1887

Abstract

Although the quest to clarify the role of wild birds in the spread of the highly pathogenic H5N1 avian influenza virus (AIV) has yielded considerable data on AIVs in wild birds worldwide, information regarding the ecology and epidemiology of AIVs in African wild birds is still very limited. During AIV surveillance in Zambia (2008–2009), 12 viruses of distinct subtypes (H3N8, H4N6, H6N2, H9N1 and H11N9) were isolated from wild waterfowl. Phylogenetic analyses demonstrated that all the isolates were of the Eurasian lineage. Whilst some genes were closely related to those of AIVs isolated from wild and domestic birds in South Africa, intimating possible AIV exchange between wild birds and poultry in southern Africa, some gene segments were closely related to those of AIVs isolated in Europe and Asia, thus confirming the inter-regional AIV gene flow among these continents. Analysis of the deduced amino acid sequences of internal proteins revealed that several isolates harboured particular residues predominantly observed in human influenza viruses. Interestingly, the isolates with human-associated residues exhibited higher levels of virus replication in the lungs of infected mice and caused more morbidity as measured by weight loss than an isolate lacking such residues. This study stresses the need for continued monitoring of AIVs in wild and domestic birds in southern Africa to gain a better understanding of the emergence of strains with the potential to infect mammals.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.030403-0
2011-06-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/92/6/1416.html?itemId=/content/journal/jgv/10.1099/vir.0.030403-0&mimeType=html&fmt=ahah

