Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 15, Number 3—March 2009

Characterization of Avian Influenza Viruses A (H5N1) from Wild Birds, Hong Kong, 2004–2008

Gavin J.D. Smith1, Dhanasekaran Vijaykrishna1, Trevor M. Ellis, Kitman C. Dyrting, Y.H. Connie Leung, Justin Bahl, Chun W. Wong, Huang Kai, Mary K.W. Chow, Lian Duan, Allen S.L. Chan, Li Juan Zhang, Honglin Chen, Geraldine S.M. Luk, J.S. Malik Peiris, and Yi GuanComments to Author 
Author affiliations: State Key Laboratory of Emerging Infectious Diseases/The University of Hong Kong, Hong Kong Special Administrative Region, People’s Republic of China (G.J.D. Smith, D. Vijaykrishna, Y.H.C. Leung, J. Bahl, H. Kai, L. Duan, L.J. Zhang, H. Chen, J.S.M. Peiris, Y. Guan); Agriculture, Fisheries and Conservation Department, Hong Kong (T.M. Ellis, K.C. Dyrting, C.W. Wong, M.K.W. Chow, A.S.L. Chan, G.S.M. Luk); HKU-Pasteur Research Centre, Pokfulam, Hong Kong (J.S. Malik Peiris)

Main Article


Antigenic analysis of influenza viruses A (H5N1) by hemagglutinin inhibition test, Hong Kong, China, 2008*

Virus Clade† Ferret antisera titers to:
VNM1203‡ (clade 1) IDN5 (clade 2.1) CDC357 (clade 2.1) MNG244 (clade 2.2) HN101 (clade 2.3.1) VNM1455 (clade 2.3.2) Anhui1 (clade 2.3.4)
VNM1203 1 640 40 <40 <40 80 40 80
Dk/Hunan/795/2002 2.1 80 640 320 160 160 160 <40
IDN5 2.1 40 1,280 640 80 40 160 160
CDC357 2.1 80 2,560 1,280 160 80 320 320
BHG/Qinghai/1A/2005 2.2 40 320 160 320 160 80 40
HN101 2.3.1 40 640 160 640 640 320 80
CPH/HK/18/2005 2.3.2 <40 40 <40 40 80 <40 <40
VNM1455 2.3.2 40 160 160 160 160 320 <40
Pfalcon/HK/5211/2006 2.3.2 <40 320 160 40 80 160 <40
Common magpie/HK/5052/2007 2.3.2 <40 320 160 160 80 320 <40
Common buzzard/HK/9213/2007 2.3.2 <40 160 80 80 80 160 <40
Little egret/HK/8863/2007 2.3.2 <40 160 80 160 80 320 <40
BCN heron/HK/659/2008 2.3.2 <40 160 80 80 80 320 <40
Magpie robin/HK/109720/08 2.3.2 <40 320 160 320 160 640 <40
Ck/Guiyang/3570/2005 2.3.3 160 160 40 160 640 160 640
Dk/Fujian/1734/2005 2.3.4 80 160 80 <40 80 40 640
JWE/HK/1038/2006 2.3.4 80 320 160 40 640 320 1,280
SB munia/HK/2572/2007 2.3.4 80 80 40 <40 80 <40 640
Pfalcon/HK/2142/2008 2.3.4 80 <40 <40 <40 <40 <40 40
Pfalcon/HK/D0028/2004 9 320 80 40 <40 80 <40 160

*VNM1203, Vietnam/1203/2004; IDN5, Indonesia/5/2005; CDC357, Indonesia/CDC357/2006; MNG244, whooper swan/Mongolia/244/2005; HN101, duck/Hunan/101/2004; VNM1455, muscovy duck/Vietnam/1455/2006; Anhui1, Anhui/1/2005; Dk, duck; BHG, bar-headed goose; CPH, Chinese pond heron; HK, Hong Kong; Pfalcon, peregrine falcon; BCN heron, black-crowned night heron; Ck, chicken; JWE, Japanese white-eye; SB munia, scaly-breasted munia. Boldface numbers indicate titers to prototype viruses.
†Clade designations according to the World Health Organization influenza (H5N1) nomenclature system (21).
‡Ferret antisera dilution started at 1:40.

