1887

Abstract

Influenza epidemics are a major health concern worldwide. Highly pathogenic avian influenza (HPAI) H5N1 viruses in Egypt have been subject to rapid genetic and antigenic changes since the first outbreak in February 2006 and have been endemic in poultry in Egypt since 2008. In this study, 33 H5N1 viruses isolated from avian hosts were antigenically analysed by using a panel of eight mAbs raised against the A/Viet Nam/1203/04 (H5N1; clade 1) and A/bar-headed goose/Qinghai-lake/1A/05 (H5N1; clade 2.2) influenza viruses. Rats were immunized with inactivated whole-virus vaccine produced by reverse genetics with the haemagglutinin and neuraminidase genes of eight antigenically different HPAI H5N1 virus isolates and six internal genes from A/Puerto Rico/8/1934 (PR8) to produce polyclonal antibodies. Cross-reactivity between the obtained polyclonal antibodies and the isolated viruses was assayed. Antigenic cartography of the isolated viruses showed that three antigenic clusters were defined based on haemagglutination inhibition (HI) analysis using mAbs and the majority of viruses isolated in 2010 and 2011 fell into two of these clusters. An antigenic map based on polyclonal rat antisera showed that all virus isolates fell within one extended cluster. Accordingly, continuous surveillance and antigenic characterization will help us determine which virus isolate(s) should be used in poultry vaccine preparation.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.043299-0
2012-12-01
2019-12-14
Loading full text...

Full text loading...

/deliver/fulltext/jgv/93/12/2564.html?itemId=/content/journal/jgv/10.1099/vir.0.043299-0&mimeType=html&fmt=ahah

