Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Identification of Reassortant Pandemic H1N1 Influenza Virus in Korean Pigs

  • Han, Jae-Yeon (Department of Veterinary Medicine Virology Laboratory College of Veterinary Medicine and BK21 Program for Veterinary Science, Seoul National University) ;
  • Park, Sung-Jun (Department of Veterinary Medicine Virology Laboratory College of Veterinary Medicine and BK21 Program for Veterinary Science, Seoul National University) ;
  • Kim, Hye-Kwon (Department of Veterinary Medicine Virology Laboratory College of Veterinary Medicine and BK21 Program for Veterinary Science, Seoul National University) ;
  • Rho, Se-Mi (Department of Veterinary Medicine Virology Laboratory College of Veterinary Medicine and BK21 Program for Veterinary Science, Seoul National University) ;
  • Nguyen, Giap Van (Department of Veterinary Medicine Virology Laboratory College of Veterinary Medicine and BK21 Program for Veterinary Science, Seoul National University) ;
  • Song, Dae-Sub (Research Unit, Green Cross Veterinary Products) ;
  • Kang, Bo-Kyu (Research Unit, Green Cross Veterinary Products) ;
  • Moon, Hyung-Jun (Research Unit, Green Cross Veterinary Products) ;
  • Yeom, Min-Joo (Research Unit, Green Cross Veterinary Products) ;
  • Park, Bong-Kyun (Department of Veterinary Medicine Virology Laboratory College of Veterinary Medicine and BK21 Program for Veterinary Science, Seoul National University)
  • Received : 2011.06.08
  • Accepted : 2011.12.30
  • Published : 2012.05.28
Download PDF
⟨ Previous Next ⟩

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

References

  1. Alexander, D. J. 2007. An overview of the epidemiology of avian influenza. Vaccine 25: 5637-5644. https://doi.org/10.1016/j.vaccine.2006.10.051
  2. Brown, I. H. 2000. The epidemiology and evolution of influenza viruses in pigs. Vet. Microbiol. 74: 29-46. https://doi.org/10.1016/S0378-1135(00)00164-4
  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. https://doi.org/10.1136/vr.136.13.328
  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.
  5. Chen, G. W. and S. R. Shih. 2009. Genomic signatures of influenza A pandemic (H1N1) 2009 virus. Emerg. Infect. Dis. 15: 1897-1903. https://doi.org/10.3201/eid1512.090845
  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. https://doi.org/10.1016/S0168-1702(02)00053-9
  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. https://doi.org/10.1006/viro.1994.1553
  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. https://doi.org/10.1128/JVI.79.5.2814-2822.2005
  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. https://doi.org/10.1126/science.1176225
  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. https://doi.org/10.3201/eid1706.101886
  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.
  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.
  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. https://doi.org/10.1177/104063870501700213
  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. https://doi.org/10.1007/s11262-011-0597-5
  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. https://doi.org/10.1007/s11262-008-0251-z
  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. https://doi.org/10.1016/j.jviromet.2008.04.001
  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.
  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. https://doi.org/10.1016/j.vetmic.2009.10.012
  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.
  21. Olsen, C. W. 2002. The emergence of novel swine influenza viruses in North America. Virus Res. 85: 199-210. https://doi.org/10.1016/S0168-1702(02)00027-8
  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. https://doi.org/10.1016/j.virusres.2008.08.005
  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: 304-307. https://doi.org/10.3201/eid1602.091230
  25. Schnitzler, S. U. and P. Schnitzler. 2009. An update on swineorigin influenza virus A/H1N1: A review. Virus Genes 39: 279-292. https://doi.org/10.1007/s11262-009-0404-8
  26. Shaw, M. W., N. H. Arden, and H. F. Maassab. 1992. New aspects of influenza viruses. Clin. Microbiol. Rev. 5: 74-92.
  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. https://doi.org/10.1371/journal.pone.0014454
  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: 98-103. https://doi.org/10.1016/j.virusres.2006.11.008
  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. https://doi.org/10.1177/104063870301500107
  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.
  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. https://doi.org/10.3201/eid1610.100665
  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. https://doi.org/10.1099/vir.0.028662-0
  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. https://doi.org/10.1093/nar/25.24.4876
  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. https://doi.org/10.1007/BF02123572
  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. https://doi.org/10.1126/science.1189132
  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.
  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. https://doi.org/10.1128/JVI.02118-09
  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. https://doi.org/10.1016/j.jcv.2009.06.022
  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. https://doi.org/10.1016/j.bbrc.2009.05.056
  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.
  42. Zou, S. 1997. A practical approach to genetic screening for influenza virus variants. J. Clin. Microbiol. 35: 2623-2627.

Cited by

  1. Reassortants of pandemic influenza A virus H1N1/2009 and endemic porcine HxN2 viruses emerge in swine populations in Germany vol.93, pp.8, 2012, https://doi.org/10.1099/vir.0.042648-0
  2. Emergence of H3N2pM‐like and novel reassortant H3N1 swine viruses possessing segments derived from the A (H1N1)pdm09 influenza virus, Korea vol.7, pp.6, 2012, https://doi.org/10.1111/irv.12154
  3. Complete Genome Sequences of Novel Reassortant H1N2 Swine Influenza Viruses Isolated from Pigs in the Republic of Korea vol.1, pp.4, 2012, https://doi.org/10.1128/genomea.00552-13
  4. Virus‐specific factors associated with zoonotic and pandemic potential vol.7, pp.suppl2, 2012, https://doi.org/10.1111/irv.12075
  5. Reassortant swine influenza viruses isolated in Japan contain genes from pandemic A(H1N1) 2009 vol.58, pp.6, 2014, https://doi.org/10.1111/1348-0421.12152
  6. Comparative pathology of pigs infected with Korean H1N1, H1N2, or H3N2 swine influenza A viruses vol.11, pp.1, 2014, https://doi.org/10.1186/1743-422x-11-170
  7. Genomic Reassortants of Pandemic A (H1N1) 2009 Virus and Endemic Porcine H1 and H3 Viruses in Swine in Japan vol.76, pp.11, 2012, https://doi.org/10.1292/jvms.14-0194
  8. Differences in transmissibility and pathogenicity of reassortants between H9N2 and 2009 pandemic H1N1 influenza A viruses from humans and swine vol.159, pp.7, 2012, https://doi.org/10.1007/s00705-014-2009-3