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. 2010 Feb 7;1(1):9–13. doi: 10.1007/s13238-010-0008-z

The emergence of pandemic influenza viruses

Yi Guan 1,✉, Dhanasekaran Vijaykrishna 1, Justin Bahl 1, Huachen Zhu 1, Jia Wang 1, Gavin J D Smith 1
PMCID: PMC4875113  PMID: 21203993

Abstract

Pandemic influenza has posed an increasing threat to public health worldwide in the last decade. In the 20th century, three human pandemic influenza outbreaks occurred in 1918, 1957 and 1968, causing significant mortality. A number of hypotheses have been proposed for the emergence and development of pandemic viruses, including direct introduction into humans from an avian origin and reassortment between avian and previously circulating human viruses, either directly in humans or via an intermediate mammalian host. However, the evolutionary history of the pandemic viruses has been controversial, largely due to the lack of background genetic information and rigorous phylogenetic analyses. The pandemic that emerged in early April 2009 in North America provides a unique opportunity to investigate its emergence and development both in human and animal aspects. Recent genetic analyses of data accumulated through long-term influenza surveillance provided insights into the emergence of this novel pandemic virus. In this review, we summarise the recent literature that describes the evolutionary pathway of the pandemic viruses. We also discuss the implications of these findings on the early detection and control of future pandemics.

