1887

Abstract

The endemicity of avian influenza viruses (AIVs) among Egyptian poultry represents a public health risk. Co-circulation of low pathogenic AIV H9N2 subtype with highly pathogenic AIV H5N1 subtype in Egyptian farms provides a possibility to generate novel reassortant viruses. Here, the genetic characteristics of surface glycoproteins of 59 Egyptian H9N2 viruses, isolated between 2013 and 2015, were analysed. To elucidate the potential of genetic reassortment, 10 H9N2 isolates were selected based on different avian hosts (chickens, ducks, pigeons and quails) and phylogenetic analyses of their full genome sequences were conducted. Additionally, we performed antigenic analysis to further investigate the antigenic evolution of H9N2 viruses isolated during 2011–2015. Different viral characteristics including receptor-binding affinity and drug resistance of representative Egyptian H9N2 viruses were further investigated. The surface glycoproteins of current Egyptian H9N2 viruses were closely related to viruses of the G1-like lineage isolated from Egypt. Several genetic markers that enhance virulence in poultry and transmission to humans were detected. Analysis of the full genome of 10 H9N2 isolates indicated that two pigeon isolates inherited five internal genes from Eurasian AIVs circulating in wild birds. Antigenic conservation of different Egyptian H9N2 isolates from chickens, pigeons and ducks was observed, whereas quail isolates showed antigenic drift. The Egyptian H9N2 viruses preferentially bound to the human-like receptor rather than to the avian-like receptor. Our results suggest that the endemic H9N2 viruses in Egypt contain elements that may favour avian-to-human transmission and thus represent a public health risk.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000657
2017-04-01
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/jgv/98/4/548.html?itemId=/content/journal/jgv/10.1099/jgv.0.000657&mimeType=html&fmt=ahah

References

  1. Naeem K, Ullah A, Manvell RJ, Alexander DJ. Avian influenza A subtype H9N2 in poultry in Pakistan. Vet Rec 1999; 145:560 [View Article][PubMed]
    [Google Scholar]
  2. Wu H, Peng X, Peng X, Cheng L, Lu X et al. Genetic and molecular characterization of H9N2 and H5 avian influenza viruses from live poultry markets in Zhejiang Province, eastern China. Sci Rep 2015; 5:17508 [View Article][PubMed]
    [Google Scholar]
  3. Guo YJ, Wen LY, Zhang Y, Wan M, Guo JF et al. [Do pigs play a role in human infection with avian influenza A H9N2 viruses?]. Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi 2005; 19:106–109 (English abstract) [PubMed]
    [Google Scholar]
  4. Peiris M, Yuen KY, Leung CW, Chan KH, Ip PL et al. Human infection with influenza H9N2. Lancet 1999; 354:916–917 [View Article][PubMed]
    [Google Scholar]
  5. Saito T, Lim W, Suzuki T, Suzuki Y, Kida H et al. Characterization of a human H9N2 influenza virus isolated in Hong Kong. Vaccine 2001; 20:125–133 [View Article][PubMed]
    [Google Scholar]
  6. Fusaro A, Monne I, Salviato A, Valastro V, Schivo A et al. Phylogeography and evolutionary history of reassortant H9N2 viruses with potential human health implications. J Virol 2011; 85:8413–8421 [View Article][PubMed]
    [Google Scholar]
  7. El-Zoghby EF, Arafa AS, Hassan MK, Aly MM, Selim A et al. Isolation of H9N2 avian influenza virus from bobwhite quail (Colinus virginianus) in Egypt. Arch Virol 2012; 157:1167–1172 [View Article][PubMed]
    [Google Scholar]
  8. Kandeil A, El-Shesheny R, Maatouq AM, Moatasim Y, Shehata MM et al. Genetic and antigenic evolution of H9N2 avian influenza viruses circulating in Egypt between 2011 and 2013. Arch Virol 2014; 159:2861–2876 [View Article][PubMed]
    [Google Scholar]
  9. Naguib MM, Arafa AS, El-Kady MF, Selim AA, Gunalan V et al. Evolutionary trajectories and diagnostic challenges of potentially zoonotic avian influenza viruses H5N1 and H9N2 co-circulating in Egypt. Infect Genet Evol 2015; 34:278–291 [View Article][PubMed]
    [Google Scholar]
  10. Kandeil A, Moatasim Y, Gomaa MR, Shehata MM, El-Shesheny R et al. Generation of a reassortant avian influenza virus H5N2 vaccine strain capable of protecting chickens against infection with Egyptian H5N1 and H9N2 viruses. Vaccine 2016; 34:218–224 [View Article][PubMed]
    [Google Scholar]
