1887

Abstract

Highly pathogenic avian influenza viruses (HPAIVs) of subtype H5N1 have continued to perpetuate with divergent genetic variants in poultry within Asia since 2003. Further dissemination of Asian-derived H5 HPAIVs to Europe, Africa and, most recently, to the North American continent has occurred. We report an outbreak of HPAIV H5N1 among falcons kept for hunting and other wild bird species bred as falcon prey in Dubai, United Arab Emirates, during the autumn of 2014. The causative agent was identified as avian influenza virus subtype H5N1, clade 2.3.2.1c, by genetic and phylogenetic analyses. High mortality in infected birds was in accordance with systemic pathomorphological and histological alterations in affected falcons. Genetic analysis showed the HPAIV H5N1 of clade 2.3.2.1c is a reassortant in which the PB2 segment was derived from an Asian-origin H9N2 virus lineage. The Dubai H5N1 viruses were closely related to contemporary H5N1 HPAIVs from Nigeria, Burkina-Faso, Romania and Bulgaria. Median-joining network analysis of 2.3.2.1c viruses revealed that the Dubai outbreak was an episode of a westward spread of these viruses on a larger scale from unidentified Asian sources. The incursion into Dubai, possibly via infected captive hunting falcons returning from hunting trips to central Asian countries, preceded outbreaks in Nigeria and other West African countries. The alarmingly enhanced geographical mobility of clade 2.3.2.1.c and clade 2.3.4.4 viruses may represent another wave of transcontinental dissemination of Asian-origin HPAIV H5 viruses, such as the outbreak at Qinghai Lake caused by clade 2.2 (‘Qinghai’ lineage) in 2005.

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2015-11-01
2024-12-05
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References

  1. Aamir U.B., Wernery U., Ilyushina N., Webster R.G. 2007; Characterization of avian H9N2 influenza viruses from United Arab Emirates 2000 to 2003. Virology 361:45–55 [View Article][PubMed]
    [Google Scholar]
  2. Alders R., Awuni J.A., Bagnol B., Farrell P., de Haan N. 2014; Impact of avian influenza on village poultry production globally. EcoHealth 11:63–72[PubMed]
    [Google Scholar]
  3. Arafa A.S., Naguib M.M., Luttermann C., Selim A.A., Kilany W.H., Hagag N., Samy A., Abdelhalim A., Hassan M.K., other authors. 2015; Emergence of a novel cluster of influenza A(H5N1) virus clade 2.2.1.2 with putative human health impact in Egypt, 2014/15. Euro Surveill 20:2–8[PubMed] [CrossRef]
    [Google Scholar]
  4. Bandelt H.J., Forster P., Röhl A. 1999; Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48 [View Article][PubMed]
    [Google Scholar]
  5. Bertran K., Busquets N., Abad F.X., García de la Fuente J., Solanes D., Cordón I., Costa T., Dolz R., Majó N. 2012; Highly (H5N1) and low (H7N2) pathogenic avian influenza virus infection in falcons via nasochoanal route and ingestion of experimentally infected prey. PLoS One 7:e32107 [View Article][PubMed]
    [Google Scholar]
  6. Biasini M., Bienert S., Waterhouse A., Arnold K., Studer G., Schmidt T., Kiefer F., Cassarino T.G., Bertoni M., other authors. 2014; SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res 42:W252–W258 [View Article][PubMed]
    [Google Scholar]
  7. Chen H., Smith G.J., Zhang S.Y., Qin K., Wang J., Li K.S., Webster R.G., Peiris J.S., Guan Y. 2005; Avian flu: H5N1 virus outbreak in migratory waterfowl. Nature 436:191–192 [View Article][PubMed]
