Skip to main content
Log in

H5 influenza, a global update

  • Review
  • Emerging and Re-emerging Viral Disease and Vaccines
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

H5 influenza viruses have caused much alarm globally due to their high pathogenic potential. As yet we have not seen sustained spread of the virus amongst humans despite a high prevalence of the virus in avian populations. Nevertheless, isolated human cases of infection have demonstrated high mortality and there are substantial efforts being taken to monitor the evolution of the virus and to undertake preparedness activities. Here we review and discuss the evolution of the A/goose/Guangdong/1/96 (H5N1) virus with emphasis on recent events.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abdelwhab, E.M., Hassan, M.K., Abdel-Moneim, A.S., Naguib, M.M., Mostafa, A., Hussein, I.T., Arafa, A., Erfan, A.M., Kilany, W.H., Agour, M.G., et al. 2016. Introduction and enzootic of A/H5N1 in Egypt: Virus evolution, pathogenicity and vaccine efficacy ten years on. Infect. Genet. Evol. 40, 80–90.

    Article  CAS  PubMed  Google Scholar 

  • Abozaid, K.G., Aly, M.M., Abdel-Moneim, A.S., and El-Kady, M.F. 2016. Widespread of H5N1 infections in apparently healthy backyard poultry. Trop. Anim. Health Prod. 48, 1221–1226.

    Article  PubMed  Google Scholar 

  • Alan, H., Ian, B., Nancy, C., Ruben, O.D., Siddhivinayak, H., Daniel, J., Jacqueline, K., John, M., Fernando, M., Takato, O., et al. 2017. Improving the selection and development of influenza vaccine viruses -Report of a WHO informal consultation on improving influenza vaccine virus selection, Hong Kong SAR, China, 18–20 November 2015. Vaccine 35, 1104–1109.

    Article  PubMed  Google Scholar 

  • Belshe, R.B., Frey, S.E., Graham, I., Mulligan, M.J., Edupuganti, S., Jackson, L.A., Wald, A., Poland, G., Jacobson, R., Keyserling, H.L., et al. 2011. Safety and immunogenicity of influenza A H5 subunit vaccines: effect of vaccine schedule and antigenic variant. J. Infect. Dis. 203, 666–673.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bridges, C.B., Lim, W., Hu-Primmer, J., Sims, L., Fukuda, K., Mak, K.H., Rowe, T., Thompson, W.W., Conn, L., Lu, X., et al. 2002. Risk of influenza A (H5N1) infection among poultry workers, Hong Kong, 1997-1998. J. Infect. Dis. 185, 1005–1010.

    Article  PubMed  Google Scholar 

  • Buchy, P., Vong, S., Chu, S., Garcia, J.M., Hien, T.T., Hien, V.M., Channa, M., Ha do, Q., Chau, N.V., Simmons, C., et al. 2010. Kinetics of neutralizing antibodies in patients naturally infected by H5N1 virus. PLoS One 5, e10864.

    Article  Google Scholar 

  • Cattoli, G., Fusaro, A., Monne, I., Coven, F., Joannis, T., El-Hamid, H.S., Hussein, A.A., Cornelius, C., Amarin, N.M., Mancin, M., et al. 2011. Evidence for differing evolutionary dynamics of A/H5N1 viruses among countries applying or not applying avian influenza vaccination in poultry. Vaccine 29, 9368–9375.

    Article  PubMed  Google Scholar 

  • Chen, H., Smith, G.J., Zhang, S.Y., Qin, K., Wang, J., Li, K.S., Webster, R.G., Peiris, J.S., and Guan, Y. 2005. Avian flu: H5N1 virus outbreak in migratory waterfowl. Nature 436, 191–192.

    Article  CAS  PubMed  Google Scholar 

  • Couacy-Hymann, E., Kouakou, V.A., Aplogan, G.L., Awoume, F., Kouakou, C.K., Kakpo, L., Sharp, B.R., McClenaghan, L., McKenzie, P., Webster, R.G., et al. 2012. Surveillance for influenza viruses in poultry and swine, west Africa, 2006-2008. Emerg. Infect. Dis. 18, 1446–1452.

