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 19, Number 9—September 2013
Research

Antigenic and Molecular Characterization of Avian Influenza A(H9N2) Viruses, Bangladesh

Karthik Shanmuganatham, Mohammed M. Feeroz, Lisa Jones-Engel, Gavin J.D. Smith, Mathieu Fourment, David Walker, Laura McClenaghan, S.M. Rabiul Alam, M. Kamrul Hasan, Patrick Seiler, John Franks, Angie Danner, Subrata Barman, Pamela McKenzie, Scott Krauss, Richard J. Webby, and Robert G. WebsterComments to Author 
Author affiliations: St. Jude Children’s Research Hospital, Memphis, Tennessee, USA (K. Shanmuganatham, D. Walker, L. McClenaghan, P. Seiler, J. Franks, A. Danner, S. Barman, P. McKenzie, S. Krauss, R.J. Webby, R.G. Webster); Jahangirnagar University, Dhaka, Bangladesh (M.M. Feeroz, S.M.R. Alam, M.K. Hasan); University of Washington, Seattle, Washington, USA (L. Jones-Engel); Duke-NUS Graduate Medical School, Singapore (G.J.D. Smith, M. Fourment); Duke Global Health Institute, Durham, North Carolina, USA (G.J.D. Smith)

Main Article

Table 3

Antigenic analyses of avian influenza A(H9N2) viruses isolated from poultry in Bangladesh during 2008–2011 compared with reference strains*

Viruses and designations HI titers† obtained with reference ferret hyperimmune serum directed against
G1 clade
 Y280 Clade
 G1 clade
 Bangladesh subtype H9N2 viruses
Qa/HK/G1/97 HK/1073/97 Ck/HK/G9/97 Ck/Bei/1/94 Ck/Pk (Swabi)/NARC/2434/06 BD/0994/11 Env/BD/600/08 Env/BD/5473/09 Env/BD/907/09
Reference viruses and designation
A/Qa/HK/G1/97 160 320 – – – – – – –
A/Ck/HK/G9/97 40 80 640 320 160 160 80 80 –
A/Ck/Beijing/1/94 – – – 80 – – – – –
A/HK/1073/97 (human) 80 320 – – – – – – –
A/Ck/Pk(Swabi)/NARC–2434/06 80 160 320 320 2,560 2,560 2,560 1,280 320
A/BD/0994/2011 (human) 80 160 160 320 1,280 2,560 1,280 640 160
A/Env/BD/600/2008 (chicken) 80 160 160 320 1,280 2,560 1,280 1,280 160
A/Env/BD/907/2009 (quail) 40 80 40 40 80 80 40 – 160
A/Env/BD/5473/2009 (chicken)
 80
 160
320
 320
2,560
2,560
 2,560
 1,280
 640
Bangladesh isolates
From chickens, n = 27‡
A/Ck/BD/2075/2009 – 80 160 320 640 2,560 1,280 640 160
A/Ck/BD/5209/2009 40 160 320 320 1,280 2,560 2,560 640 320
A/Env/BD/8202/2010 (chicken) 80 160 320 320 1,280 1,280 1,280 640 320
A/Env/BD/8465/2010 (chicken) 160 320 640 320 2,560 >5,120 2,560 2,560 320
A/Ck/BD/8725/2010 80 160 320 320 1,280 2,560 1,280 640 160
A/Ck/BD/9334/2010 40 80 160 160 640 1,280 640 320 160
A/Env/BD/10234/2011 (chicken) 40 160 320 320 1,280 >5,120 2,560 1,280 320
A/Ck/BD/10450/2011 80 160 320 320 640 1,280 640 1,280 160
A/Ck/BD/11309/2011 40 160 320 320 1,280 2,560 1,280 1,280 320
A/Ck/BD/13962/2011 40 160 160 320 320 640 1,280 320 80
From quail, n = 10‡                  
A/Env/BD/5144/ 2009 (quail) – 40 40 40 160 160 160 80 40
A/Env/BD /10306/2011 (quail) 40 160 40 40 40 40 80 – –
A/Env/BD/10316/2011 (quail) 160 320 80 80 160 80 80 80 80
A/Env/BD/12103/ 2011 (quail) 40 40 40 40 40 40 – – 40
A/Env/BD/12116/ 2011 (quail) – – – – – – – – –
A/Env/BD/12119/2011 (quail) 80 160 80 80 80 160 80 80 80
From other poultry species, n = 7‡                  
A/Env/BD/1041/2009 (duck) – – – – – – – – –
A/Dk/BD/1231/2009 40 160 160 320 1,280 2,560 1,280 640 320
A/Pi/BD/4303/2009 40 160 160 160 640 2,560 1,280 640 160
A/Env/BD/12068/2011 (pigeon) 160 160 40 80 80 80 40 40 80
A/Env/BD/9306/2010 (parrot) 80 160 160 320 640 2,560 1,280 640 320
A/Env/BD/12077/2011 (turkey) 40 160 320 320 1,280 >5,120 2,560 640 320

*Boldface indicates homologous serum. HI, hemagglutination inhibition.
†HI tests were performed according to standard procedures (27).Titers are expressed as the reciprocal of the highest dilution of the last dilution that completely inhibited hemagglutination of 0.5% chicken erythrocytes.
‡Total number of influenza (H9N2) isolates with a similar HI pattern.

