden, and H. F. Maassab. 1992. New aspects of influenza viruses. Clin. Microbiol. Rev. 5: 74-92.
    Pubmed PMC
  27. Shi, W., F. Lei, C. Zhu, F. Sievers, and D. G. Higgins. 2010. A complete analysis of HA and NA genes of influenza A viruses. PLoS One 5: e14454.
    Pubmed PMC CrossRef
  28. Song, D. S., C. S. Lee, K. Jung, B. K. Kang, J. S. Oh, Y. D. Yoon, et al. 2007. Isolation and phylogenetic analysis of H1N1 swine influenza virus isolated in Korea. Virus Res. 125: 98103.
    Pubmed CrossRef
  29. Song, D. S., J. Y. Lee, J. S. Oh, K. S. Lyoo, K. J. Yoon, Y. H. Park, and B. K. Park. 2003. Isolation of H3N2 swine influenza virus in South Korea. J. Vet. Diagn. Invest. 15: 30-34.
    Pubmed CrossRef
  30. Song, M. S., J. H. Lee, P. N. Pascua, Y. H. Baek, H. I. Kwon, K. J. Park, et al. 2009. Evidence of human-to-swine transmission of the pandemic (H1N1) 2009 influenza virus in South Korea. J. Clin. Microbiol. 48: 3204-3211.
    Pubmed PMC CrossRef
  31. Sreta, D., S. Tantawet, S. N. Na Ayudhya, A. Thontiravong, M. Wongphatcharachai, J. Lapkuntod, et al. 2010. Pandemic (H1N1) 2009 virus on commercial swine farm, Thailand. Emerg. Infect. Dis. 16: 1587-1590.
    Pubmed PMC
  32. Starick, E., E. Lange, S. Fereidouni, C. Bunzenthal, R. Hoveler, A. Kuczka, et al. 2011. Reassorted pandemic (H1N1) 2009 influenza A virus discovered from pigs in Germany. J. Gen. Virol. 92: 1184-1188.
  33. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTAL_X Windows interface:Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25: 4876-4882.
    Pubmed PMC CrossRef
  34. Tobita, K., A. Sugiura, C. Enomote, and M. Furuyama. 1975. Plaque assay and primary isolation of influenza A viruses in an established line of canine kidney cells (MDCK) in the presence of trypsin. Med. Microbiol. Immunol. 162: 9-14.
    Pubmed CrossRef
  35. Vijaykrishna, D., L. L. Poon, H. C. Zhu, S. K. Ma, O. T. Li, C. L. Cheung, et al. 2010. Reassortment of pandemic H1N1/2009 influenza A virus in swine. Science 328: 1529.
    Pubmed CrossRef
  36. Webster, R. G., W. J. Bean, O. T. Gorman, T. M. Chambers, and Y. Kawaoka. 1992. Evolution and ecology of influenza A viruses. Microbiol. Rev. 56: 152-179.
    Pubmed PMC
  37. Weingartl, H. M., Y. Berhane, T. Hisanaga, J. Neufeld, H. Kehler, C. Emburry-Hyatt, et al. 2010. Genetic and pathobiologic characterization of pandemic H1N1 2009 influenza viruses from a naturally infected swine herd. J. Virol. 84: 2245-2256.
    Pubmed PMC CrossRef
  38. WHO. 2009. Current WHO Phase of Pandemic Alert.
  39. Xu, C., Q. Zhu, H. Yang, X. Zhang, C. Qiao, Y. Chen, et al. 2009. Two genotypes of H1N2 swine influenza viruses appeared among pigs in China. J. Clin. Virol. 46: 192-195.
    Pubmed CrossRef
  40. Yu, H., P. C. Zhang, Y. J. Zhou, G. X. Li, J. Pan, L. P. Yan, et al. 2009. Isolation and genetic characterization of avian-like H1N1 and novel ressortant H1N2 influenza viruses from pigs in China. Biochem. Biophys Res. Commun. 386: 278-283.
    Pubmed CrossRef
  41. Zhou, N. N., D. A. Senne, J. S. Landgraf, S. L. Swenson, G. Erickson, K. Rossow, et al. 1999. Genetic reassortment of avian, swine, and human influenza A viruses in American pigs. J. Virol. 73: 8851-8856.
    Pubmed PMC
  42. Zou, S. 1997. A practical approach to genetic screening for influenza virus variants. J. Clin. Microbiol. 35: 2623-2627.
    Pubmed PMC

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Article

Research article

J. Microbiol. Biotechnol. 2012; 22(5): 699-707

Published online May 28, 2012 https://doi.org/10.4014/jmb.1106.05062

Copyright © The Korean Society for Microbiology and Biotechnology.