    Article  PubMed  PubMed Central  Google Scholar 

  • Di Trani, L., Porru, S., Bonfanti, L., Cordioli, P., Cesana, B.M., Boni, A., Di Carlo, A.S., Arici, C., Donatelli, I., Tomao, P., et al. 2012. Serosurvey against H5 and H7 avian influenza viruses in Italian poultry workers. Avian Dis. 56, 1068–1071.

    Article  PubMed  Google Scholar 

  • El-Shesheny, R., Kandeil, A., Bagato, O., Maatouq, A.M., Moatasim, Y., Rubrum, A., Song, M.S., Webby, R.J., Ali, M.A., and Kayali, G. 2014. Molecular characterization of avian influenza H5N1 virus in Egypt and the emergence of a novel endemic subclade. J. Gen. Virol. 95, 1444–1463.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • El Rifay, A.S., Elabd, M.A., Abu Zeid, D., Gomaa, M.R., Tang, L., McKenzie, P.P., Webby, R.J., Ali, M.A., and Kayali, G. 2015. Household transmission of zoonotic influenza viruses in a cohort of Egyptian poultry growers. JMIR Res. Protoc. 4, e74.

    Article  Google Scholar 

  • Eladl, A.E., El-Azm, K.I., Ismail, A.E., Ali, A., Saif, Y.M., and Lee, C.W. 2011. Genetic characterization of highly pathogenic H5N1 avian influenza viruses isolated from poultry farms in Egypt. Virus Genes 43, 272–280.

    Article  CAS  PubMed  Google Scholar 

  • Fiore, A.E., Bridges, C.B., and Cox, N.J. 2009. Seasonal influenza vaccines. Curr. Top Microbiol. Immunol. 333, 43–82.

    CAS  PubMed  Google Scholar 

  • Furuya-Kanamori, L., Cox, M., Milinovich, G.J., Magalhaes, R.J., Mackay, I.M., and Yakob, L. 2016. Heterogeneous and dynamic prevalence of asymptomatic influenza virus infections. Emerg. Infect. Dis. 22, 1052–1056.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gerdil, C. 2003. The annual production cycle for influenza vaccine. Vaccine 21, 1776–1779.

    Article  PubMed  Google Scholar 

  • Goji, N.A., Nolan, C., Hill, H., Wolff, M., Noah, D.L., Williams, T.B., Rowe, T., and Treanor, J.J. 2008. Immune responses of healthy subjects to a single dose of intramuscular inactivated influenza A/Vietnam/1203/2004 (H5N1) vaccine after priming with an antigenic variant. J. Infect. Dis. 198, 635–641.

    Article  PubMed  Google Scholar 

  • Gomaa, M.R., Kandeil, A., Kayed, A.S., Elabd, M.A., Zaki, S.A., Abu Zeid, D., El Rifay, A.S., Mousa, A.A., Farag, M.M., McKenzie, P.P., et al. 2016. Serological evidence of human infection with avian influenza A H7 virus in Egyptian poultry growers. PLoS One 11, e0155294.

    Google Scholar 

  • Gu, M., Zhao, G., Zhao, K., Zhong, L., Huang, J., Wan, H., Wang, X., Liu, W., Liu, H., Peng, D., et al. 2013. Novel variants of clade 2.3.4 highly pathogenic avian influenza A(H5N1) viruses, China. Emerg. Infect. Dis. 19, 2021–2024.

    Article  PubMed  PubMed Central  Google Scholar 

  • Guan, Y., Poon, L.L., Cheung, C.Y., Ellis, T.M., Lim, W., Lipatov, A.S., Chan, K.H., Sturm-Ramirez, K.M., Cheung, C.L., Leung, Y.H., et al. 2004. H5N1 influenza: a protean pandemic threat. Proc. Natl. Acad. Sci. USA 101, 8156–8161.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herfst, S., Schrauwen, E.J., Linster, M., Chutinimitkul, S., de Wit, E., Munster, V.J., Sorrell, E.M., Bestebroer, T.M., Burke, D.F., Smith, D.J., et al. 2012. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336, 1534–1541.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Imai, M., Watanabe, T., Hatta, M., Das, S.C., Ozawa, M., Shinya, K., Zhong, G., Hanson, A., Katsura, H., Watanabe, S., et al. 2012. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 486, 420–428.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ip, H.S., Torchetti, M.K., Crespo, R., Kohrs, P., DeBruyn, P., Mansfield, K.G., Baszler, T., Badcoe, L., Bodenstein, B., Shearn-Bochsler, V., et al. 2015. Novel Eurasian highly pathogenic avian influenza A H5 viruses in wild birds, Washington, USA, 2014. Emerg. Infect. Dis. 21, 886–890.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Islam, M.R., Haque, M.E., Giasuddin, M., Chowdhury, E.H., Samad, M.A., Parvin, R., Nooruzzaman, M., Rahman, M.M., and Monoura, P. 2012. New introduction of clade 2.3.2.1 avian influenza virus (H5N1) into Bangladesh. Transbound Emerg. Dis. 59, 460–463.

