Skip to main content
SpringerLink
Log in

Characterization of a newly emerged genetic cluster of H1N1 and H1N2 swine influenza virus in the United States

  • Published:
Virus Genes Aims and scope Submit manuscript

Abstract

H1 influenza A viruses that were distinct from the classical swine H1 lineage were identified in pigs in Canada in 2003–2004; antigenic and genetic characterization identified the hemagglutinin (HA) as human H1 lineage. The viruses identified in Canadian pigs were human lineage in entirety or double (human–swine) reassortants. Here, we report the whole genome sequence analysis of four human-like H1 viruses isolated from U.S. swine in 2005 and 2007. All four isolates were characterized as triple reassortants with an internal gene constellation similar to contemporary U.S. swine influenza virus (SIV), with HA and neuraminidase (NA) most similar to human influenza virus lineages. A 2007 human-like H1N1 was evaluated in a pathogenesis and transmission model and compared to a 2004 reassortant H1N1 SIV isolate with swine lineage HA and NA. The 2007 isolate induced disease typical of influenza virus and was transmitted to contact pigs; however, the kinetics and magnitude differed from the 2004 H1N1 SIV. This study indicates that the human-like H1 SIV can efficiently replicate and transmit in the swine host and now co-circulates with contemporary SIVs as a distinct genetic cluster of H1 SIV.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. K.P. Myers, C.W. Olsen, G.C. Gray, Clin. Infect. Dis. 44, 1084–1088 (2007)

    Article  PubMed  PubMed Central  Google Scholar 

  2. N.N. Zhou, D.A. Senne, J.S. Landgraf, S.L. Swenson, G. Erickson, K. Rossow, L. Liu, K. Yoon, S. Krauss, R.G. Webster, J. Virol. 73, 8851–8856 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  3. A.L. Vincent, W. Ma, K.M. Lager, B.H. Janke, J.A. Richt, Adv. Virus Res. 72, 127–154 (2008)

    Article  CAS  PubMed  Google Scholar 

  4. A.I. Karasin, J. Landgraf, S. Swenson, G. Erickson, S. Goyal, M. Woodruff, G. Scherba, G. Anderson, C.W. Olsen, J. Clin. Microbiol. 40, 1073–1079 (2002)

    Article  PubMed  PubMed Central  Google Scholar 

  5. R.J. Webby, K. Rossow, G. Erickson, Y. Sims, R. Webster, Virus Res. 103, 67–73 (2004)

    Article  CAS  PubMed  Google Scholar 

  6. A.L. Vincent, K.M. Lager, W. Ma, P. Lekcharoensuk, M.R. Gramer, C. Loiacono, J.A. Richt, Vet. Microbiol. 118, 212–222 (2006)

    Article  CAS  PubMed  Google Scholar 

  7. R.J. Webby, S.L. Swenson, S.L. Krauss, P.J. Gerrish, S.M. Goyal, R.G. Webster, J. Virol. 74, 8243–8251 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. J.A. Richt, K.M. Lager, B.H. Janke, R.D. Woods, R.G. Webster, R.J. Webby, J. Clin. Microbiol. 41, 3198–3205 (2003)

    Article  PubMed  PubMed Central  Google Scholar 

  9. C.W. Olsen, A.I. Karasin, S. Carman, Y. Li, N. Bastien, D. Ojkic, D. Alves, G. Charbonneau, B.M. Henning, D.E. Low, L. Burton, G. Broukhanski, Emerg. Infect. Dis. 12, 1132–1135 (2006)

    Article  PubMed  PubMed Central  Google Scholar 

  10. Y.K. Choi, S.M. Goyal, M.W. Farnham, H.S. Joo, Virus Res. 87, 173–179 (2002)

    Article  CAS  PubMed  Google Scholar 

  11. W. Ma, M. Gramer, K. Rossow, K.J. Yoon, J. Virol. 80, 5092–5096 (2006)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. P. Lekcharoensuk, K.M. Lager, R. Vemulapalli, M. Woodruff, A.L. Vincent, J.A. Richt, Emerg. Infect. Dis. 12, 787–794 (2006)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. W. Ma, A.L. Vincent, M.R. Gramer, C.B. Brockwell, K.M. Lager, B.H. Janke, P.C. Gauger, D.P. Patnayak, R.J. Webby, J.A. Richt, Proc. Natl Acad. Sci. USA 104, 20949–20954 (2007)

