Skip to main content

Emergence of novel reassortant H3N2 swine influenza viruses with the 2009 pandemic H1N1 genes in the United States


Reassortant H1 swine influenza viruses (SIVs) carrying 2009 pandemic H1N1 virus (pH1N1) genes have been isolated from pigs worldwide. Seven novel reassortant H3N2 SIVs were identified from diseased pigs in the USA from winter 2010 to spring 2011. These novel viruses contain three or five internal genes from pH1N1 and continue to circulate in swine herds. The emergence of novel reassortant H3N2 SIVs demonstrates reassortment between pH1N1 and endemic SIVs in pigs and justifies continuous surveillance.

This is a preview of subscription content, access via your institution.

Fig. 1


  1. 1.

    Pennsylvania Department of Health (Sept 5, 2011) Novel influenza-A cases linked to county fair; Pennsylvanians should continue flu prevention practices and report flu-like illness

  2. 2.

    Bussey KA, Bousse TL, Desmet EA, Kim B, Takimoto T (2010) PB2 residue 271 plays a key role in enhanced polymerase activity of influenza A viruses in mammalian host cells. J Virol 84:4395–4406

    PubMed  Article  CAS  Google Scholar 

  3. 3.

    Centers for Disease Control and Prevention (2011) Swine-origin influenza A (H3N2) virus infection in two children—Indiana and Pennsylvania. Morb Mortal Wkl Rep (MMWR) 60:1213–1215

    Google Scholar 

  4. 4.

    Cox CM, Neises D, Garten RJ, Bryant B, Hesse RA, Anderson GA, Trevino-Garrison I, Shu B, Lindstrom S, Klimov AI, Finelli L (2011) Swine influenza virus A (H3N2) infection in human, Kansas, USA, 2009. Emerg Infect Dis 17:1143–1144

    PubMed  Article  Google Scholar 

  5. 5.

    Ducatez MF, Hause B, Stigger-Rosser E, Darnell D, Corzo C, Juleen K, Simonson R, Brockwell-Staats C, Rubrum A, Wang D, Webb A, Crumpton JC, Lowe J, Gramer M, Webby RJ (2011) Multiple reassortment between pandemic (H1N1) 2009 and endemic influenza viruses in pigs, United States. Emerg Infect Dis 17:1624–1629

    PubMed  Article  Google Scholar 

  6. 6.

    Gabriel G, Dauber B, Wolff T, Planz O, Klenk HD, Stech J (2005) The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proc Natl Acad Sci USA 102:18590–18595

    PubMed  Article  CAS  Google Scholar 

  7. 7.

    Howard WA, Essen SC, Strugnell BW, Russell C, Barass L, Reid SM, Brown IH (2011) Reassortant pandemic (H1N1) 2009 virus in pigs, United Kingdom. Emerg Infect Dis 17:1049–1052

    PubMed  Article  Google Scholar 

  8. 8.

    Howden KJ, Brockhoff EJ, Caya FD, McLeod LJ, Lavoie M, Ing JD, Bystrom JM, Alexandersen S, Pasick JM, Berhane Y, Morrison ME, Keenliside JM, Laurendeau S, Rohonczy EB (2009) An investigation into human pandemic influenza virus (H1N1) 2009 on an Alberta swine farm. Can Vet J 50:1153–1161

    PubMed  Google Scholar 

  9. 9.

    Kimble JB, Sorrell E, Shao H, Martin PL, Perez DR (2011) Compatibility of H9N2 avian influenza surface genes and 2009 pandemic H1N1 internal genes for transmission in the ferret model. Proc Natl Acad Sci USA 108:12084–12088

    PubMed  Article  CAS  Google Scholar 

  10. 10.

    Kitikoon P, Sreta D, Nuntawan Na Ayudhya S, Wongphatcharachai M, Lapkuntod J, Prakairungnamthip D, Bunpapong N, Suradhat S, Thanawongnuwech R, Amonsin A (2011) Brief report: molecular characterization of a novel reassorted pandemic H1N1 2009 in Thai pigs. Virus Genes. doi:10.1007/s11262-11011-10597-11265

    PubMed  Google Scholar 

  11. 11.

    Li Z, Chen H, Jiao P, Deng G, Tian G, Li Y, Hoffmann E, Webster RG, Matsuoka Y, Yu K (2005) Molecular basis of replication of duck H5N1 influenza viruses in a mammalian mouse model. J Virol 79:12058–12064

    PubMed  Article  CAS  Google Scholar 

  12. 12.