    Article  CAS  PubMed  Google Scholar 

  • Kandun, I.N., Wibisono, H., Sedyaningsih, E.R., Yusharmen, Hadisoedarsuno, W., Purba, W., Santoso, H., Septiawati, C., Tresnaningsih, E., Heriyanto, B., et al. 2006. Three Indonesian clusters of H5N1 virus infection in 2005. N. Engl. J. Med. 355, 2186–2194.

    Article  CAS  PubMed  Google Scholar 

  • Kayali, G., Kandeil, A., El-Shesheny, R., Kayed, A.S., Gomaa, M.M., Maatouq, A.M., Shehata, M.M., Moatasim, Y., Bagato, O., Cai, Z., et al. 2014. Active surveillance for avian influenza virus, Egypt, 2010-2012. Emerg. Infect. Dis. 20, 542–551.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kayali, G., Kandeil, A., El-Shesheny, R., Kayed, A.S., Maatouq, A.M., Cai, Z., McKenzie, P.P., Webby, R.J., El Refaey, S., Kandeel, A., et al. 2016. Avian influenza A(H5N1) virus in Egypt. Emerg. Infect. Dis. 22, 379–388.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kayali, G., Webby, R.J., Ducatez, M.F., El Shesheny, R.A., Kandeil, A.M., Govorkova, E.A., Mostafa, A., and Ali, M.A. 2011. The epidemiological and molecular aspects of influenza H5N1 viruses at the human-animal interface in Egypt. PLoS One 6, e17730.

    Article  Google Scholar 

  • Kitphati, R., Pooruk, P., Lerdsamran, H., Poosuwan, S., Louisirirotchanakul, S., Auewarakul, P., Chokphaibulkit, K., Noisumdaeng, P., Sawanpanyalert, P., and Puthavathana, P. 2009. Kinetics and longevity of antibody response to influenza A H5N1 virus infection in humans. Clin. Vaccine Immunol. 16, 978–981.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee, C.W., Senne, D.A., and Suarez, D.L. 2004. Effect of vaccine use in the evolution of Mexican lineage H5N2 avian influenza virus. J. Virol. 78, 8372–8381.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, K.S., Guan, Y., Wang, J., Smith, G.J., Xu, K.M., Duan, L., Rahardjo, A.P., Puthavathana, P., Buranathai, C., Nguyen, T.D., et al. 2004. Genesis of a highly pathogenic and potentially pandemic H5N1 influenza virus in eastern Asia. Nature 430, 209–213.

    Article  CAS  PubMed  Google Scholar 

  • Li, L.H., Yu, Z., Chen, W.S., Liu, S.L., Lu, Y., Zhang, Y.J., Chen, E.F., and Lin, J.F. 2013. Evidence for H5 avian influenza infection in Zhejiang province, China, 2010-2012: a cross-sectional study. J. Thorac. Dis. 5, 790–796.

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu, J., Xiao, H., Lei, F., Zhu, Q., Qin, K., Zhang, X.W., Zhang, X.L., Zhao, D., Wang, G., Feng, Y., et al. 2005. Highly pathogenic H5N1 influenza virus infection in migratory birds. Science 309, 1206.

    Article  CAS  PubMed  Google Scholar 

  • Naguib, M.M., Abdelwhab, E.M., and Harder, T.C. 2016. Evolutionary features of influenza A/H5N1 virus populations in Egypt: poultry and human health implications. Arch. Virol. 161, 1963–1967.

