EcoHealth

, Volume 9, Issue 1, pp 60–69 | Cite as

Highly Pathogenic H5N1 Avian Influenza Viruses Exhibit Few Barriers to Gene Flow in Vietnam

  • Margaret Carrel
  • Xiu-Feng Wan
  • Tung Nguyen
  • Michael Emch
Original Contribution

Abstract

Locating areas where genetic change is inhibited can illuminate underlying processes that drive evolution of pathogens. The persistence of highly pathogenic H5N1 avian influenza in Vietnam since 2003, and the continuous molecular evolution of Vietnamese avian influenza viruses, indicates that local environmental factors are supportive not only of incidence but also of viral adaptation. This article explores whether gene flow is constant across Vietnam, or whether there exist boundary areas where gene flow exhibits discontinuity. Using a dataset of 125 highly pathogenic H5N1 avian influenza viruses, principal components analysis and wombling analysis are used to indicate the location, magnitude, and statistical significance of genetic boundaries. Results show that a small number of geographically minor boundaries to gene flow in highly pathogenic H5N1 avian influenza viruses exist in Vietnam, but that overall there is little division in genetic exchange. This suggests that differences in genetic characteristics of viruses from one region to another are not the result of barriers to H5N1 viral exchange in Vietnam, and that H5N1 avian influenza is able to spread relatively unimpeded across the country.