  11. Kayali G, Kandeil A, El-Shesheny R, Kayed AS, Gomaa MM et al. Active surveillance for avian influenza virus, Egypt, 2010–2012. Emerg Infect Dis 2014; 20:542–551 [View Article][PubMed]
    [Google Scholar]
  12. Dong G, Xu C, Wang C, Wu B, Luo J et al. Reassortant H9N2 influenza viruses containing H5N1-like PB1 genes isolated from black-billed magpies in southern China. PLoS One 2011; 6:e25808 [View Article][PubMed]
    [Google Scholar]
  13. Iqbal M, Yaqub T, Reddy K, Mccauley JW. Novel genotypes of H9N2 influenza A viruses isolated from poultry in Pakistan containing NS genes similar to highly pathogenic H7N3 and H5N1 viruses. PLoS One 2009; 4:e5788 [View Article][PubMed]
    [Google Scholar]
  14. Monne I, Yamage M, Dauphin G, Claes F, Ahmed G et al. Reassortant avian influenza A(H5N1) viruses with H9N2-PB1 gene in poultry, Bangladesh. Emerg Infect Dis 2013; 19:1630–1634 [View Article][PubMed]
    [Google Scholar]
  15. Abdelwhab EM, Abdel-Moneim AS. Epidemiology, ecology and gene pool of influenza A virus in Egypt: will Egypt be the epicentre of the next influenza pandemic?. Virulence 2015; 6:6–18 [View Article][PubMed]
    [Google Scholar]
  16. Kayali G, Kandeil A, El-Shesheny R, Kayed AS, Maatouq AM et al. Avianinfluenza A(H5N1) virus in Egypt. Emerg Infect Dis J 2016; 22: [Crossref]
    [Google Scholar]
  17. Gomaa MR, Kayed AS, Elabd MA, Zeid DA, Zaki SA et al. Avian influenza A(H5N1) and A(H9N2) seroprevalence and risk factors for infection among Egyptians: a prospective, controlled seroepidemiological study. J Infect Dis 2015; 211:1399–1407 [View Article][PubMed]
    [Google Scholar]
  18. Aamir UB, Wernery U, Ilyushina N, Webster RG. Characterization of avian H9N2 influenza viruses from United Arab Emirates 2000 to 2003. Virology 2007; 361:45–55 [View Article][PubMed]
    [Google Scholar]
  19. Golender N, Panshin A, Banet-Noach C, Nagar S, Pokamunski S et al. Genetic characterization of avian influenza viruses isolated in Israel during 2000–2006. Virus Genes 2008; 37:289–297 [View Article][PubMed]
    [Google Scholar]
  20. Tosh C, Nagarajan S, Behera P, Rajukumar K, Purohit K et al. Genetic analysis of H9N2 avian influenza viruses isolated from India. Arch Virol 2008; 153:1433–1439 [View Article][PubMed]
    [Google Scholar]
  21. Sorrell EM, Wan H, Araya Y, Song H, Perez DR. Minimal molecular constraints for respiratory droplet transmission of an avian-human H9N2 influenza A virus. Proc Natl Acad Sci USA 2009; 106:7565–7570 [View Article][PubMed]
    [Google Scholar]
  22. Lin YP, Shaw M, Gregory V, Cameron K, Lim W et al. Avian-to-human transmission of H9N2 subtype influenza A viruses: relationship between H9N2 and H5N1 human isolates. Proc Natl Acad Sci USA 2000; 97:9654–9658 [View Article][PubMed]
    [Google Scholar]
  23. Rolling T, Koerner I, Zimmermann P, Holz K, Haller O et al. Adaptive mutations resulting in enhanced polymerase activity contribute to high virulence of influenza A virus in mice. J Virol 2009; 83:6673–6680 [View Article][PubMed]
    [Google Scholar]
  24. Wang J, Sun Y, Xu Q, Tan Y, Pu J et al. Mouse-adapted H9N2 influenza A virus PB2 protein M147L and E627K mutations are critical for high virulence. PLoS One 2012; 7:e40752 [View Article][PubMed]
    [Google Scholar]
  25. Zhou B, Pearce MB, Li Y, Wang J, Mason RJ et al. Asparagine substitution at PB2 residue 701 enhances the replication, pathogenicity, and transmission of the 2009 pandemic H1N1 influenza A virus. PLoS One 2013; 8:e67616 [View Article][PubMed]
    [Google Scholar]
  26. Conenello GM, Tisoncik JR, Rosenzweig E, Varga ZT, Palese P et al. A single N66S mutation in the PB1-F2 protein of influenza A virus increases virulence by inhibiting the early interferon response in vivo. J Virol 2011; 85:652–662 [View Article][PubMed]
    [Google Scholar]
  27. Jiao P, Tian G, Li Y, Deng G, Jiang Y et al. A single-amino-acid substitution in the NS1 protein changes the pathogenicity of H5N1 avian influenza viruses in mice. J Virol 2008; 82:1146–1154 [View Article][PubMed]
    [Google Scholar]
  28. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol Rev 1992; 56:152–179[PubMed]
    [Google Scholar]
  29. Xu KM, Smith GJ, Bahl J, Duan L, Tai H et al. The genesis and evolution of H9N2 influenza viruses in poultry from southern China, 2000 to 2005. J Virol 2007; 81:10389–10401 [View Article][PubMed]
    [Google Scholar]