References

  1. Abdel-Moneim A. S. , Shany S. A. , Fereidouni S. R. , Eid B. T. , el-Kady M. F. , Starick E. , Harder T. , Keil G. M. . ( 2009; ). Sequence diversity of the haemagglutinin open reading frame of recent highly pathogenic avian influenza H5N1 isolates from Egypt. . Arch Virol 154:, 1559–1562.[PubMed] [CrossRef]
    [Google Scholar]
  2. Abdelwhab E. M. , Hafez H. M. . ( 2011; ). An overview of the epidemic of highly pathogenic H5N1 avian influenza virus in Egypt: epidemiology and control challenges. . Epidemiol Infect 139:, 647–657.[PubMed] [CrossRef]
    [Google Scholar]
  3. Abdelwhab S. M. , Arafa A. S. , Erfan A. M. , Aly M. M. , Hafez H. M. . ( 2010a; ). Modified H5 real-time reverse transcriptase-PCR oligonucleotides for detection of divergent avian influenza H5N1 viruses in Egypt. . Avian Dis 54:, 1301–1305.[PubMed] [CrossRef]
    [Google Scholar]
  4. Abdelwhab S. M. , Erfan A. M. , Grund C. , Ziller M. , Arafa A. S. , Beer M. , Aly M. M. , Hafez H. M. , Harder T. C. . ( 2010b; ). Simultaneous detection and differentiation by multiplex real time RT-PCR of highly pathogenic avian influenza subtype H5N1 classic (clade 2.2.1 proper) and escape mutant (clade 2.2.1 variant) lineages in Egypt. . Virol J 7:, 260.[PubMed] [CrossRef]
    [Google Scholar]
  5. Abdelwhab E. M. , Grund C. , Aly M. M. , Beer M. , Harder T. C. , Hafez H. M. . ( 2012; ). Influence of maternal immunity on vaccine efficacy and susceptibility of one day old chicks against Egyptian highly pathogenic avian influenza H5N1. . Vet Microbiol 155:, 13–20.[PubMed] [CrossRef]
    [Google Scholar]
  6. Aly M. M. , Arafa A. , Hassan M. K. . ( 2008; ). Epidemiological findings of outbreaks of disease caused by highly pathogenic H5N1 avian influenza virus in poultry in Egypt during 2006. . Avian Dis 52:, 269–277.[PubMed] [CrossRef]
    [Google Scholar]
  7. Arafa A. , Suarez D. L. , Hassan M. K. , Aly M. M. . ( 2010; ). Phylogenetic analysis of hemagglutinin and neuraminidase genes of highly pathogenic avian influenza H5N1 Egyptian strains isolated from 2006 to 2008 indicates heterogeneity with multiple distinct sublineages. . Avian Dis 54: (Suppl.), 345–349.[PubMed] [CrossRef]
    [Google Scholar]
  8. Balish A. L. , Davis C. T. , Saad M. D. , El-Sayed N. , Esmat H. , Tjaden J. A. , Earhart K. C. , Ahmed L. E. , Abd El-Halem M. . & other authors ( 2010; ). Antigenic and genetic diversity of highly pathogenic avian influenza A (H5N1) viruses isolated in Egypt. . Avian Dis 54: (Suppl.), 329–334.[PubMed] [CrossRef]
    [Google Scholar]
  9. Baras B. , Stittelaar K. J. , Simon J. H. , Thoolen R. J. , Mossman S. P. , Pistoor F. H. , van Amerongen G. , Wettendorff M. A. , Hanon E. , Osterhaus A. D. . ( 2008; ). Cross-protection against lethal H5N1 challenge in ferrets with an adjuvanted pandemic influenza vaccine. . PLoS ONE 3:, e1401.[PubMed] [CrossRef]
    [Google Scholar]
  10. Boon A. C. , Webby R. J. . ( 2009; ). Antigenic cross-reactivity among H5N1 viruses. . Curr Top Microbiol Immunol 333:, 25–40.[PubMed]
    [Google Scholar]
  11. Cai Z. , Zhang T. , Wan X. F. . ( 2010; ). A computational framework for influenza antigenic cartography. . PLOS Comput Biol 6:, e1000949.[PubMed] [CrossRef]
    [Google Scholar]
  12. Carrat F. , Flahault A. . ( 2007; ). Influenza vaccine: the challenge of antigenic drift. . Vaccine 25:, 6852–6862.[PubMed] [CrossRef]
    [Google Scholar]
  13. Cattoli G. , Fusaro A. , Monne I. , Coven F. , Joannis T. , El-Hamid H. S. , Hussein A. A. , Cornelius C. , Amarin N. M. . & other authors ( 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.[PubMed] [CrossRef]
    [Google Scholar]
  14. Chen H. , Smith G. J. , Li K. S. , Wang J. , Fan X. H. , Rayner J. M. , Vijaykrishna D. , Zhang J. X. , Zhang L. J. . & other authors ( 2006; ). Establishment of multiple sublineages of H5N1 influenza virus in Asia: implications for pandemic control. . Proc Natl Acad Sci U S A 103:, 2845–2850.[PubMed] [CrossRef]
    [Google Scholar]
  15. Chenna R. , Sugawara H. , Koike T. , Lopez R. , Gibson T. J. , Higgins D. G. , Thompson J. D. . ( 2003; ). Multiple sequence alignment with the clustal series of programs. . Nucleic Acids Res 31:, 3497–3500.[PubMed] [CrossRef]
    [Google Scholar]
  16. Claas E. C. , Osterhaus A. D. , van Beek R. , De Jong J. C. , Rimmelzwaan G. F. , Senne D. A. , Krauss S. , Shortridge K. F. , Webster R. G. . ( 1998; ). Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. . Lancet 351:, 472–477.[PubMed] [CrossRef]
    [Google Scholar]