    Article  CAS  PubMed  Google Scholar 

  • Nasreen, S., Khan, S.U., Luby, S.P., Gurley, E.S., Abedin, J., Zaman, R.U., Sohel, B.M., Rahman, M., Hancock, K., Levine, M.Z., et al. 2015. Highly pathogenic Avian Influenza A(H5N1) virus infection among workers at live bird markets, Bangladesh, 2009–2010. Emerg. Infect. Dis. 21, 629–637.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nasreen, S., Uddin Khan, S., Azziz-Baumgartner, E., Hancock, K., Veguilla, V., Wang, D., Rahman, M., Alamgir, A.S., Sturm-Ramirez, K., Gurley, E.S., et al. 2013. Seroprevalence of antibodies against highly pathogenic avian influenza A (H5N1) virus among poultry workers in Bangladesh, 2009. PLoS One 8, e73200.

    Article  Google Scholar 

  • Njabo, K.Y., Zanontian, L., Sheta, B.N., Samy, A., Galal, S., Schoenberg, F.P., and Smith, T.B. 2016. Living with avian FLU–Persistence of the H5N1 highly pathogenic avian influenza virus in Egypt. Vet. Microbiol. 187, 82–92.

    Article  PubMed  Google Scholar 

  • Nolan, T.M., Richmond, P.C., Skeljo, M.V., Pearce, G., Hartel, G., Formica, N.T., Hoschler, K., Bennet, J., Ryan, D., Papanaoum, K., et al. 2008. Phase I and IIrandomised trials of the safety and immunogenicity of a prototype adjuvanted inactivated split-virus influenza A (H5N1) vaccine in healthy adults. Vaccine 26, 4160–4167.

    Article  CAS  PubMed  Google Scholar 

  • Okoye, J.O., Eze, D.C., Krueger, W.S., Heil, G.L., White, S.K., Merrill, H.R., and Gray, G.C. 2014. Evidence for subclinical H5N1 avian influenza infections among Nigerian poultry workers. J. Med. Virol. 86, 2070–2075.

    Article  PubMed  Google Scholar 

  • Pasick, J., Berhane, Y., Joseph, T., Bowes, V., Hisanaga, T., Handel, K., and Alexandersen, S. 2015. Reassortant highly pathogenic influenza A H5N2 virus containing gene segments related to Eurasian H5N8 in British Columbia, Canada, 2014. Sci. Rep. 5, 9484.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reed, C., Bruden, D., Byrd, K.K., Veguilla, V., Bruce, M., Hurlburt, D., Wang, D., Holiday, C., Hancock, K., Ortiz, J.R., et al. 2014. Characterizing wild bird contact and seropositivity to highly pathogenic avian influenza A (H5N1) virus in Alaskan residents. Influenza Other Respir. Viruses 8, 516–523.

    Article  PubMed  PubMed Central  Google Scholar 

  • Reid, S.M., Shell, W.M., Barboi, G., Onita, I., Turcitu, M., Cioranu, R., Marinova-Petkova, A., Goujgoulova, G., Webby, R.J., Webster, R.G., et al. 2011. First reported incursion of highly pathogenic notifiable avian influenza A H5N1 viruses from clade 2.3.2 into European poultry. Transbound Emerg. Dis. 58, 76–78.

    Article  CAS  PubMed  Google Scholar 

  • Saad, M.D., Ahmed, L.S., Gamal-Eldein, M.A., Fouda, M.K., Khalil, F., Yingst, S.L., Parker, M.A., and Montevillel, M.R. 2007. Possible avian influenza (H5N1) from migratory bird, Egypt. Emerg. Infect. Dis. 13, 1120–1121.

    Article  PubMed  PubMed Central  Google Scholar 

  • Salzberg, S.L., Kingsford, C., Cattoli, G., Spiro, D.J., Janies, D.A., Aly, M.M., Brown, I.H., Couacy-Hymann, E., de Mia, G.M., Dung do, H., et al. 2007. Genome analysis linking recent European and African influenza (H5N1) viruses. Emerg. Infect. Dis. 13, 713–718.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith, G.J. and Donis, R.O. 2015. Nomenclature updates resulting from the evolution of avian influenza A(H5) virus clades 2.1.3.2a, 2.2.1, and 2.3.4 during 2013-2014. Influenza Other Respir. Viruses 9, 271–276.

