1887

Abstract

The current epidemic of highly pathogenic avian influenza H5N1 virus is considered to pose a significant threat to the health of wild and domestic avian species, and even to human beings. The Black Sea–Mediterranean Flyway is one of the most important epidemic areas of H5N1. However, the epidemic along this flyway has not been fully explored. To better understand the role of hosts in the spread and evolution of H5N1 virus along the flyway, a phylogeographic study was conducted using haemagglutinin (HA) gene sequences obtained during 2005–2013. To infer phylodynamic spread in time and space, we used a flexible Bayesian statistical framework and modelled viral spatial diffusion as a continuous-time Markov-chain process along time-measured genealogies. Our results revealed that H5N1 virus isolated from wild birds showed an increase in genetic variation of HA gene from 2005–2007. The mean genetic distance of viruses isolated from poultry reached its peak in 2010, and dropped in 2011, increasing again in 2012–2013. The reconstruction of virus circulation revealed a different viral-migration network of H5N1 virus by different hosts. Western Russia constituted a link in viral migration from Russia to Europe and Africa. Cross-species transmission of H5N1 viruses predominated in the migration network of the Black Sea–Mediterranean Flyway. This might be due to the migration of birds across long distances and interaction between local poultry and migratory birds. Additionally, the short-distance spread of H5N1 viruses among poultry followed local transportation networks. Such findings will aid in developing effective disease control and prevention strategies.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000534
2016-09-01
2024-12-09
Loading full text...

Full text loading...

/deliver/fulltext/jgv/97/9/2129.html?itemId=/content/journal/jgv/10.1099/jgv.0.000534&mimeType=html&fmt=ahah