    [Google Scholar]
  8. Chmielewski R., Swayne D.E. 2011; Avian influenza: public health and food safety concerns. Annu Rev Food Sci Technol 2:37–57 [View Article][PubMed]
    [Google Scholar]
  9. Donis R.O., Smith G.J., World Health Organization/World Organisation for Animal H.F., Agriculture Organization H.E.W.G. 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 Resp Viruses 212:183–194
    [Google Scholar]
  10. Fan S., Deng G., Song J., Tian G., Suo Y., Jiang Y., Guan Y., Bu Z., Kawaoka Y., Chen H. 2009; Two amino acid residues in the matrix protein M1 contribute to the virulence difference of H5N1 avian influenza viruses in mice. Virology 384:28–32 [View Article][PubMed]
    [Google Scholar]
  11. Fereidouni S.R., Harder T.C., Gaidet N., Ziller M., Hoffmann B., Hammoumi S., Globig A., Starick E. 2012; Saving resources: avian influenza surveillance using pooled swab samples and reduced reaction volumes in real-time RT-PCR. J Virol Methods 186:119–125 [View Article][PubMed]
    [Google Scholar]
  12. Gall A., Hoffmann B., Harder T., Grund C., Ehricht R., Beer M. 2009; Rapid and highly sensitive neuraminidase subtyping of avian influenza viruses by use of a diagnostic DNA microarray. J Clin Microbiol 47:2985–2988 [View Article][PubMed]
    [Google Scholar]
  13. Gupta R., Brunak S. 2002; Prediction of glycosylation across the human proteome and the correlation to protein function. In Proceedings of Pacific Symposium on Biocomputing 2002 vol. 7 pp. 310–322 River Edge, NJ: World Scientific;
    [Google Scholar]
  14. Hall T. 1999; BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
    [Google Scholar]
  15. He S., Shi J., Qi X., Huang G., Chen H., Lu C. 2015; Lethal infection by a novel reassortant H5N1 avian influenza A virus in a zoo-housed tiger. Microbes Infect 17:54–61 [View Article][PubMed]
    [Google Scholar]
  16. Höper D., Hoffmann B., Beer M. 2009; Simple, sensitive, and swift sequencing of complete H5N1 avian influenza virus genomes. J Clin Microbiol 47:674–679 [View Article][PubMed]
    [Google Scholar]
  17. Ip H.S., Torchetti M.K., Crespo R., Kohrs P., DeBruyn P., Mansfield K.G., Baszler T., Badcoe L., Bodenstein B., other authors. 2015; Novel Eurasian highly pathogenic avian influenza A H5 viruses in wild birds, Washington, USA, 2014. Emerg Infect Dis 21:886–890 [View Article][PubMed]
    [Google Scholar]
  18. Jiao P., Tian G., Li Y., Deng G., Jiang Y., Liu C., Liu W., Bu Z., Kawaoka Y., Chen H. 2008; A single-amino-acid substitution in the NS1 protein changes the pathogenicity of H5N1 avian influenza viruses in mice. J Virol 82:1146–1154 [View Article][PubMed]
    [Google Scholar]
  19. Jonges M., Bataille A., Enserink R., Meijer A., Fouchier R.A., Stegeman A., Koch G., Koopmans M. 2011; Comparative analysis of avian influenza virus diversity in poultry and humans during a highly pathogenic avian influenza A (H7N7) virus outbreak. J Virol 85:10598–10604 [View Article][PubMed]
    [Google Scholar]
  20. Katoh K., Standley D.M. 2013; MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780 [View Article][PubMed]
    [Google Scholar]
  21. Khan O.A., Shuaib M.A., Rhman S.S., Ismail M.M., Hammad Y.A., Baky M.H., Fusaro A., Salviato A., Cattoli G. 2009; Isolation and identification of highly pathogenic avian influenza H5N1 virus from houbara bustards (Chlamydotis undulata macqueenii) and contact falcons. Avian Pathol 38:35–39 [View Article][PubMed]