    Article  PubMed  PubMed Central  Google Scholar 

  • Toner, E.S., Adalja, A.A., Nuzzo, J.B., Inglesby, T.V., Henderson, D.A., and Burke, D.S. 2013. Assessment of serosurveys for H5N1. Clin. Infect. Dis. 56, 1206–1212.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ungchusak, K., Auewarakul, P., Dowell, S.F., Kitphati, R., Auwanit, W., Puthavathana, P., Uiprasertkul, M., Boonnak, K., Pittayawonganon, C., Cox, N.J., et al. 2005. Probable person-to-person transmission of avian influenza A (H5N1). N. Engl. J. Med. 352, 333–340.

    Article  CAS  PubMed  Google Scholar 

  • van Kerkhove, M.D. 2013. Brief literature review for the WHO global influenza research agenda–highly pathogenic avian influenza H5N1 risk in humans. Influenza Other Respir. Viruses 7 Suppl 2, 26–33.

    Article  Google Scholar 

  • Wang, H., Feng, Z., Shu, Y., Yu, H., Zhou, L., Zu, R., Huai, Y., Dong, J., Bao, C., Wen, L., et al. 2008. Probable limited person-to-person transmission of highly pathogenic avian influenza A (H5N1) virus in China. Lancet 371, 1427–1434.

    Article  PubMed  Google Scholar 

  • Wang, T.T., Parides, M.K., and Palese, P. 2012. Seroevidence for H5N1 influenza infections in humans: meta-analysis. Science 335, 1463.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watanabe, Y., Ibrahim, M.S., Ellakany, H.F., Kawashita, N., Daidoji, T., Takagi, T., Yasunaga, T., Nakaya, T., and Ikuta, K. 2012. Antigenic analysis of highly pathogenic avian influenza virus H5N1 sublineages co-circulating in Egypt. J. Gen. Virol. 93, 2215–2226.

    Article  CAS  PubMed  Google Scholar 

  • Webby, R.J., Perez, D.R., Coleman, J.S., Guan, Y., Knight, J.H., Govorkova, E.A., McClain-Moss, L.R., Peiris, J.S., Rehg, J.E., Tuomanen, E.I., et al. 2004. Responsiveness to a pandemic alert: use of reverse genetics for rapid development of influenza vaccines. Lancet 363, 1099–1103.

    Article  CAS  PubMed  Google Scholar 

  • Webster, R.G. and Govorkova, E.A. 2006. H5N1 influenza–continuing evolution and spread. N. Engl. J. Med. 355, 2174–2177.

    Article  CAS  PubMed  Google Scholar 

  • Webster, R.G., Peiris, M., Chen, H., and Guan, Y. 2006. H5N1 outbreaks and enzootic influenza. Emerg. Infect. Dis. 12, 3–8.

    Article  PubMed  PubMed Central  Google Scholar 

  • WHO. 2005. Evolution of H5N1 avian influenza viruses in Asia. Emerg. Infect. Dis. 11, 1515–1521.

    Google Scholar 

  • WHO. 2006. Avian influenza–situation in Indonesia–update 16.

  • WHO. 2017. Cumulative number of confirmed human cases of avian influenza A(H5N1) reported to WHO. World Health Organization, 2017.

  • WHO/EMRO. 2016. Avian Influenza A(H5N1) Situation Update. In World Health Organization, E.M.R.O. (ed.). World Health Organization, Eastern Mediterranean Regional Office, Egypt.

  • WHO/OIE/FAO. 2012. Continued evolution of highly pathogenic avian influenza A (H5N1): updated nomenclature. Influenza Other Respir. Viruses 6, 1–5.

  • WHO/OIE/FAO. 2014. Revised and updated nomenclature for highly pathogenic avian influenza A (H5N1) viruses. Influenza Other Respir. Viruses 8, 384–388.

    Article  Google Scholar 

  • Yang, P., Ma, C., Shi, W., Cui, S., Lu, G., Peng, X., Zhang, D., Liu, Y., Liang, H., Zhang, Y., et al. 2012. A serological survey of antibodies to H5, H7 and H9 avian influenza viruses amongst the duck-related workers in Beijing, China. PLoS One 7, e50770.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Richard J. Webby.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Harfoot, R., Webby, R.J. H5 influenza, a global update. J Microbiol. 55, 196–203 (2017). https://doi.org/10.1007/s12275-017-7062-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-017-7062-7

Keywords

Navigation