    Ma W, Oberst R, Li X, Clouser D, Hesse R, Rowland R, Richt JA (2010) Rapid detection of the pandemic 2009 H1N1 virus M gene by real-time and gel-based RT-PCR assays. Influenza Other Respi Viruses 4:397–403

    PubMed  Article  CAS  Google Scholar 

  13. 13.

    Matrosovich MN, Gambaryan AS, Teneberg S, Piskarev VE, Yamnikova SS, Lvov DK, Robertson JS, Karlsson KA (1997) Avian influenza A viruses differ from human viruses by recognition of sialyloligosaccharides and gangliosides and by a higher conservation of the HA receptor-binding site. Virology 233:224–234

    PubMed  Article  CAS  Google Scholar 

  14. 14.

    Mehle A, Doudna JA (2009) Adaptive strategies of the influenza virus polymerase for replication in humans. Proc Natl Acad Sci USA 106:21312–21316

    PubMed  Article  CAS  Google Scholar 

  15. 15.

    Moreno A, Di Trani L, Faccini S, Vaccari G, Nigrelli D, Boniotti MB, Falcone E, Boni A, Chiapponi C, Sozzi E, Cordioli P (2011) Novel H1N2 swine influenza reassortant strain in pigs derived from the pandemic H1N1/2009 virus. Vet Microbiol 149:472–477

    PubMed  Article  CAS  Google Scholar 

  16. 16.

    Richt JA, Lager KM, Janke BH, Woods RD, Webster RG, Webby RJ (2003) Pathogenic and antigenic properties of phylogenetically distinct reassortant H3N2 swine influenza viruses cocirculating in the United States. J Clin Microbiol 41:3198–3205

    PubMed  Article  Google Scholar 

  17. 17.

    Schrauwen EJ, Herfst S, Chutinimitkul S, Bestebroer TM, Rimmelzwaan GF, Osterhaus AD, Kuiken T, Fouchier RA (2011) Possible increased pathogenicity of pandemic (H1N1) 2009 influenza virus upon reassortment. Emerg Infect Dis 17:200–208

    PubMed  Google Scholar 

  18. 18.

    Starick E, Lange E, Fereidouni S, Bunzenthal C, Hoveler R, Kuczka A, grosse Beilage E, Hamann HP, Klingelhofer I, Steinhauer D, Vahlenkamp T, Beer M, Harder T (2011) Reassorted pandemic (H1N1) 2009 influenza A virus discovered from pigs in Germany. J Gen Virol 92:1184–1188

    PubMed  Article  CAS  Google Scholar 

  19. 19.

    Subbarao EK, London W, Murphy BR (1993) A single amino acid in the PB2 gene of influenza A virus is a determinant of host range. J Virol 67:1761–1764

    PubMed  CAS  Google Scholar 

  20. 20.

    Sun D, Schwartz KJ, Janke GH, Haney D, Block S, Yoon KJ (2011) Occurrence of novel reassortants between North American swine influenza virus and pandemic 2009 H1N1 virus in US swine. In: American Society for Virology 30th Annual Meeting, University of Minnesota, Minneapolis, p 221

  21. 21.

    UDSA (2010) 2009 Pandemic H1N1 Influenza presumptive and confirmed results (January 19, 2010)

  22. 22.

    Vijaykrishna D, Poon LL, Zhu HC, Ma SK, Li OT, Cheung CL, Smith GJ, Peiris JS, Guan Y (2010) Reassortment of pandemic H1N1/2009 influenza A virus in swine. Science 328:1529

    PubMed  Article  CAS  Google Scholar 

  23. 23.

    Vincent AL, Ma W, Lager KM, Janke BH, Richt JA (2008) Swine influenza viruses a North American perspective. Adv Virus Res 72:127–154

    PubMed  Article  CAS  Google Scholar 

  24. 24.

    Webby RJ, Rossow K, Erickson G, Sims Y, Webster R (2004) Multiple lineages of antigenically and genetically diverse influenza A virus co-circulate in the United States swine population. Virus Res 103:67–73

    PubMed  Article  CAS  Google Scholar 

Download references


This study was partially supported by a grant from the National Institute of Allergy and Infectious Diseases, National Institute of Health, Department of Health and Human Services (Contract No. HHSN266200700005C), and by CEEZAD program of the Department of Homeland Security (Cooperative Agreement No. 2010-ST-061-AG0001-02).

Author information



Corresponding author

Correspondence to Wenjun Ma.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Liu, Q., Ma, J., Liu, H. et al. Emergence of novel reassortant H3N2 swine influenza viruses with the 2009 pandemic H1N1 genes in the United States. Arch Virol 157, 555–562 (2012).

Download citation


  • Reassortment
  • Pandemic H1N1
  • H3N2 swine influenza virus