Main Article

  1. Li  KS, Guan  Y, Wang  J, Smith  GJ, Xu  KM, Duan  L, Genesis of a highly pathogenic and potentially pandemic H5N1 influenza virus in eastern Asia. Nature. 2004;430:20913. DOIPubMedGoogle Scholar
  2. Food and Agricultural Organization of the United Nations. FOAAIDEnews. Avian influenza disease emergency. Situation update 55. 2008 [cited 2008 Aug 28]. Available from
  3. World Health Organization Global Influenza Program Surveillance Network. Evolution of H5N1 avian influenza viruses in Asia. Emerg Infect Dis. 2005;11:151521.PubMedGoogle Scholar
  4. Guan  Y, Peiris  JS, Lipatov  AS, Ellis  TM, Dyrting  KC, Krauss  S, Emergence of multiple genotypes of H5N1 avian influenza viruses in Hong Kong SAR. Proc Natl Acad Sci U S A. 2002;99:89505. DOIPubMedGoogle Scholar
  5. Tumpey  TM, Suarez  DL, Perkins  LEL, Senne  DA, Lee  JG, Lee  YJ, Characterization of a highly pathogenic H5N1 avian influenza A virus isolated from duck meat. J Virol. 2002;76:634455. DOIPubMedGoogle Scholar
  6. Chen  H, Smith  GJD, Zhang  SY, Qin  K, Wang  J, Li  KS, H5N1 virus outbreak in migratory waterfowl. Nature. 2005;436:1912. DOIPubMedGoogle Scholar
  7. Chen  H, Smith  GJ, Li  KS, Wang  J, Fan  XF, Rayner  JM, Establishment of multiple sub-lineages of H5N1 influenza virus in Asia—implications for pandemic control. Proc Natl Acad Sci U S A. 2006;103:284550. DOIPubMedGoogle Scholar
  8. Smith  GJ, Naipospos  TS, Nguyen  TD, de Jong  MD, Vijaykrishna  D, Usman  TB, Evolution and adaptation of H5N1 influenza virus in avian and human hosts in Indonesia and Vietnam. Virology. 2006;350:25868. DOIPubMedGoogle Scholar
  9. Tran  TH, Nguyen  TL, Nguyen  TD, Luong  TS, Pham  PM, Nguyen  VC, Avian influenza A (H5N1) in 10 patients in Vietnam. N Engl J Med. 2004;350:117988. DOIPubMedGoogle Scholar
  10. Lee  CW, Suarez  DL, Tumpey  TM, Sung  HW, Kwon  YK, Lee  YJ, Characterization of highly pathogenic H5N1 avian influenza A viruses isolated from South Korea. J Virol. 2005;79:3692702. DOIPubMedGoogle Scholar
  11. Mase  M, Tsukamoto  K, Imada  T, Imai  K, Tanimura  N, Nakamura  K, Characterization of H5N1 influenza A viruses isolated during the 2003–2004 influenza outbreaks in Japan. Virology. 2005;332:16776. DOIPubMedGoogle Scholar
  12. Lee  YJ, Choi  YK, Kim  YJ, Song  MS, Jeong  OM, Lee  EK, Highly pathogenic avian influenza virus (H5N1) in domestic poultry and relationship with migratory birds, South Korea. Emerg Infect Dis. 2008;14:48790. DOIPubMedGoogle Scholar
  13. Sims  LD. Experience in control of avian influenza in Asia. Dev Biol (Basel). 2007;130:3943.PubMedGoogle Scholar
  14. Ellis  TM, Bousfield  RB, Bissett  LA, Dyrting  KC, Luk  GSM, Tsim  ST, Investigation of outbreaks of highly pathogenic H5N1 avian influenza in waterfowl and wild birds in Hong Kong in late 2002. Avian Pathol. 2004;33:492505. DOIPubMedGoogle Scholar
  15. Sims  LD, Ellis  TM, Liu  KK, Dyrting  K, Wong  H, Peiris  M, Avian influenza in Hong Kong 1997–2002. Avian Dis. 2003;47(Suppl):8328. DOIPubMedGoogle Scholar
  16. Sims  LD, Guan  Y, Ellis  TM, Liu  KK, Dyrting  K, Wong  H, An update on avian influenza in Hong Kong 2002. Avian Dis. 2003;47(Suppl):10836. DOIPubMedGoogle Scholar
  17. Ellis  TM, Dyrting  KC, Wong  CW, Chadwick  B, Chan  C, Chiang  M, Analysis of H5N1 avian influenza infections from wild bird surveillance in Hong Kong from January 2006 to October 2007. Avian Pathol. In press.
  18. Smith  GJD, Fan  XH, Wang  J, Li  KS, Qin  K, Zhang  JX, Emergence and predominance of an H5N1 influenza variant in China. Proc Natl Acad Sci U S A. 2006;103:1693641. DOIPubMedGoogle Scholar
  19. Guan  Y, Poon  LLM, Cheung  CY, Ellis  TM, Lim  W, Lipatov  AS, H5N1 influenza: a protean pandemic threat. Proc Natl Acad Sci U S A. 2004;101:815661. DOIPubMedGoogle Scholar
  20. Viney  C, Phillipps  K, Ying  LC. Birds of Hong Kong and South China, 7th ed. Hong Kong: Government Printer; 1996.