    [Google Scholar]
  22. Kim J.H., Hatta M., Watanabe S., Neumann G., Watanabe T., Kawaoka Y. 2010; Role of host-specific amino acids in the pathogenicity of avian H5N1 influenza viruses in mice. J Gen Virol 91:1284–1289 [View Article][PubMed]
    [Google Scholar]
  23. Kohls A., Hafez H.M., Harder T., Jansen A., Lierz P., Lüschow D., Schweiger B., Lierz M. 2011; Avian influenza virus risk assessment in falconry. Virol J 8:187 [View Article][PubMed]
    [Google Scholar]
  24. Kwon H.I., Song M.S., Pascua P.N., Baek Y.H., Lee J.H., Hong S.P., Rho J.B., Kim J.K., Poo H., other authors. 2011; Genetic characterization and pathogenicity assessment of highly pathogenic H5N1 avian influenza viruses isolated from migratory wild birds in 2011, South Korea. Virus Res 160:305–315 [View Article][PubMed]
    [Google Scholar]
  25. Lee E.K., Kang H.M., Kim K.I., Choi J.G., To T.L., Nguyen T.D., Song B.M., Jeong J., Choi K.S., other authors. 2015; Genetic evolution of H5 highly pathogenic avian influenza virus in domestic poultry in Vietnam between 2011 and 2013. Poult Sci 94:650–661 [View Article][PubMed]
    [Google Scholar]
  26. Li J., Ishaq M., Prudence M., Xi X., Hu T., Liu Q., Guo D. 2009; Single mutation at the amino acid position 627 of PB2 that leads to increased virulence of an H5N1 avian influenza virus during adaptation in mice can be compensated by multiple mutations at other sites of PB2. Virus Res 144:123–129 [View Article][PubMed]
    [Google Scholar]
  27. Lierz M., Hafez H.M., Klopfleisch R., Lüschow D., Prusas C., Teifke J.P., Rudolf M., Grund C., Kalthoff D., other authors. 2007; Protection and virus shedding of falcons vaccinated against highly pathogenic avian influenza A virus (H5N1). Emerg Infect Dis 13:1667–1674 [View Article][PubMed]
    [Google Scholar]
  28. Liu H.L., Lv Y., Zheng D.X., Zhao Y.L., Sun C.Y., Zhang W., Li J.M., Wang Z.L. 2010; [Detection of molecular markers of amantadine resistance in avian influenza viruses by pyrosequencing]. Bing Du Xue Bao 26:392–395 (in Chinese) [PubMed]
    [Google Scholar]
  29. Marjuki H., Wernery U., Yen H.L., Franks J., Seiler P., Walker D., Krauss S., Webster R.G. 2009; Isolation of highly pathogenic avian influenza H5N1 virus from saker falcons (Falco cherrug) in the Middle East. Adv Virol 2009:1–7 [View Article][PubMed]
    [Google Scholar]
  30. Minh B.Q., Nguyen M.A., von Haeseler A. 2013; Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol 30:1188–1195 [View Article][PubMed]
    [Google Scholar]
  31. Monne I., Meseko C., Joannis T., Shittu I., Ahmed M., Tassoni L., Fusaro A., Cattoli G. 2015; Highly pathogenic avian influenza A(H5N1) virus in poultry, Nigeria, 2015. Emerg Infect Dis 21:1275–1277 [View Article][PubMed]
    [Google Scholar]
  32. Nakajima S., Nakajima K., Nobusawa E., Zhao J., Tanaka S., Fukuzawa K. 2007; Comparison of epitope structures of H3HAs through protein modeling of influenza A virus hemagglutinin: mechanism for selection of antigenic variants in the presence of a monoclonal antibody. Microbiol Immunol 51:1179–1187 [View Article][PubMed]
    [Google Scholar]
  33. Nguyen L.T., Schmidt H.A., von Haeseler A., Minh B.Q. 2015; IQ-TREE: a fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Mol Biol Evol 32:268–274 [View Article]
    [Google Scholar]