Identification of Reassortant Pandemic H1N1 Influenza Virus in Korean Pigs

Jae Yeon Han 1, Sung Jun Park 1, Hye Kwon Kim 1, Semi Rho 1, Giap Van Nguyen 1, Daesub Song 2, Bo Kyu Kang 2, Hyung Jun Moon 2, Min Joo Yeom 2 and Bong Kyun Park 1*

1Department of Veterinary Medicine Virology Laboratory College of Veterinary Medicine and BK21 Program for Veterinary Science, Seoul National University, Seoul 151-742, Korea, 2Research Unit, Green Cross Veterinary Products, Yong-In 449-903, Korea

Received: June 8, 2011; Accepted: December 29, 2011

Abstract

Since the 2009 pandemic human H1N1 influenza A virus
emerged in April 2009, novel reassortant strains have
been identified throughout the world. This paper describes
the detection and isolation of reassortant strains associated
with human pandemic influenza H1N1 and swine influenza
H1N2 (SIV) viruses in swine populations in South Korea.
Two influenza H1N2 reassortants were detected, and
subtyped by PCR. The strains were isolated using Madin-
Darby canine kidney (MDCK) cells, and genetically
characterized by phylogenetic analysis for genetic diversity.
They consisted of human, avian, and swine virus genes
that were originated from the 2009 pandemic H1N1 virus
and a neuraminidase (NA) gene from H1N2 SIV previously
isolated in North America. This identification of
reassortment events in swine farms raises concern that
reassortant strains may continuously circulate within swine
populations, calling for the further study and surveillance
of pandemic H1N1 among swine.

Keywords: H1N2 influenza A virus, pandemic (H1N1) 2009 influenza A virus, reassortment, South Korea, swine