  21. World Health Organization. Towards a unified nomenclature system for the highly pathogenic H5N1 avian influenza viruses. 2007 [cited 2008 May 21]. Available from
  22. Duan  L, Bahl  J, Smith  GJ, Wang  J, Vijaykrishna  D, Zhang  LJ, The development and genetic diversity of H5N1 influenza virus in China, 1996–2006. Virology. 2008;380:24354. DOIPubMedGoogle Scholar
  23. Spackman  E, Senne  DA, Myers  TJ, Bulaga  LL, Garber  LP, Perdue  ML, Development of a real-time reverse transcriptase PCR assay for type A influenza virus and the avian H5 and H7 hemagglutinin subtypes. J Clin Microbiol. 2002;40:325660. DOIPubMedGoogle Scholar
  24. Guan  Y, Shortridge  KF, Krauss  S, Chin  PS, Dyrting  KC, Ellis  TM, H9N2 influenza viruses possessing H5N1-like internal genomes continue to circulate in poultry in southeastern China. J Virol. 2000;74:937280. DOIPubMedGoogle Scholar
  25. Bao  Y, Bolotov  P, Dernovoy  D, Kiryutin  B, Zaslavsky  L, Tatusova  T, The influenza virus resource at the National Center for Biotechnology Information. J Virol. 2008;82:596601. DOIPubMedGoogle Scholar
  26. Nylander  JAA. MrModelTest version 2. Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden. 2004 [cited 2008 May 21] Available from
  27. Swofford  DL. PAUP*: phylogenetic analysis using parsimony (and other methods) 4.0 beta. Sunderland (MA): Sinauer Associates; 2001.
  28. Huelsenbeck  JP, Ronquist  FR. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17:7545. DOIPubMedGoogle Scholar
  29. Ha  Y, Stevens  DJ, Skehel  JJ, Wiley  DC. X-ray structures of H5 avian and H9 swine influenza virus hemagglutinins bound to avian and human receptor analogs. Proc Natl Acad Sci U S A. 2001;98:111816. DOIPubMedGoogle Scholar
  30. Stevens  J, Blixt  O, Tumpey  TM, Taubenberger  JK, Paulson  JC, Wilson  IA. Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus. Science. 2006;312:40410. DOIPubMedGoogle Scholar
  31. Yamada  S, Suzuki  Y, Suzuki  T, Le  MQ, Nidom  CA, Tagawa  YS, Hemagglutinin mutations responsible for the binding of H5N1 influenza A viruses to human type receptors. Nature. 2006;444:37882. DOIPubMedGoogle Scholar
  32. Wang  J, Vijaykrishna  D, Duan  L, Bahl  J, Zhang  JX. Identification of the progenitors of Indonesia and Vietnam avian influenza A (H5N1) viruses from southern China. J Virol. 2008;82:340514. DOIPubMedGoogle Scholar
  33. Treanor  JJ, Hayden  FG, Vrooman  PS, Barbarash  R, Bettis  R, Riff  D, Efficacy and safety of the oral neuraminidase inhibitor oseltamivir in treating acute influenza: a randomized controlled trial. JAMA. 2000;283:101624. DOIPubMedGoogle Scholar
  34. Cheung  CL, Rayner  JM, Smith  GJD, Wang  P, Naipospos  TSP, Zhang  J, Distribution of amantadine-resistant H5N1 avian influenza variants in Asia. J Infect Dis. 2006;193:16269. DOIPubMedGoogle Scholar
  35. Roberton  SI, Bell  DJ, Smith  GJ, Nicholls  JM, Chan  KH, Nguyen  DT, Avian Influenza H5N1 in viverrids: implications for wildlife health and conservation. Proc Biol Sci. 2006;273:172932. DOIPubMedGoogle Scholar
  36. Dung Nguyen  T, Vinh Nguyen  T, Vijaykrishna  D, Webster  RG, Guan  Y, Malik  PJS, Multiple sublineages of influenza A virus (H5N1), Vietnam, 2005–2007. Emerg Infect Dis. 2008;14:6326. DOIPubMedGoogle Scholar
  37. Starick  E, Beer  M, Hoffmann  B, Staubach  C, Werner  O, Globig  A, Phylogenetic analyses of highly pathogenic avian influenza virus isolates from Germany in 2006 and 2007 suggest at least three separate introductions of H5N1 virus. Vet Microbiol. 2008;128:24352. DOIPubMedGoogle Scholar
  38. World Health Organization. Antigenic and genetic characteristics of H5N1 viruses and candidate H5N1 vaccine viruses developed for potential use as human vaccines. 2008 [cited 2008 May 21]. Available from

Main Article

1These authors contributed equally to this article.

Page created: December 07, 2010
Page updated: December 07, 2010
Page reviewed: December 07, 2010
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.