    Article  CAS  PubMed  Google Scholar 

  14. F.S. Dawood, S. Jain, L. Finelli, M.W. Shaw, S. Lindstrom, R.J. Garten, L.V. Gubareva, X. Xu, C.B. Bridges, T.M. Uyeki, N. Engl. J. Med. 360, 2605–2615 (2009)

  15. R.J. Garten, C.T. Davis, C.A. Russell, B. Shu, S. Lindstrom, A. Balish, W.M. Sessions, X. Xu, E. Skepner, V. Deyde, M. Okomo-Adhiambo, L. Gubareva, J. Barnes, C.B. Smith, S.L. Emery, M.J. Hillman, P. Rivailler, J. Smagala, M. de Graaf, D.F. Burke, R.A. Fouchier, C. Pappas, C.M. Alpuche-Aranda, H. Lopez-Gatell, H. Olivera, I. Lopez, C.A. Myers, D. Faix, P.J. Blair, C. Yu, K.M. Keene, P.D. Dotson Jr., D. Boxrud, A.R. Sambol, S.H. Abid, K. St. George, T. Bannerman, A.L. Moore, D.J. Stringer, P. Blevins, G.J. Demmler-Harrison, M. Ginsberg, P. Kriner, S. Waterman, S. Smole, H.F. Guevara, E.A. Belongia, P.A. Clark, S.T. Beatrice, R. Donis, J. Katz, L. Finelli, C.B. Bridges, M. Shaw, D.B. Jernigan, T.M. Uyeki, D.J. Smith, A.I. Klimov, N.J. Cox, Science (2009). doi:https://doi.org/10.1126/science.1176225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. A.I. Karasin, S. Carman, C.W. Olsen, J. Clin. Microbiol. 44, 1123–1126 (2006)

    Article  PubMed  PubMed Central  Google Scholar 

  17. M.R. Gramer, SIV: An update on circulating strains, advances in diagnostic tests and interpretation of test results, in 38th Annual Meeting of the American Association of Swine Veterinarians, Orlando, FL, 2007

  18. C.H. Chan, K.L. Lin, Y. Chan, Y.L. Wang, Y.T. Chi, H.L. Tu, H.K. Shieh, W.T. Liu, J. Virol. Methods 136, 38–43 (2006)

    Article  CAS  PubMed  Google Scholar 

  19. E. Hoffmann, J. Stech, Y. Guan, R.G. Webster, D.R. Perez, Arch. Virol. 146, 2275–2289 (2001)

    Article  CAS  PubMed  Google Scholar 

  20. K. Tamura, J. Dudley, M. Nei, S. Kumar, Mol. Biol. Evol. 24, 1596–1599 (2007)

    Article  CAS  PubMed  Google Scholar 

  21. A.J. Caton, G.G. Brownlee, J.W. Yewdell, W. Gerhard, Cell 31, 417–427 (1982)

    Article  CAS  PubMed  Google Scholar 

  22. M.N. Matrosovich, A.S. Gambaryan, S. Teneberg, V.E. Piskarev, S.S. Yamnikova, D.K. Lvov, J.S. Robertson, K.A. Karlsson, Virology 233, 224–234 (1997)

    Article  CAS  PubMed  Google Scholar 

  23. T.G. Fanning, J.K. Taubenberger, Virus Res. 65, 33–42 (1999)

    Article  CAS  PubMed  Google Scholar 

  24. T.G. Fanning, A.H. Reid, J.K. Taubenberger, Virology 276, 417–423 (2000)

    Article  CAS  PubMed  Google Scholar 

  25. P. Kitikoon, D. Nilubol, B.J. Erickson, B.H. Janke, T. Hoover, S. Sornsen, E.L. Thacker, Vet. Immunol. Immunopathol. 112, 117–128 (2006)