  17. De Vriese J. , Steensels M. , Palya V. , Gardin Y. , Dorsey K. M. , Lambrecht B. , Van Borm S. , van den Berg T. . ( 2010; ). Passive protection afforded by maternally-derived antibodies in chickens and the antibodies’ interference with the protection elicited by avian influenza-inactivated vaccines in progeny. . Avian Dis 54: (Suppl.), 246–252.[PubMed] [CrossRef]
    [Google Scholar]
  18. Ducatez M. F. , Cai Z. , Peiris M. , Guan Y. , Ye Z. , Wan X. F. , Webby R. J. . ( 2011; ). Extent of antigenic cross-reactivity among highly pathogenic H5N1 influenza viruses. . J Clin Microbiol 49:, 3531–3536.[PubMed] [CrossRef]
    [Google Scholar]
  19. Eladl A. E. , El-Azm K. I. , Ismail A. E. , Ali A. , Saif Y. M. , Lee C. W. . ( 2011; ). Genetic characterization of highly pathogenic H5N1 avian influenza viruses isolated from poultry farms in Egypt. . Virus Genes 43:, 272–280.[PubMed] [CrossRef]
    [Google Scholar]
  20. Escorcia M. , Vázquez L. , Méndez S. T. , Rodríguez-Ropón A. , Lucio E. , Nava G. M. . ( 2008; ). Avian influenza: genetic evolution under vaccination pressure. . Virol J 5:, 15.[PubMed] [CrossRef]
    [Google Scholar]
  21. Govorkova E. A. , Webby R. J. , Humberd J. , Seiler J. P. , Webster R. G. . ( 2006; ). Immunization with reverse-genetics-produced H5N1 influenza vaccine protects ferrets against homologous and heterologous challenge. . J Infect Dis 194:, 159–167.[PubMed] [CrossRef]
    [Google Scholar]
  22. Grund C. , Abdelwhab S. M. , Arafa A. S. , Ziller M. , Hassan M. K. , Aly M. M. , Hafez H. M. , Harder T. C. , Beer M. . ( 2011; ). Highly pathogenic avian influenza virus H5N1 from Egypt escapes vaccine-induced immunity but confers clinical protection against a heterologous clade 2.2.1 Egyptian isolate. . Vaccine 29:, 5567–5573.[PubMed] [CrossRef]
    [Google Scholar]
  23. 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. . & other authors ( 2004; ). H5N1 influenza: a protean pandemic threat. . Proc Natl Acad Sci U S A 101:, 8156–8161.[PubMed] [CrossRef]
    [Google Scholar]
  24. Hafez M. H. , Arafa A. , Abdelwhab E. M. , Selim A. , Khoulosy S. G. , Hassan M. K. , Aly M. M. . ( 2010; ). Avian influenza H5N1 virus infections in vaccinated commercial and backyard poultry in Egypt. . Poult Sci 89:, 1609–1613.[PubMed] [CrossRef]
    [Google Scholar]
  25. Hall T. A. . ( 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]
  26. Hanson B. J. , Boon A. C. , Lim A. P. , Webb A. , Ooi E. E. , Webby R. J. . ( 2006; ). Passive immunoprophylaxis and therapy with humanized monoclonal antibody specific for influenza A H5 hemagglutinin in mice. . Respir Res 7:, 126.[PubMed] [CrossRef]
    [Google Scholar]
  27. Hassan M. K. , Kilany W. H. , Abdelwhab E. M. , Arafa A. S. , Selim A. , Samy A. , Samir M. , Le Brun Y. , Jobre Y. , Aly M. M. . ( 2012; ). Distribution of avian influenza H5N1 viral RNA in tissues of AI-vaccinated and unvaccinated contact chickens after experimental infection. . Arch Virol 157:, 951–959.[PubMed] [CrossRef]
    [Google Scholar]
  28. Kaverin N. V. , Rudneva I. A. , Govorkova E. A. , Timofeeva T. A. , Shilov A. A. , Kochergin-Nikitsky K. S. , Krylov P. S. , Webster R. G. . ( 2007; ). Epitope mapping of the hemagglutinin molecule of a highly pathogenic H5N1 influenza virus by using monoclonal antibodies. . J Virol 81:, 12911–12917.[PubMed] [CrossRef]
    [Google Scholar]
  29. Kayali G. , El-Shesheny R. , Kutkat M. A. , Kandeil A. M. , Mostafa A. , Ducatez M. F. , McKenzie P. P. , Govorkova E. A. , Nasraa M. H. . & other authors ( 2011a; ). Continuing threat of influenza (H5N1) virus circulation in Egypt. . Emerg Infect Dis 17:, 2306–2308.[PubMed] [CrossRef]
    [Google Scholar]
  30. Kayali G. , Webby R. J. , Ducatez M. F. , El Shesheny R. A. , Kandeil A. M. , Govorkova E. A. , Mostafa A. , Ali M. A. . ( 2011b; ). The epidemiological and molecular aspects of influenza H5N1 viruses at the human-animal interface in Egypt. . PLoS ONE 6:, e17730.[PubMed] [CrossRef]
    [Google Scholar]
  31. Kim J. K. , Kayali G. , Walker D. , Forrest H. L. , Ellebedy A. H. , Griffin Y. S. , Rubrum A. , Bahgat M. M. , Kutkat M. A. . & other authors ( 2010; ). Puzzling inefficiency of H5N1 influenza vaccines in Egyptian poultry. . Proc Natl Acad Sci U S A 107:, 11044–11049.[PubMed] [CrossRef]
    [Google Scholar]
  32. Lee C. W. , Senne D. A. , Suarez D. L. . ( 2004; ). Effect of vaccine use in the evolution of Mexican lineage H5N2 avian influenza virus. . J Virol 78:, 8372–8381.[PubMed] [CrossRef]
    [Google Scholar]
  33. Peyre M. , Samaha H. , Makonnen Y. J. , Saad A. , Abd-Elnabi A. , Galal S. , Ettel T. , Dauphin G. , Lubroth J. . & other authors ( 2009; ). Avian influenza vaccination in Egypt: limitations of the current strategy. . J Mol Genet Med 3:, 198–204.[PubMed]