References

  1. Alexander, D. J. 2007. An overview of the epidemiology of avian influenza. Vaccine 25: 5637-5644.
    Pubmed CrossRef
  2. Brown, I. H. 2000. The epidemiology and evolution of influenza viruses in pigs. Vet. Microbiol. 74: 29-46.
    CrossRef
  3. Brown, I. H., P. Chakraverty, P. A. Harris, and D. J. Alexander. 1995. Disease outbreaks in pigs in Great Britain due to an influenza A virus of H1N2 subtype. Vet. Rec. 136: 328-329.
    Pubmed CrossRef
  4. Brown, I. H., P. A. Harris, J. W. McCauley, and D. J. Alexander. 1998. Multiple genetic reassortment of avian and human influenza A viruses in European pigs, resulting in the emergence of an H1N2 virus of novel genotype. J. Gen. Virol. 79: 2947-2955.
    Pubmed
  5. Chen, G. W. and S. R. Shih. 2009. Genomic signatures of influenza A pandemic (H1N1) 2009 virus. Emerg. Infect. Dis. 15: 1897-1903.
    Pubmed
  6. Choi, Y. K., S. M. Goyal, M. W. Farnham, and H. S. Joo. 2002. Phylogenetic analysis of H1N2 isolates of influenza A virus from pigs in the United States. Virus Res. 87: 173-179.
    CrossRef
  7. Claas, E. C., Y. Kawaoka, J. C. de Jong, N. Masurel, and R. G. Webster. 1994. Infection of children with avian-human reassortant influenza virus from pigs in Europe. Virology 204:453-457.
    Pubmed CrossRef
  8. Fouchier, R. A., V. Munster, A. Wallensten, T. M. Bestebroer, S. Herfst, D. Smith, et al. 2005. Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J. Virol. 79: 2814-2822.
    Pubmed KoreaMed CrossRef
  9. Garten, R. J., C. T. Davis, C. A. Russell, B. Shu, S. Lindstrom, A. Balish, et al. 2009. Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325: 197-201.
    Pubmed KoreaMed CrossRef
  10. Howard, W. A., S. C. Essen, B. W. Strugnell, C. Russell, L. Barass, S. M. Reid, and I. H. Brown. 2011. Reassortant pandemic (H1N1) 2009 virus in pigs, United Kingdom. Emerg. Infect. Dis. 17: 1049-1052.
    Pubmed CrossRef
  11. Ito, T., J. N. Couceiro, S. Kelm, L. G. Baum, S. Krauss, M. R. Castrucci, et al. 1998. Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. J. Virol. 72:7367-7373.
    Pubmed KoreaMed
  12. Jo, S. K., H. S. Kim, S. W. Cho, and S. H. Seo. 2007. Genetic and antigenic characterization of swine H1N2 influenza viruses isolated from Korean pigs. J. Microbiol. Biotechnol. 17: 868-872.
    Pubmed
  13. Jung, K. and C. Chae. 2004. Phylogenetic analysis of an H1N2 influenza A virus isolated from a pig in Korea. Brief Report. Arch. Virol. 149: 1415-1422.
  14. Jung, K. and C. Chae. 2005. First outbreak of respiratory disease associated with swine influenza H1N2 virus in pigs in Korea. J. Vet. Diagn. Invest. 17: 176-178.
    Pubmed CrossRef
  15. Kitikoon, P., D. Sreta, S. N. Na Ayudhya, M. Wongphatcharachai, J. Lapkuntod, D. Prakairungnamthip, et al. 2011. Brief report:Molecular characterization of a novel reassorted pandemic H1N1 2009 in Thai pigs. Virus Genes 43: 1-5.
    Pubmed CrossRef
  16. Lee, C. S., B. K. Kang, H. K. Kim, S. J. Park, B. K. Park, K. Jung, and D. S. Song. 2008. Phylogenetic analysis of swine influenza viruses recently isolated in Korea. Virus Genes 37:168-176.
    Pubmed CrossRef
  17. Lee, C. S., B. K. Kang, D. H. Lee, S. H. Lyou, B. K. Park, S. K. Ann, et al. 2008. One-step multiplex RT-PCR for detection and subtyping of swine influenza H1, H3, N1, N2 viruses in clinical samples using a dual priming oligonucleotide (DPO) system. J. Virol. Methods 151: 30-34.
    Pubmed CrossRef
  18. Luoh, S. M., M. W. McGregor, and V. S. Hinshaw. 1992. Hemagglutinin mutations related to antigenic variation in H1 swine influenza viruses. J. Virol. 66: 1066-1073.
    Pubmed KoreaMed
  19. Massin, P., G. Kuntz-Simon, C. Barbezange, C. Deblanc, A. Oger, E. Marquet-Blouin, et al. 2010. Temperature sensitivity on growth and/or replication of H1N1, H1N2 and H3N2 influenza A viruses isolated from pigs and birds in mammalian cells. Vet. Microbiol. 142: 232-241.
    Pubmed CrossRef
  20. Moreno, A., L. Di Trani, S. Faccini, G. Vaccari, D. Nigrelli, M. B. Boniotti, et al. 2010. Novel H1N2 swine influenza reassortant strain in pigs derived from the pandemic H1N1/2009 virus. Vet. Microbiol. 149: 472-477.
    Pubmed CrossRef
  21. Olsen, C. W. 2002. The emergence of novel swine influenza viruses in North America. Virus Res. 85: 199-210.