    Article  CAS  PubMed  Google Scholar 

  26. L.J. Reed, H. Muench, Am. J. Hyg. 27, 493–497 (1938)

    Google Scholar 

  27. P.G. Halbur, P.S. Paul, M.L. Frey, J. Landgraf, K. Eernisse, X.J. Meng, M.A. Lum, J.J. Andrews, J.A. Rathje, Vet. Pathol. 32, 648–660 (1995)

    Article  CAS  PubMed  Google Scholar 

  28. D.F. Palmer, M.T. Coleman, W.R. Dowdle, G.C. Schild, Advanced Laboratory Techniques for Influenza Diagnosis. Immunology Series No. 6 (U. S. Department of Health, Education and Welfare, Washington, DC, 1975), pp. 51–52

  29. G.A. Landolt, C.W. Olsen, Anim. Health Res. Rev. 8, 1–21 (2007)

    Article  PubMed  Google Scholar 

  30. M. Matrosovich, A. Tuzikov, N. Bovin, A. Gambaryan, A. Klimov, M.R. Castrucci, I. Donatelli, Y. Kawaoka, J. Virol. 74, 8502–8512 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. T. Ito, J.N. Couceiro, S. Kelm, L.G. Baum, S. Krauss, M.R. Castrucci, I. Donatelli, H. Kida, J.C. Paulson, R.G. Webster, Y. Kawaoka, J. Virol. 72, 7367–7373 (1998)

    CAS  PubMed  PubMed Central  Google Scholar 

  32. G.J.D. Smith, D. Vijaykrishna, J. Bahl, S.J. Lycett, M. Worobey, O.G. Pybus, S.K. Ma, C.L. Cheung, J. Raghwani, S. Bhatt, J.S.M. Peiris, Y. Guan, A. Rambaut, Nature 459, 1122–1125 (2009)

    Article  CAS  PubMed  Google Scholar 

  33. A.I. Karasin, K. West, S. Carman, C.W. Olsen, J. Clin. Microbiol. 42, 4349–4354 (2004)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. C.W. Olsen, A. Karasin, G. Erickson, Virus Res. 93, 115–121 (2003)

    Article  CAS  PubMed  Google Scholar 

  35. H. Yu, G.H. Zhang, R.H. Hua, Q. Zhang, T.Q. Liu, M. Liao, G.Z. Tong, Biochem. Biophys. Res. Commun. 356, 91–96 (2007)

    Article  CAS  PubMed  Google Scholar 

  36. M.M.W.R. Morb, Mortal Wkly. Rep. 58, 400–402 (2009)

    Google Scholar 

Download references

Acknowledgments

We thank the NADC sequencing facility, Matt Kappes, Michelle Harland, Deb Adolphson, Brian Pottebaum, and Jason Huegel for assistance with laboratory techniques and animal studies and Dr. Brian Brunelle for critical review of the manuscript. Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture.

Author information

Authors and Affiliations

  1. Virus and Prion Diseases of Livestock Research Unit, National Animal Disease Center, USDA-ARS, 2300 Dayton Road, Ames, IA, 50010, USA

    Amy L. Vincent, Wenjun Ma, Kelly M. Lager & Juergen A. Richt

  2. Department of Veterinary Diagnostic and Production Animal Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA, USA

    Wenjun Ma & Bruce H. Janke

  3. Minnesota Veterinary Diagnostic Laboratory, University of Minnesota, St. Paul, MN, USA

    Marie R. Gramer

Authors
  1. Amy L. Vincent
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wenjun Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kelly M. Lager
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marie R. Gramer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Juergen A. Richt
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bruce H. Janke
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Amy L. Vincent.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vincent, A.L., Ma, W., Lager, K.M. et al. Characterization of a newly emerged genetic cluster of H1N1 and H1N2 swine influenza virus in the United States. Virus Genes 39, 176–185 (2009). https://doi.org/10.1007/s11262-009-0386-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11262-009-0386-6

Keywords

Search

Navigation