References

  1. Abolnik C. 2007; Molecular characterization of H5N2 avian influenza viruses isolated from South African ostriches in 2006. Avian Dis 51:873–879 [View Article][PubMed]
    [Google Scholar]
  2. Abolnik C., Bisschop S., Gerdes T., Olivier A., Horner R. 2007; Outbreaks of avian influenza H6N2 viruses in chickens arose by a reassortment of H6N8 and H9N2 ostrich viruses. Virus Genes 34:37–45 [View Article][PubMed]
    [Google Scholar]
  3. Abolnik C., Gerdes G. H., Sinclair M., Ganzevoort B. W., Kitching J. P., Burger C. E., Romito M., Dreyer M., Swanepoel S. et al. 2010; Phylogenetic analysis of influenza A viruses (H6N8, H1N8, H4N2, H9N2, H10N7) isolated from wild birds, ducks, and ostriches in South Africa from 2007 to 2009. Avian Dis 54:Suppl.313–322 [View Article][PubMed]
    [Google Scholar]
  4. Alexander D. J. 2007; Summary of avian influenza activity in Europe, Asia, Africa, and Australasia, 2002-2006. Avian Dis 51:Suppl.161–166 [View Article][PubMed]
    [Google Scholar]
  5. Bahl J., Vijaykrishna D., Holmes E. C., Smith G. J. D., Guan Y. 2009; Gene flow and competitive exclusion of avian influenza A virus in natural reservoir hosts. Virology 390:289–297 [View Article][PubMed]
    [Google Scholar]
  6. Beare A. S., Webster R. G. 1991; Replication of avian influenza viruses in humans. Arch Virol 119:37–42 [View Article][PubMed]
    [Google Scholar]
  7. Brown I. H. 2010; Summary of avian influenza activity in Europe, Asia, and Africa, 2006–2009. Avian Dis 54:Suppl.187–193 [View Article][PubMed]
    [Google Scholar]
  8. Brown J. D., Goekjian G., Poulson R., Valeika S., Stallknecht D. E. 2009; Avian influenza virus in water: infectivity is dependent on pH, salinity and temperature. Vet Microbiol 136:20–26 [View Article][PubMed]
    [Google Scholar]
  9. Capua I., Alexander D. J. 2006; The challenge of avian influenza to the veterinary community. Avian Pathol 35:189–205 [View Article][PubMed]
    [Google Scholar]
  10. Caron A., Abolnik C., Mundava J., Gaidet N., Burger C. E., Mochotlhoane B., Bruinzeel L., Chiweshe N., de Garine-Wichatitsky M., Cumming G. S. 2010; Persistence of low pathogenic avian influenza virus in waterfowl in a Southern African ecosystem. EcoHealth Epub ahead of print [View Article][PubMed]
    [Google Scholar]
  11. Chen G.-W., Chang S.-C., Mok C.-K., Lo Y.-L., Kung Y.-N., Huang J.-H., Shih Y.-H., Wang J.-Y., Chiang C. et al. 2006; Genomic signatures of human versus avian influenza A viruses. Emerg Infect Dis 12:1353–1360[PubMed] [CrossRef]
    [Google Scholar]
  12. Conenello G. M., Zamarin D., Perrone L. A., Tumpey T., Palese P. 2007; A single mutation in the PB1-F2 of H5N1 (HK/97) and 1918 influenza A viruses contributes to increased virulence. PLoS Pathog 3:1414–1421 [View Article][PubMed]
    [Google Scholar]
  13. de Wit E., Kawaoka Y., de Jong M. D., Fouchier R. A. 2008; Pathogenicity of highly pathogenic avian influenza virus in mammals. Vaccine 26:Suppl. 4D54–D58 [View Article][PubMed]
    [Google Scholar]
  14. Driskell E. A., Jones C. A., Stallknecht D. E., Howerth E. W., Tompkins S. M. 2010; Avian influenza virus isolates from wild birds replicate and cause disease in a mouse model of infection. Virology 399:280–289 [View Article][PubMed]
    [Google Scholar]
  15. Duan L., Campitelli L., Fan X. H., Leung Y. H., Vijaykrishna D., Zhang J. X., Donatelli I., Delogu M., Li K. S. et al. 2007; Characterization of low-pathogenic H5 subtype influenza viruses from Eurasia: implications for the origin of highly pathogenic H5N1 viruses. J Virol 81:7529–7539 [View Article][PubMed]
    [Google Scholar]
  16. Ducatez M. F., Olinger C. M., Owoade A. A., De Landtsheer S., Ammerlaan W., Niesters H. G. M., Osterhaus A. D. M. E., Fouchier R. A. M., Muller C. P. 2006; Avian flu: multiple introductions of H5N1 in Nigeria. Nature 442:37 [View Article][PubMed]
    [Google Scholar]
  17. Finkelstein D. B., Mukatira S., Mehta P. K., Obenauer J. C., Su X., Webster R. G., Naeve C. W. 2007; Persistent host markers in pandemic and H5N1 influenza viruses. J Virol 81:10292–10299 [View Article][PubMed]
    [Google Scholar]
  18. Gaidet N., Dodman T., Caron A., Balança G., Desvaux S., Goutard F., Cattoli G., Lamarque F., Hagemeijer W., Monicat F. 2007; Avian influenza viruses in water birds, Africa. Emerg Infect Dis 13:626–629 [View Article][PubMed]
    [Google Scholar]
  19. Gaidet N., Cattoli G., Hammoumi S., Newman S. H., Hagemeijer W., Takekawa J. Y., Cappelle J., Dodman T., Joannis T. et al. 2008; Evidence of infection by H5N2 highly pathogenic avian influenza viruses in healthy wild waterfowl. PLoS Pathog 4:e1000127 [View Article][PubMed]
    [Google Scholar]
  20. Gill J. S., Webby R., Gilchrist M. J. R., Gray G. C. 2006; Avian influenza among waterfowl hunters and wildlife professionals. Emerg Infect Dis 12:1284–1286[PubMed] [CrossRef]
    [Google Scholar]
  21. Gillim-Ross L., Santos C., Chen Z., Aspelund A., Yang C.-F., Ye D., Jin H., Kemble G., Subbarao K. 2008; Avian influenza H6 viruses productively infect and cause illness in mice and ferrets. J Virol 82:10854–10863 [View Article][PubMed]
    [Google Scholar]
  22. Hinshaw V. S., Webster R. G., Easterday B. C., Bean W. J. Jr 1981; Replication of avian influenza A viruses in mammals. Infect Immun 34:354–361[PubMed]
    [Google Scholar]
  23. Huelsenbeck J. P., Ronquist F. R. 2001; mrbayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755 [View Article][PubMed]
    [Google Scholar]
  24. Joseph T., McAuliffe J., Lu B., Jin H., Kemble G., Subbarao K. 2007; Evaluation of replication and pathogenicity of avian influenza a H7 subtype viruses in a mouse model. J Virol 81:10558–10566 [View Article][PubMed]
    [Google Scholar]