References

  1. Abdelwhab E. M., Selim A., Arafa A., Galal S., Kilany W. H., Hassan M. K., Aly M. M., Hafez M. H. 2010; Circulation of avian influenza H5N1 in live bird markets in Egypt. Avian Dis 54:911–914 [View Article][PubMed]
    [Google Scholar]
  2. Akanbi O. B., Taiwo V. O. 2014; Backyard poultry mortality associated with highly pathogenic avian influenza (HPAI) H5N1 outbreaks in nigeria. IOSR JAVS 7:23–27 [View Article]
    [Google Scholar]
  3. Alexander D. J. 2007; An overview of the epidemiology of avian influenza. Vaccine 25:5637–5644 [View Article]
    [Google Scholar]
  4. Brown I. H. 2010; Summary of avian influenza activity in Europe, Asia, and Africa, 2006–2009. Avian Dis 54:187–193 [View Article][PubMed]
    [Google Scholar]
  5. De Benedictis P., Manuel Joannis T., Hannatu Lombin L., Shittu I., Serena Beato M., Rebonato V., Cattoli G., Capua I. 2007; Field and laboratory findings of the first incursion of the Asian H5N1 highly pathogenic avian influenza virus in Africa. Avian Pathol 36:115–117 [View Article][PubMed]
    [Google Scholar]
  6. Gaidet N., Newman S. H., Hagemeijer W., Dodman T., Cappelle J., Hammoumi S., De Simone L., Takekawa J. Y. 2008; Duck migration and past influenza a (H5N1) outbreak areas. Emerg Infect Dis 14:1164–1166 [View Article][PubMed]
    [Google Scholar]
  7. Gilbert M., Chaitaweesub P., Parakamawongsa T., Premashthira S., Tiensin T., Kalpravidh W., Wagner H., Slingenbergh J. 2006; Free-grazing ducks and highly pathogenic avian influenza, Thailand. Emerg Infect Dis 12:227–234 [View Article][PubMed]
    [Google Scholar]
  8. Guan Y., Smith G., Webby R., Webster R. 2009; Molecular epidemiology of H5N1 avian influenza. Rev Sci Tech 28:39–47 [View Article][PubMed]
    [Google Scholar]
  9. Hill N. J., Takekawa J. Y., Ackerman J. T., Hobson K. A., Herring G., Cardona C. J., Runstadler J. A., Boyce W. M. 2012; Migration strategy affects avian influenza dynamics in mallards (Anas platyrhynchos). Mol Ecol 21:5986–5999 [View Article][PubMed]
    [Google Scholar]
  10. Hulse-Post D. J., Sturm-Ramirez K. M., Humberd J., Seiler P., Govorkova E. A., Krauss S., Scholtissek C., Puthavathana P., Buranathai C. et al. 2005; Role of domestic ducks in the propagation and biological evolution of highly pathogenic H5N1 influenza viruses in Asia. Proc Natl Acad Sci U S A 102:10682–10687 [View Article]
    [Google Scholar]
  11. Jiang Q., Zhou J., Jiang Z., Xu B. 2014; Identifying risk factors of avian infectious diseases at household level in Poyang Lake region, China. Prev Vet Med 116:151–160 [View Article][PubMed]
    [Google Scholar]
  12. Kang H.-M., Batchuluun D., Kim M.-C., Choi J.-G., Erdene-Ochir T.-O., Paek M.-R., Sugir T., Sodnomdarjaa R., Kwon J.-H. et al. 2011; Genetic analyses of H5N1 avian influenza virus in Mongolia, 2009 and its relationship with those of eastern Asia. Vet Microbiol 147:170–175 [View Article][PubMed]
    [Google Scholar]
  13. Katoh K., Misawa K., Kuma K., Miyata T. 2002; MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066 [View Article][PubMed]
    [Google Scholar]
  14. Kilpatrick A. M., Chmura A. A., Gibbons D. W., Fleischer R. C., Marra P. P., Daszak P. 2006; Predicting the global spread of H5N1 avian influenza. Proc Natl Acad Sci 103:19368–19373 [View Article]
    [Google Scholar]
  15. Kou Z., Li Y., Yin Z., Guo S., Wang M., Gao X., Li P., Tang L., Jiang P. et al. 2009; The survey of H5N1 flu virus in wild birds in 14 provinces of China from 2004 to 2007. PLoS One 4:e6926 [View Article][PubMed]
    [Google Scholar]
  16. Lemey P., Rambaut A., Drummond A. J., Suchard M. A. 2009; Bayesian phylogeography finds its roots. PLoS Comput Biol 5:e1000520 [View Article][PubMed]
    [Google Scholar]
  17. Lewis N. S., Verhagen J. H., Javakhishvili Z., Russell C. A., Lexmond P., Westgeest K. B., Bestebroer T. M., Halpin R. A., Lin X. et al. 2015; Influenza A virus evolution and spatio-temporal dynamics in Eurasian wild birds: a phylogenetic and phylogeographical study of whole-genome sequence data. J Gen Virol 96:2050–2060 [View Article][PubMed]
    [Google Scholar]
  18. Li K., Guan Y., Wang J., Smith G., Xu K., Duan L., Rahardjo A., 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]
  19. Li R., Jiang Z., Xu B. 2014; Global spatiotemporal and genetic footprint of the H5N1 avian influenza virus. Int J Health Geogr 13:14 [View Article][PubMed]
    [Google Scholar]
  20. 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]
  21. Olsen B., Munster V. J., Wallensten A., Waldenstrom J., Osterhaus A. D. M. E., Fouchier R. A. 2006; Global patterns of influenza A virus in wild birds. Science 312:384–388 [View Article][PubMed]
    [Google Scholar]
  22. Peterson A. T. 2006; Ecologic niche modeling and spatial patterns of disease transmission. Emerg Infect Dis 12:1822 [View Article][PubMed]
    [Google Scholar]
  23. Peterson A. T., Williams R. A. 2008; Risk mapping of highly pathogenic avian influenza distribution and spread. Ecol and Soc 13:15
    [Google Scholar]
  24. Rabaa M. A., Hang V. T., Wills B., Farrar J., Simmons C. P., Holmes E. C. 2010; Phylogeography of recently emerged DENV-2 in Southern Viet Nam. PLoS Negl Trop Dis 4:e766 [View Article][PubMed]
    [Google Scholar]
  25. Reperant L. A., Fuckar N. S., Osterhaus A. D., Dobson A. P., Kuiken T. 2010; Spatial and temporal association of outbreaks of H5N1 influenza virus infection in wild birds with the 0°C isotherm. PLoS Pathog 6:e1000854 [View Article][PubMed]
    [Google Scholar]
  26. Russell C. A., Jones T. C., Barr I. G., Cox N. J., Garten R. J., Gregory V., Gust I. D., Hampson A. W., Hay A. J. et al. 2008; The global circulation of seasonal influenza A (H3N2) viruses. Science 320:340–346 [View Article][PubMed]
    [Google Scholar]
  27. Tian H., Zhou S., Dong L., Van Boeckel T. P., Cui Y., Wu Y., Cazelles B., Huang S., Yang R. et al. 2015a; Avian influenza H5N1 viral and bird migration networks in Asia. Proc Natl Acad Sci 112:172–177 [View Article]
    [Google Scholar]
  28. Tian H., Cui Y., Dong L., Zhou S., Li X., Huang S., Yang R., Xu B. 2015b; Spatial, temporal and genetic dynamics of highly pathogenic avian influenza A (H5N1) virus in China. BMC Infect Dis 15:54–15 [View Article][PubMed]
    [Google Scholar]
  29. Vijaykrishna D., Bahl J., Riley S., Duan L., Zhang J. X., Chen H., Peiris J. S., Smith G. J., Guan Y. 2008; Evolutionary dynamics and emergence of panzootic H5N1 influenza viruses. PLoS Pathog 4:e1000161 [View Article][PubMed]
    [Google Scholar]
  30. Wang G., Zhang T., Li X., Jiang Z., Jiang Q., Chen Q., Tu X., Chen Z., Chang J. et al. 2014; Serological evidence of H7, H5 and H9 avian influenza virus co-infection among herons in a city park in Jiangxi, China. Sci Rep 4:6345 [View Article][PubMed]
    [Google Scholar]
  31. Wang Y., Jiang Z., Jin Z., Tan H., Xu B. 2013; Risk factors for infectious diseases in backyard poultry farms in the Poyang Lake area, China. PLoS One 8:e67366 [View Article][PubMed]
    [Google Scholar]
  32. WHO, OIE, FAO & H5N1 Evolution Working Group 2008; Toward a unified nomenclature system for highly pathogenic avian influenza virus (H5N1). Emerg Infect Dis 14:e1
    [Google Scholar]
  33. Wilking H., Ziller M., Staubach C., Globig A., Harder T. C., Conraths F. J. 2009; Chances and limitations of wild bird monitoring for the avian influenza virus H5N1 — detection of pathogens highly mobile in time and space. PLoS One 4:e6639 [View Article][PubMed]
    [Google Scholar]
  34. Zhang T., Bi Y., Tian H., Li X., Liu D., Wu Y., Jin T., Wang Y., Chen Q. et al. 2014; Human infection with influenza virus A(H10N8) from live poultry markets, China, 2014. Emerg Infect Dis 20:2076–2079 [View Article][PubMed]
    [Google Scholar]
/content/journal/jgv/10.1099/jgv.0.000534
Loading
/content/journal/jgv/10.1099/jgv.0.000534
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