Keywords

H5N1 avian influenza gene flow wombling Vietnam 

References

  1. Barbujani G, Sokal RR (1990) Zones of sharp genetic change in Europe are also linguistic boundaries. Proceedings of the National Academy of Sciences of the United States of America 87:1816.PubMedCrossRefGoogle Scholar
  2. Barbujani G, Oden NL, Sokal RR (1989) Detecting regions of abrupt change in maps of biological variables. Systematic Biology 38:376.Google Scholar
  3. Brierley AS, Thorpe JP, Pierce GJ, Clarke MR, Boyle PR (1995) Genetic variation in the neritic squid Loligo forbesi (Myopsida: Loliginidae) in the northeast Atlantic Ocean. Marine Biology 122:79-86.CrossRefGoogle Scholar
  4. Carrel MA, Emch M, Jobe RT, Moody A, Wan XF (2010) Spatiotemporal structure of molecular evolution of H5N1 highly pathogenic avian influenza viruses in Vietnam. PLoS One 5:e8631.PubMedCrossRefGoogle Scholar
  5. Chen H, Smith GJ, Li KS, Wang J, Fan XH, Rayner JM, et al. (2006) Establishment of multiple sublineages of H5N1 influenza virus in Asia: implications for pandemic control. Proceedings of the National Academy of Sciences of the United States of America 103:2845-50.PubMedCrossRefGoogle Scholar
  6. Cristalli A, Capua I (2007) Practical problems in controlling H5N1 high pathogenicity avian influenza at village level in Vietnam and introduction of biosecurity measures. Avian Diseases 51:461-2.PubMedCrossRefGoogle Scholar
  7. Davis CT, Balish AL, O’Neill E, Nguyen CV, Cox NJ, Xiyan X, et al. (2010) Detection and characterization of clade 7 high pathogenicity avian influenza H5N1 viruses in chickens seized at ports of entry and live poultry markets in Vietnam. Avian Diseases 54:307-12.PubMedCrossRefGoogle Scholar
  8. FAO. 2011. Bird flu rears its head again. Food and Agriculture Organization of the United Nations Media Centre. http://www.fao.org/news/story/en/item/87196/icode/. Accessed 19 January 2012.
  9. Fourment M, Gibbs M (2006) PATRISTIC: a program for calculating patristic distances and graphically comparing the components of genetic change. BMC Evolutionary Biology 6:1.PubMedCrossRefGoogle Scholar
  10. Gambotto A, Barratt-Boyes SM, de Jong MD, Neumann G, Kawaoka Y (2008) Human infection with highly pathogenic H5N1 influenza virus. Lancet 371:1464-75.PubMedCrossRefGoogle Scholar
  11. Geiss GK, Salvatore M, Tumpey TM, Carter VS, Wang X, Basler CF, et al. (2002) Cellular transcriptional profiling in influenza A virus-infected lung epithelial cells: the role of the nonstructural NS1 protein in the evasion of the host innate defense and its potential contribution to pandemic influenza. Proceedings of the National Academy of Sciences of the United States of America 99:10736-41.PubMedCrossRefGoogle Scholar
  12. Gilbert M, Chaitaweesub P, Parakamawongsa T, Premashthira S, Tiensin T, Kalpravidh W, et al. (2006) Free-grazing ducks and highly pathogenic avian influenza, Thailand. Emerging Infectious Diseases 12:227-34.PubMedCrossRefGoogle Scholar
  13. Gilbert M, Xiao X, Pfeiffer DU, Epprecht M, Boles S, Czarnecki C, et al. (2008) Mapping H5N1 highly pathogenic avian influenza risk in Southeast Asia. Proceedings of the National Academy of Sciences of the United States of America 105:4769-74.PubMedCrossRefGoogle Scholar
  14. Hulse-Post D, Franks J, Boyd K, Salomon R, Hoffmann E, Yen HL, et al. (2007) Molecular Changes in the Polymerase Genes (PA and PB1) Associated with High Pathogenicity of H5N1 Influenza Virus in Mallard Ducks. Journal of Virology 81:8515.PubMedCrossRefGoogle Scholar
  15. Jacquez GM (2010) Geographic boundary analysis in spatial and spatio-temporal epidemiology: Perspective and prospects. Spatial and Spatio-temporal Epidemiology 1: 207-218.PubMedCrossRefGoogle Scholar
  16. Jacquez GM, Maruca S, Fortin MJ (2000) From fields to objects: a review of geographic boundary analysis. Journal of Geographical Systems 2:221-41.CrossRefGoogle Scholar
  17. Lam TTY, Ip HS, Ghedin E, Wentworth DE, Halpin RA, Stockwell TB, et al. (2011) Migratory flyway and geographical distance are barriers to the gene flow of influenza virus among North American birds. Ecology Letters 15:24-33.PubMedCrossRefGoogle Scholar
  18. Li XH, Tian HD, Heiner M, Li DM (2011) Global Occurrence and Spread of Highly Pathogenic Avian Influenza Virus of the Subtype H5N1. Avian Diseases 55:21-8.PubMedCrossRefGoogle Scholar
  19. Magalhães RS, Ortiz-Pelaez A, Thi K, Dinh Q, Otte J, Pfeiffer D (2010) Associations between attributes of live poultry trade and HPAI H5N1 outbreaks: a descriptive and network analysis study in northern Vietnam. BMC Veterinary Research 6:10.CrossRefGoogle Scholar