  25. Kida H., Ito T., Yasuda J., Shimizu Y., Itakura C., Shortridge K. F., Kawaoka Y., Webster R. G. 1994; Potential for transmission of avian influenza viruses to pigs. J Gen Virol 75:2183–2188 [View Article][PubMed]
    [Google Scholar]
  26. Kim H.-R., Lee Y.-J., Lee K.-K., Oem J.-K., Kim S.-H., Lee M. -H., Lee O.-S., Park C.-K. 2010; Genetic relatedness of H6 subtype avian influenza viruses isolated from wild birds and domestic ducks in Korea and their pathogenicity in animals. J Gen Virol 91:208–219 [View Article][PubMed]
    [Google Scholar]
  27. Li K. S., Xu K. M., Peiris J. S., Poon L. L., Yu K. Z., Yuen K. Y., Shortridge K. F., Webster R. G., Guan Y. 2003; Characterization of H9 subtype influenza viruses from the ducks of southern China: a candidate for the next influenza pandemic in humans?. J Virol 77:6988–6994 [View Article][PubMed]
    [Google Scholar]
  28. Li K. S., Guan Y., Wang J., Smith G. J. D., Xu K. M., Duan L., Rahardjo A. P., Puthavathana P., Buranathai C. et al. 2004; Genesis of a highly pathogenic and potentially pandemic H5N1 influenza virus in eastern Asia. Nature 430:209–213 [View Article][PubMed]
    [Google Scholar]
  29. Munster V. J., Baas C., Lexmond P., Waldenström J., Wallensten A., Fransson T., Rimmelzwaan G. F., Beyer W. E., Schutten M. et al. 2007; Spatial, temporal, and species variation in prevalence of influenza A viruses in wild migratory birds. PLoS Pathog 3:e61 [View Article][PubMed]
    [Google Scholar]
  30. Murphy B. R., Hinshaw V. S., Sly D. L., London W. T., Hosier N. T., Wood F. T., Webster R. G., Chanock R. M. 1982; Virulence of avian influenza A viruses for squirrel monkeys. Infect Immun 37:1119–1126[PubMed]
    [Google Scholar]
  31. Myers K. P., Setterquist S. F., Capuano A. W., Gray G. C. 2007; Infection due to 3 avian influenza subtypes in United States veterinarians. Clin Infect Dis 45:4–9 [View Article][PubMed]
    [Google Scholar]
  32. Olsen B., Munster V. J., Wallensten A., Waldenström J., Osterhaus A. D., Fouchier R. A. 2006; Global patterns of influenza A virus in wild birds. Science 312:384–388 [View Article][PubMed]
    [Google Scholar]
  33. Peiris J. S., de Jong M. D., Guan Y. 2007; Avian influenza virus (H5N1): a threat to human health. Clin Microbiol Rev 20:243–267 [View Article][PubMed]
    [Google Scholar]
  34. Posada D., Crandall K. A. 2001; Selecting the best-fit model of nucleotide substitution. Syst Biol 50:580–601 [View Article][PubMed]
    [Google Scholar]
  35. Reed L. J., Muench H. 1938; A simple method of estimating fifty percent endpoints. Am J Hyg 27:493–497
    [Google Scholar]
  36. Röhm C., Horimoto T., Kawaoka Y., Süss J., Webster R. G. 1995; Do hemagglutinin genes of highly pathogenic avian influenza viruses constitute unique phylogenetic lineages?. Virology 209:664–670 [View Article][PubMed]
    [Google Scholar]
  37. Shaw M., Cooper L., Xu X., Thompson W., Krauss S., Guan Y., Zhou N., Klimov A., Cox N. et al. 2002; Molecular changes associated with the transmission of avian influenza a H5N1 and H9N2 viruses to humans. J Med Virol 66:107–114 [View Article][PubMed]
    [Google Scholar]
  38. Shinya K., Makino A., Ozawa M., Kim J. H., Sakai-Tagawa Y., Ito M., Le Q. M., Kawaoka Y. 2009; Ostrich involvement in the selection of H5N1 influenza virus possessing mammalian-type amino acids in the PB2 protein. J Virol 83:13015–13018 [View Article][PubMed]
    [Google Scholar]
  39. Shortridge K. F. 1992; Pandemic influenza: a zoonosis?. Semin Respir Infect 7:11–25[PubMed]
    [Google Scholar]
  40. Simulundu E., Mweene A. S., Tomabechi D., Hang’ombe B. M., Ishii A., Suzuki Y., Nakamura I., Sawa H., Sugimoto C. et al. 2009; Characterization of H3N6 avian influenza virus isolated from a wild white pelican in Zambia. Arch Virol 154:1517–1522 [View Article][PubMed]
    [Google Scholar]
  41. Smith G. J. D., Fan X. H., Wang J., Li K. S., Qin K., Zhang J. X., Vijaykrishna D., Cheung C. L., Huang K. et al. 2006; Emergence and predominance of an H5N1 influenza variant in China. Proc Natl Acad Sci U S A 103:16936–16941 [View Article][PubMed]
    [Google Scholar]
  42. Swofford, D. L. (2001). paup*: phylogenetic analysis using parsimony (and other methods) 4.0 beta. Sunderland, MA: Sinauer Associates
  43. 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 [View Article][PubMed]
    [Google Scholar]
  44. Wan H., Sorrell E. M., Song H., Hossain M. J., Ramirez-Nieto G., Monne I., Stevens J., Cattoli G., Capua I. et al. 2008; Replication and transmission of H9N2 influenza viruses in ferrets: evaluation of pandemic potential. PLoS ONE 3:e2923 [View Article][PubMed]
    [Google Scholar]
  45. Wang G., Zhan D., Li L., Lei F., Liu B., Liu D., Xiao H., Feng Y., Li J. et al. 2008; H5N1 avian influenza re-emergence of Lake Qinghai: phylogenetic and antigenic analyses of the newly isolated viruses and roles of migratory birds in virus circulation. J Gen Virol 89:697–702 [View Article][PubMed]
    [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. World Health Organization (2010). Cumulative number of confirmed human cases of avian influenza A/(H5N1) reported to WHO http://www.who.int/csr/disease/avian_influenza/country/cases_table_2010_12_29/en/index.html Accessed 4 January 2011
  48. Xu K. M., Smith G. J. D., Bahl J., Duan L., Tai H., Vijaykrishna D., Wang J., Zhang J. X., Li K. S. et al. 2007; The genesis and evolution of H9N2 influenza viruses in poultry from southern China, 2000 to 2005. J Virol 81:10389–10401 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.030403-0
Loading
/content/journal/jgv/10.1099/vir.0.030403-0
Loading

Data & Media loading...

Supplements

Supplementary material 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