    CrossRef
  22. Olsen, C. W., I. H. Brown, B. C. Easterday, and V. Reeth. 2006. In B. E. Straw, J. J. Zimmerman, S. D’Allaire, and D. J. Taylor (eds.). Disease of Swine. The Blackwell Publishing Professinal.
  23. Pascua, P. N., M. S. Song, J. H. Lee, H. W. Choi, J. H. Han, J. H. Kim, et al. 2008. Seroprevalence and genetic evolutions of swine influenza viruses under vaccination pressure in Korean swine herds. Virus Res. 138: 43-49.
    Pubmed CrossRef
  24. Pereda, A., J. Cappuccio, M. A. Quiroga, E. Baumeister, L. Insarralde, M. Ibar, et al. 2010. Pandemic (H1N1) 2009 outbreak on pig farm, Argentina. Emerg. Infect. Dis. 16: 304307.
    Pubmed
  25. Schnitzler, S. U. and P. Schnitzler. 2009. An update on swineorigin influenza virus A/H1N1: A review. Virus Genes 39:279-292.
    Pubmed CrossRef
  26. Shaw, M. W., N. H. Arden, and H. F. Maassab. 1992. New aspects of influenza viruses. Clin. Microbiol. Rev. 5: 74-92.
    Pubmed KoreaMed
  27. Shi, W., F. Lei, C. Zhu, F. Sievers, and D. G. Higgins. 2010. A complete analysis of HA and NA genes of influenza A viruses. PLoS One 5: e14454.
    Pubmed KoreaMed CrossRef
  28. Song, D. S., C. S. Lee, K. Jung, B. K. Kang, J. S. Oh, Y. D. Yoon, et al. 2007. Isolation and phylogenetic analysis of H1N1 swine influenza virus isolated in Korea. Virus Res. 125: 98103.
    Pubmed CrossRef
  29. Song, D. S., J. Y. Lee, J. S. Oh, K. S. Lyoo, K. J. Yoon, Y. H. Park, and B. K. Park. 2003. Isolation of H3N2 swine influenza virus in South Korea. J. Vet. Diagn. Invest. 15: 30-34.
    Pubmed CrossRef
  30. Song, M. S., J. H. Lee, P. N. Pascua, Y. H. Baek, H. I. Kwon, K. J. Park, et al. 2009. Evidence of human-to-swine transmission of the pandemic (H1N1) 2009 influenza virus in South Korea. J. Clin. Microbiol. 48: 3204-3211.
    Pubmed KoreaMed CrossRef
  31. Sreta, D., S. Tantawet, S. N. Na Ayudhya, A. Thontiravong, M. Wongphatcharachai, J. Lapkuntod, et al. 2010. Pandemic (H1N1) 2009 virus on commercial swine farm, Thailand. Emerg. Infect. Dis. 16: 1587-1590.
    Pubmed KoreaMed
  32. Starick, E., E. Lange, S. Fereidouni, C. Bunzenthal, R. Hoveler, A. Kuczka, et al. 2011. Reassorted pandemic (H1N1) 2009 influenza A virus discovered from pigs in Germany. J. Gen. Virol. 92: 1184-1188.
  33. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTAL_X Windows interface:Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25: 4876-4882.
    Pubmed KoreaMed CrossRef
  34. Tobita, K., A. Sugiura, C. Enomote, and M. Furuyama. 1975. Plaque assay and primary isolation of influenza A viruses in an established line of canine kidney cells (MDCK) in the presence of trypsin. Med. Microbiol. Immunol. 162: 9-14.
    Pubmed CrossRef
  35. Vijaykrishna, D., L. L. Poon, H. C. Zhu, S. K. Ma, O. T. Li, C. L. Cheung, et al. 2010. Reassortment of pandemic H1N1/2009 influenza A virus in swine. Science 328: 1529.
    Pubmed CrossRef
  36. Webster, R. G., W. J. Bean, O. T. Gorman, T. M. Chambers, and Y. Kawaoka. 1992. Evolution and ecology of influenza A viruses. Microbiol. Rev. 56: 152-179.
    Pubmed KoreaMed
  37. Weingartl, H. M., Y. Berhane, T. Hisanaga, J. Neufeld, H. Kehler, C. Emburry-Hyatt, et al. 2010. Genetic and pathobiologic characterization of pandemic H1N1 2009 influenza viruses from a naturally infected swine herd. J. Virol. 84: 2245-2256.
    Pubmed KoreaMed CrossRef
  38. WHO. 2009. Current WHO Phase of Pandemic Alert.
  39. Xu, C., Q. Zhu, H. Yang, X. Zhang, C. Qiao, Y. Chen, et al. 2009. Two genotypes of H1N2 swine influenza viruses appeared among pigs in China. J. Clin. Virol. 46: 192-195.
    Pubmed CrossRef
  40. Yu, H., P. C. Zhang, Y. J. Zhou, G. X. Li, J. Pan, L. P. Yan, et al. 2009. Isolation and genetic characterization of avian-like H1N1 and novel ressortant H1N2 influenza viruses from pigs in China. Biochem. Biophys Res. Commun. 386: 278-283.
    Pubmed CrossRef
  41. Zhou, N. N., D. A. Senne, J. S. Landgraf, S. L. Swenson, G. Erickson, K. Rossow, et al. 1999. Genetic reassortment of avian, swine, and human influenza A viruses in American pigs. J. Virol. 73: 8851-8856.
    Pubmed KoreaMed
  42. Zou, S. 1997. A practical approach to genetic screening for influenza virus variants. J. Clin. Microbiol. 35: 2623-2627.
    Pubmed KoreaMed