Keywords: pandemic influenza, influenza virus, pandemics control

References

  1. Andreasen V., Viboud C., Simonsen L. Epidemiologic characterization of the 1918 influenza pandemic summer wave in Copenhagen: implications for pandemic control strategies. J Infect Dis. 2008;197:270–278. doi: 10.1086/524065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Centers for Disease ControlPrevention Swine influenza A (H1N1) infection in two children—southern California, March–April 2009. Morb Mortal Wkly Rep. 2009;58:400–402. [PubMed] [Google Scholar]
  3. Fang R., Jou W.M., Huylebroeck D., Devos R., Fiers W. Complete structure of A/duck/Ukraine/63 influenza hemagglutinin gene: animal virus as progenitor of human H3 Hong Kong 1968 influenza hemagglutinin. Cell. 1981;25:315–323. doi: 10.1016/0092-8674(81)90049-0. [DOI] [PubMed] [Google Scholar]
  4. Gammelin M., Altmuller A., Reinhardt U., Mandler J., Harley V.R., Hudson P.J., Fitch W.M., Scholtissek C. Phylogenetic analysis of nucleoproteins suggests that human influenza A viruses emerged from a 19th-century avian ancestor. Mol Biol Evol. 1990;7:194–200. doi: 10.1093/oxfordjournals.molbev.a040594. [DOI] [PubMed] [Google Scholar]
  5. Gorman O.T., Donis R.O., Kawaoka Y., Webster R.G. Evolution of influenza A virus PB2 genes: implications for evolution of the ribonucleoprotein complex and origin of human influenza A virus. J Virol. 1990;64:4893–4902. doi: 10.1128/jvi.64.10.4893-4902.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Gorman O.T., Bean W.J., Kawaoka Y., Donatelli I., Guo Y.J., Webster R.G. Evolution of influenza A virus nucleoprotein genes: implications for the origins of H1N1 human and classical swine viruses. J Virol. 1991;65:3704–3714. doi: 10.1128/jvi.65.7.3704-3714.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Kawaoka Y., Krauss S., Webster R.G. Avian-to-human transmission of the PB1 gene of influenza A viruses in the 1957 and 1968 pandemics. J Virol. 1989;63:4603–4608. doi: 10.1128/jvi.63.11.4603-4608.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Kilbourne E.D. Influenza pandemics of the 20th century. Emerg Infect Dis. 2006;12:9–14. doi: 10.3201/eid1201.051254. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ludwig S., Stitz L., Planz O., Van H., Fitch W.M., Scholtissek C. European swine virus as a possible source for the next pandemic? Virology. 1995;212:555–561. doi: 10.1006/viro.1995.1513. [DOI] [PubMed] [Google Scholar]
  10. Masurel N., Marine W.M. Recycling of Asian and Hong Kong Influenza A virus hemagglutinins in man. Am J Epidemiol. 1973;97:44–49. doi: 10.1093/oxfordjournals.aje.a121483. [DOI] [PubMed] [Google Scholar]
  11. Miller M.A., Viboud C., Balinska M., Simonsen L. The signature features of influenza pandemics-implications for policy. N Engl J Med. 2009;360:2595–2598. doi: 10.1056/NEJMp0903906. [DOI] [PubMed] [Google Scholar]
  12. Peiris J.S., Guan Y., Markwell D., Ghose P., Webster R.G., Shortridge K.F. Cocirculation of avian H9N2 and contemporary “human” H3N2 influenza A viruses in pigs in southeastern China: potential for genetic reassortment? J Virol. 2001;75:9679–9686. doi: 10.1128/JVI.75.20.9679-9686.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Scholtissek C., Rohde W., von Hoyningen V., Rott R. On the origin of the human influenza virus subtype H2N2 and H3N2. Virology. 1978;87:13–20. doi: 10.1016/0042-6822(78)90153-8. [DOI] [PubMed] [Google Scholar]
  14. Schultz U., Fitch W.M., Ludwig S., Mandler J., Scholtissek C. Evolution of pig influenza viruses. Virology. 1991;183:61–73. doi: 10.1016/0042-6822(91)90118-U. [DOI] [PubMed] [Google Scholar]
  15. Smith G.J., Bahl J., Vijaykrishna D., Zhang J., Poon L.L., Chen H., Webster R.G., Peiris J.S., Guan Y. Dating the emergence of pandemic influenza viruses. Proc Natl Acad Sci U S A. 2009;106:11709–11712. doi: 10.1073/pnas.0904991106. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Smith G.J., Vijaykrishna D., Bahl J., Lycett S.J., Worobey M., Pybus O.G., Ma S.K., Cheung C.L., Raghwani J., Bhatt S., et al. Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature. 2009;459:1122–1125. doi: 10.1038/nature08182. [DOI] [PubMed] [Google Scholar]
  17. Taubenberger J.K., Reid A.H., Lourens R.M., Wang R., Jin G., Fanning T.G. Characterization of the 1918 influenza virus polymerase genes. Nature. 2005;437:889–893. doi: 10.1038/nature04230. [DOI] [PubMed] [Google Scholar]
  18. Taubenberger J.K., Reid A.H., Lourens R.M., Wang R., Jin G., Fanning T.G. Molecular virology: was the 1918 pandemic caused by a bird flu? (Reply) Nature. 2006;440:E9–E10. doi: 10.1038/nature04825. [DOI] [PubMed] [Google Scholar]
  19. Taubenberger J.K., Morens D.M. 1918 influenza: the mother of all pandemics. Emerg Infect Dis. 2006;12:15–22. doi: 10.3201/eid1209.05-0979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Tumpey T.M., Basler C.F., Aguilar P.V., Zeng H., Solórzano A., Swayne D.E., Cox N.J., Katz J.M., Taubenberger J.K., Palese P., et al. Characterization of the reconstructed 1918 Spanish influenza pandemic virus. Science. 2005;310:77–80. doi: 10.1126/science.1119392. [DOI] [PubMed] [Google Scholar]
  21. Webster R.G., Bean W.J., Gorman O.T., Chambers T.M., Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol Rev. 1992;56:152–179. doi: 10.1128/mr.56.1.152-179.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Zhou N.N., Senne D.A., Landgraf J.S., Swenson S.L., Erickson G., Rossow K., Liu L., Yoon K., Krauss S., Webster R.G. Genetic reassortment of avian, swine, and human influenza A viruses in American pigs. J Virol. 1999;73:8851–8856. doi: 10.1128/jvi.73.10.8851-8856.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]

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