  30. Zhang P, Tang Y, Liu X, Peng D, Liu W et al. Characterization of H9N2 influenza viruses isolated from vaccinated flocks in an integrated broiler chicken operation in eastern China during a 5 year period (1998–2002). J Gen Virol 2008; 89:3102–3112 [View Article][PubMed]
    [Google Scholar]
  31. Li C, Yu K, Tian G, Yu D, Liu L et al. Evolution of H9N2 influenza viruses from domestic poultry in mainland China. Virology 2005; 340:70–83 [View Article][PubMed]
    [Google Scholar]
  32. Sun Y, Pu J, Fan L, Sun H, Wang J et al. Evaluation of the protective efficacy of a commercial vaccine against different antigenic groups of H9N2 influenza viruses in chickens. Vet Microbiol 2012; 156:193–199 [View Article][PubMed]
    [Google Scholar]
  33. Bahari P, Pourbakhsh SA, Shoushtari H, Bahmaninejad MA. Molecular characterization of H9N2 avian influenza viruses isolated from vaccinated broiler chickens in northeast Iran. Trop Anim Health Prod 2015; 47:1195–1201 [View Article][PubMed]
    [Google Scholar]
  34. Shen HQ, Yan ZQ, Zeng FG, Liao CT, Zhou QF et al. Isolation and phylogenetic analysis of hemagglutinin gene of H9N2 influenza viruses from chickens in South China from 2012 to 2013. J Vet Sci 2015; 16:317–324 [View Article][PubMed]
    [Google Scholar]
  35. Caton AJ, Brownlee GG, Yewdell JW, Gerhard W. The antigenic structure of the influenza virus A/PR/8/34 hemagglutinin (H1 subtype). Cell 1982; 31:417–427 [View Article][PubMed]
    [Google Scholar]
  36. Kaverin NV, Rudneva IA, Ilyushina NA, Lipatov AS, Krauss S et al. Structural differences among hemagglutinins of influenza A virus subtypes are reflected in their antigenic architecture: analysis of H9 escape mutants. J Virol 2004; 78:240–249 [View Article][PubMed]
    [Google Scholar]
  37. Guan Y, Smith GJ. Genetic characterisation of H9N2 influenza viruses in southern China. Hong Kong Med J 2016; 22:4–6
    [Google Scholar]
  38. Perez DR, Lim W, Seiler JP, Yi G, Peiris M et al. Role of quail in the interspecies transmission of H9 influenza A viruses: molecular changes on HA that correspond to adaptation from ducks to chickens. J Virol 2003; 77:3148–3156 [View Article][PubMed]
    [Google Scholar]
  39. Sang X, Wang A, Ding J, Kong H, Gao X et al. Adaptation of H9N2 AIV in guinea pigs enables efficient transmission by direct contact and inefficient transmission by respiratory droplets. Sci Rep 2015; 5:15928 [View Article][PubMed]
    [Google Scholar]
  40. Srinivasan K, Raman R, Jayaraman A, Viswanathan K, Sasisekharan R. Quantitative characterization of glycan-receptor binding of H9N2 influenza A virus hemagglutinin. PLoS One 2013; 8:e59550 [View Article][PubMed]
    [Google Scholar]
  41. Wan H, Perez DR. Amino acid 226 in the hemagglutinin of H9N2 influenza viruses determines cell tropism and replication in human airway epithelial cells. J Virol 2007; 81:5181–5191 [View Article][PubMed]
    [Google Scholar]
  42. Hoffmann E, Stech J, Guan Y, Webster RG, Perez DR. Universal primer set for the full-length amplification of all influenza A viruses. Arch Virol 2001; 146:2275–2289 [View Article][PubMed]
    [Google Scholar]
  43. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis for Windows 95/98/NT. Nucleic Acids Symp 1999; 41:95–98
    [Google Scholar]
  44. Tamura K, Peterson D, Peterson N, Stecher G, Nei M et al. mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011; 28:2731–2739 [View Article][PubMed]
    [Google Scholar]
  45. WHO WHO Manual on Animal Influenza Diagnosis and Surveillance World Health Organization: Geneva, Switzerland; 2002
    [Google Scholar]
  46. Cai Z, Zhang T, Wan XF. A computational framework for influenza antigenic cartography. PLoS Comput Biol 2010; 6:e1000949 [View Article][PubMed]
    [Google Scholar]
  47. Cai Z, Zhang T, Wan XF. Concepts and applications for influenza antigenic cartography. Influenza Other Respir Viruses 2011; 5:204–207[PubMed]
    [Google Scholar]
  48. Matrosovich MN, Gambaryan AS. Solid-phase assays of receptor-binding specificity. Methods Mol Biol 2012; 865:71–94 [View Article][PubMed]
    [Google Scholar]
  49. Hayden FG, Cote KM, Douglas RG Jr. Plaque inhibition assay for drug susceptibility testing of influenza viruses. Antimicrob Agents Chemother 1980; 17:865–870 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000657
Loading
/content/journal/jgv/10.1099/jgv.0.000657
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
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