  20. Martin V, Pfeiffer DU, Zhou X, Xiao X, Prosser DJ, Guo F, et al. (2011) Spatial distribution and risk factors of highly pathogenic avian influenza (HPAI) H5N1 in China. PLoS Pathogens 7:e1001308.PubMedCrossRefGoogle Scholar
  21. Muramoto Y, Le TQ, Phuong LS, Nguyen T, Nguyen TH, Sakai-Tagawa Y, et al. (2006) Pathogenicity of H5N1 influenza A viruses isolated in Vietnam between late 2003 and 2005. The Journal of veterinary medical science / the Japanese Society of Veterinary Science 68:735-7.PubMedCrossRefGoogle Scholar
  22. Neumann G, Kawaoka Y (2006) Host range restriction and pathogenicity in the context of influenza pandemic. Emerging Infectious Diseases 12:881-6.PubMedCrossRefGoogle Scholar
  23. Nguyen DC, Uyeki TM, Jadhao S, Maines T, Shaw M, Matsuoka Y, et al. (2005) Isolation and characterization of avian influenza viruses, including highly pathogenic H5N1, from poultry in live bird markets in Hanoi, Vietnam, in 2001. Journal of Virology 79:4201-12.PubMedCrossRefGoogle Scholar
  24. Nguyen T, Davis CT, Stembridge W, Shu B, Balish A, Inui K, et al. (2009) Characterization of a highly pathogenic avian influenza H5N1 virus sublineage in poultry seized at ports of entry into Vietnam. Virology 387:250-6.PubMedCrossRefGoogle Scholar
  25. Novembre J, Stephens M (2008) Interpreting principal component analyses of spatial population genetic variation. Nature genetics 40:646-9.PubMedCrossRefGoogle Scholar
  26. Paul M, Tavornpanich S, Abrial D, Gasqui P, Charras-Garrido M, Thanapongtharm W, et al. 2010. Anthropogenic factors and the risk of highly pathogenic avian influenza H5N1: prospects from a spatial-based model. Veterinary Research 41:28.PubMedCrossRefGoogle Scholar
  27. Piertney SB, Maccoll ADC, Bacon PJ, Dallas JF (1998) Local genetic structure in red grouse (Lagopus lagopus scoticus): evidence from microsatellite DNA markers. Molecular Ecology 7:1645-54.PubMedCrossRefGoogle Scholar
  28. Real LA, Henderson JC, Biek R, Snaman J, Jack TL, Childs JE, et al. (2005) Unifying the spatial population dynamics and molecular evolution of epidemic rabies virus. Proceedings of the National Academy of Sciences of the United States of America 102:12107.PubMedCrossRefGoogle Scholar
  29. Rosenberg MS, Anderson CD (2010) PASSaGE: Pattern analysis, spatial statistics and geographic exegesis. Version 2. Methods in Ecology and Evolution 2:229-32.CrossRefGoogle Scholar
  30. Smith GJ, Naipospos TS, Nguyen TD, de Jong MD, Vijaykrishna D, Usman TB, et al. (2006) Evolution and adaptation of H5N1 influenza virus in avian and human hosts in Indonesia and Vietnam. Virology 350:258-68.PubMedCrossRefGoogle Scholar
  31. Tada T, Suzuki K, Sakurai Y, Kubo M, Okada H, Itoh T, et al. (2011) NP Body Domain and PB2 Contribute to Increased Virulence of H5N1 Highly Pathogenic Avian Influenza Viruses in Chickens. Journal of Virology 85:1834.PubMedCrossRefGoogle Scholar
  32. Wallace RG, Fitch WM (2008) Influenza A H5N1 immigration is filtered out at some international borders. PLoS ONE 3:e1697.PubMedCrossRefGoogle Scholar
  33. Wan XF, Nguyen T, Davis CT, Smith CB, Zhao ZM, Carrel M, et al. (2008) Evolution of highly pathogenic H5N1 avian influenza viruses in Vietnam between 2001 and 2007. PLoS ONE 3:e3462.PubMedCrossRefGoogle Scholar
  34. Wasilenko JL, Lee CW, Sarmento L, Spackman E, Kapczynski DR, Suarez DL, et al. (2008) NP, PB1, and PB2 viral genes contribute to altered replication of H5N1 avian influenza viruses in chickens. Journal of Virology 82:4544.PubMedCrossRefGoogle Scholar
  35. Wheeler DC, Waller LA (2008) Mountains, valleys, and rivers: the transmission of raccoon rabies over a heterogeneous landscape. Journal of Agricultural, Biological, and Environmental Statistics 13:388-406.PubMedCrossRefGoogle Scholar
  36. Womble WH (1951) Differential Systematics. Science 114:315-22. PubMedCrossRefGoogle Scholar

Copyright information

© International Association for Ecology and Health 2012

Authors and Affiliations

  • Margaret Carrel
    • 1
  • Xiu-Feng Wan
    • 2
  • Tung Nguyen
    • 3
  • Michael Emch
    • 4
  1. 1.Department of GeographyUniversity of IowaIowa CityUSA
  2. 2.Department of Basic Sciences, College of Veterinary MedicineMississippi State UniversityMississippi StateUSA
  3. 3.Department of Animal HealthNational Center for Veterinary DiagnosticsHanoiVietnam
  4. 4.Department of GeographyUniversity of North Carolina-Chapel HillChapel HillUSA

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