  34. OIE 2015 Update on Highly Pathogenic Avian Influenza in Animals (Type H5 and H7) http://www.oie.int/animal-health-in-the-world/update-on-avian-influenza/2015/
    [Google Scholar]
  35. Pabbaraju K., Tellier R., Wong S., Li Y., Bastien N., Tang J.W., Drews S.J., Jang Y., Davis C.T., other authors. 2014; Full-genome analysis of avian influenza A(H5N1) virus from a human, North America, 2013. Emerg Infect Dis 20:887–891 [View Article][PubMed]
    [Google Scholar]
  36. Reid S.M., Shell W.M., Barboi G., Onita I., Turcitu M., Cioranu R., Marinova-Petkova A., Goujgoulova G., Webby R.J., other authors. 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 [View Article][PubMed]
    [Google Scholar]
  37. Seo S.H., Hoffmann E., Webster R.G. 2002; Lethal H5N1 influenza viruses escape host anti-viral cytokine responses. Nat Med 8:950–954 [View Article][PubMed]
    [Google Scholar]
  38. Spesock A., Malur M., Hossain M.J., Chen L.M., Njaa B.L., Davis C.T., Lipatov A.S., York I.A., Krug R.M., Donis R.O. 2011; The virulence of 1997 H5N1 influenza viruses in the mouse model is increased by correcting a defect in their NS1 proteins. J Virol 85:7048–7058 [View Article][PubMed]
    [Google Scholar]
  39. Su Y., Yang H.Y., Zhang B.J., Jia H.L., Tien P. 2008; Analysis of a point mutation in H5N1 avian influenza virus hemagglutinin in relation to virus entry into live mammalian cells. Arch Virol 153:2253–2261 [View Article][PubMed]
    [Google Scholar]
  40. Suguitan A.L. Jr, Matsuoka Y., Lau Y.F., Santos C.P., Vogel L., Cheng L.I., Orandle M., Subbarao K. 2012; The multibasic cleavage site of the hemagglutinin of highly pathogenic A/Vietnam/1203/2004 (H5N1) avian influenza virus acts as a virulence factor in a host-specific manner in mammals. J Virol 86:2706–2714 [View Article][PubMed]
    [Google Scholar]
  41. University of Minnesota 2015 Impact of Poultry and Egg Production Losses and Poultry Processing Losses due to the Avian Influenza http://www.extension.umn.edu/community/economic-impact-analysis/reports/docs/2015-impact-of-poultry-production-losses-due-to-avian-infuenza.pdf
    [Google Scholar]
  42. Wang W., Lu B., Zhou H., Suguitan A.L. Jr, Cheng X., Subbarao K., Kemble G., Jin H. 2010; Glycosylation at 158N of the hemagglutinin protein and receptor binding specificity synergistically affect the antigenicity and immunogenicity of a live attenuated H5N1 A/Vietnam/1203/2004 vaccine virus in ferrets. J Virol 84:6570–6577 [View Article][PubMed]
    [Google Scholar]
  43. Webster R., Hulse D. 2005; Controlling avian flu at the source. Nature 435:415–416 [View Article][PubMed]
    [Google Scholar]
  44. Wernery U., Shanmuganatham K.K., Krylov P.S., Joseph S., Friedman K., Krauss S., Webster R.G. 2013; H9N2 influenza viruses from birds used in falconry. Influenza Other Resp Viruses 7:1241–1245 [View Article][PubMed]
    [Google Scholar]
  45. WHO/OIE/FAO H5N1 Evolution Working Group 2012; Continued evolution of highly pathogenic avian influenza A (H5N1): updated nomenclature. Influenza Other Respi Viruses 6:1–5 [View Article][PubMed]
    [Google Scholar]
  46. Yang Z.Y., Wei C.J., Kong W.P., Wu L., Xu L., Smith D.F., Nabel G.J. 2007; Immunization by avian H5 influenza hemagglutinin mutants with altered receptor binding specificity. Science 317:825–828 [View Article][PubMed]
    [Google Scholar]
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