    [Google Scholar]
  34. Plotkin J. B. , Dushoff J. . ( 2003; ). Codon bias and frequency-dependent selection on the hemagglutinin epitopes of influenza A virus. . Proc Natl Acad Sci U S A 100:, 7152–7157.[PubMed] [CrossRef]
    [Google Scholar]
  35. Rauw F. , Palya V. , Van Borm S. , Welby S. , Tatar-Kis T. , Gardin Y. , Dorsey K. M. , Aly M. M. , Hassan M. K. . & other authors ( 2011; ). Further evidence of antigenic drift and protective efficacy afforded by a recombinant HVT-H5 vaccine against challenge with two antigenically divergent Egyptian clade 2.2.1 HPAI H5N1 strains. . Vaccine 29:, 2590–2600.[PubMed] [CrossRef]
    [Google Scholar]
  36. Saad M. D. , Ahmed L. S. , Gamal-Eldein M. A. , Fouda M. K. , Khalil F. , Yingst S. L. , Parker M. A. , Montevillel M. R. . ( 2007; ). Possible avian influenza (H5N1) from migratory bird, Egypt. . Emerg Infect Dis 13:, 1120–1121.[PubMed] [CrossRef]
    [Google Scholar]
  37. Swayne D. E. . ( 2006; ). Recommendations from the avian influenza vaccine workshop. . Ann N Y Acad Sci 1081:, 226–227.[PubMed] [CrossRef]
    [Google Scholar]
  38. Swayne D. E. . ( 2009; ). Avian influenza vaccines and therapies for poultry. . Comp Immunol Microbiol Infect Dis 32:, 351–363.[PubMed] [CrossRef]
    [Google Scholar]
  39. Swayne D. E. , Kapczynski D. . ( 2008; ). Strategies and challenges for eliciting immunity against avian influenza virus in birds. . Immunol Rev 225:, 314–331.[PubMed] [CrossRef]
    [Google Scholar]
  40. Tamura K. , Dudley J. , Nei M. , Kumar S. . ( 2007; ). mega4: Molecular Evolutionary Genetics Analysis (mega) software version 4.0. . Mol Biol Evol 24:, 1596–1599.[PubMed] [CrossRef]
    [Google Scholar]
  41. Wang H. , Jiang C. . ( 2009; ). Avian influenza H5N1: an update on molecular pathogenesis. Sci China Series C . . Life Sci 52:, 459–463.[CrossRef]
    [Google Scholar]
  42. Watanabe Y. , Ibrahim M. S. , Ellakany H. F. , Kawashita N. , Mizuike R. , Hiramatsu H. , Sriwilaijaroen N. , Takagi T. , Suzuki Y. , Ikuta K. . ( 2011; ). Acquisition of human-type receptor binding specificity by new H5N1 influenza virus sublineages during their emergence in birds in Egypt. . PLoS Pathog 7:, e1002068.[PubMed] [CrossRef]
    [Google Scholar]
  43. Watanabe Y. , Ibrahim M. S. , Ellakany H. F. , Kawashita N. , Daidoji T. , Takagi T. , Yasunaga T. , Nakaya T. , Ikuta K. . ( 2012; ). Antigenic analysis of highly pathogenic avian influenza virus H5N1 sublineages co-circulating in Egypt. . J Gen Virol 93:, 2215–2226.[PubMed] [CrossRef]
    [Google Scholar]
  44. 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. . & other authors ( 2004; ). Responsiveness to a pandemic alert: use of reverse genetics for rapid development of influenza vaccines. . Lancet 363:, 1099–1103.[PubMed] [CrossRef]
    [Google Scholar]
  45. Webster R. G. . ( 2002; ). The importance of animal influenza for human disease. . Vaccine 20: (Suppl. 2), S16–S20.[PubMed] [CrossRef]
    [Google Scholar]
  46. Webster R. G. , Bean W. J. , Gorman O. T. , Chambers T. M. , Kawaoka Y. . ( 1992; ). Evolution and ecology of influenza A viruses. . Microbiol Rev 56:, 152–179.[PubMed]
    [Google Scholar]
  47. WHO ( 2002; ). WHO Manual on Animal Influenza Diagnosis and Surveillance, 2nd edn. Geneva, Switzerland:: World Health Organization;.
    [Google Scholar]
  48. WHO ( 2009; ). WHO Information for Laboratory Diagnosis of New Influenza A (H1N1) Virus in Humans, 21 May 2009. . Geneva, Switzerland:: World Health Organization;.
  49. WHO/OIE/FAO ( 2009; ). Continuing progress towards a unified nomenclature for the highly pathogenic H5N1 avian influenza viruses: divergence of clade 2.2 viruses. . Influenza Other Respir Viruses 3, 59–62.[CrossRef]
    [Google Scholar]
  50. WHO/OIE/FAO ( 2012; ). Continued evolution of highly pathogenic avian influenza A (H5N1): Updated nomenclature. . Influenza Other Respir Viruses 6, 1–5.[CrossRef]
    [Google Scholar]
  51. Wiley D. C. , Wilson I. A. , Skehel J. J. . ( 1981; ). Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. . Nature 289:, 373–378.[PubMed] [CrossRef]
    [Google Scholar]
  52. Wilson I. A. , Cox N. J. . ( 1990; ). Structural basis of immune recognition of influenza virus hemagglutinin. . Annu Rev Immunol 8:, 737–771.[PubMed] [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.043299-0
Loading
/content/journal/jgv/10.1099/vir.0.043299-0
Loading

Data & Media loading...

Supplements

Supplementary table 

PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error