Main Article

References
  1. Butt  KM, Smith  GJ, Chen  H, Zhang  LJ, Leung  YH, Xu  KM, Human infection with an avian H9N2 influenza A virus in Hong Kong in 2003. J Clin Microbiol. 2005;43:5760–7 and. DOIPubMedGoogle Scholar
  2. Lin  YP, Shaw  M, Gregory  V, Cameron  K, Lim  W, Klimov  A, Avian-to-human transmission of H9N2 subtype influenza A viruses: relationship between H9N2 and H5N1 human isolates. Proc Natl Acad Sci U S A. 2000;97:9654–8 and. DOIPubMedGoogle Scholar
  3. Peiris  JS, Guan  Y, Markwell  D, Ghose  P, Webster  RG, Shortridge  KF. Cocirculation of avian H9N2 and contemporary “human” H3N2 influenza A viruses in pigs in southeastern China: potential for genetic reassortment? J Virol. 2001;75:9679–86 and. DOIPubMedGoogle Scholar
  4. Peiris  M, Yuen  KY, Leung  CW, Chan  KH, Ip  PLS, Lai  RWM, Human infection with influenza H9N2. Lancet. 1999;354:916–7 and. DOIPubMedGoogle Scholar
  5. Apurba Chakraborty. Outbreak of mild respiratory disease caused by H5N1 and H9N2 infections among young children in Dhaka, Bangladesh. Health and Science Bulletin (ICDDR,B). 2011 [cited 2012 Dec 18]. http://www.icddrb.org/what-we-do/publications/cat_view/52-publications/10042-icddrb-periodicals/10048-health-and-science-bulletin-bangla-and-english/11089-vol-9-no-2-english-2011-/11092-outbreak-of-mild-respiratory-disease-caused-by-h5n1-and-h9n2-infections-among-young-children-in-dhaka-bangladesh-2011
  6. 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;74:9372–80 and. DOIPubMedGoogle Scholar
  7. Guan  Y, Shortridge  KF, Krauss  S, Webster  RG. Molecular characterization of H9N2 influenza viruses: were they the donors of the “internal” genes of H5N1 viruses in Hong Kong? Proc Natl Acad Sci U S A. 1999;96:9363–7 and. DOIPubMedGoogle Scholar
  8. 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 and. DOIPubMedGoogle Scholar
  9. Alexander  DJ. Report on avian influenza in the Eastern Hemisphere during 1997–2002. Avian Dis. 2003;47(Suppl):792–7 and. DOIPubMedGoogle Scholar
  10. Cameron  KR, Gregory  V, Banks  J, Brown  IH, Alexander  DJ, Hay  AJ, H9N2 subtype influenza A viruses in poultry in Pakistan are closely related to the H9N2 viruses responsible for human infection in Hong Kong. Virology. 2000;278:36–41 and. DOIPubMedGoogle Scholar
  11. Fusaro  A, Monne  I, Salviato  A, Valastro  V, Schivo  A, Amarin  NM, Phylogeography and evolutionary history of reassortant H9N2 viruses with potential human health implications. J Virol. 2011;85:8413–21. DOIPubMedGoogle Scholar
  12. Ge  FF, Zhou  JP, Liu  J, Wang  J, Zhang  WY, Sheng  LP, Genetic evolution of H9 subtype influenza viruses from live poultry markets in Shanghai, China. J Clin Microbiol. 2009;47:3294–300 and. DOIPubMedGoogle Scholar
  13. Golender  N, Panshin  A, Banet-Noach  C, Nagar  S, Pokamunski  S, Pirak  M, Genetic characterization of avian influenza viruses isolated in Israel during 2000–2006. Virus Genes. 2008;37:289–97 and. DOIPubMedGoogle Scholar
  14. 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 and. DOIPubMedGoogle Scholar
  15. Lee  YJ, Shin  JY, Song  MS, Lee  YM, Choi  JG, Lee  EK, Continuing evolution of H9 influenza viruses in Korean poultry. Virology. 2007;359:313–23 and. DOIPubMedGoogle Scholar
  16. Li  C, Yu  K, Tian  G, Yu  D, Liu  L, Jing  B, Evolution of H9N2 influenza viruses from domestic poultry in Mainland China. Virology. 2005;340:70–83 and. DOIPubMedGoogle Scholar
  17. Toroghi  R, Momayez  R. Biological and molecular characterization of avian influenza virus (H9N2) isolates from Iran. Acta Virol. 2006;50:163–8 .PubMedGoogle Scholar
  18. Xu  KM, Li  KS, Smith  GJ, Li  JW, Tai  H, Zhang  JX, Evolution and molecular epidemiology of H9N2 influenza A viruses from quail in southern China, 2000 to 2005. J Virol. 2007;81:2635–45 and. DOIPubMedGoogle Scholar
  19. Guo  YJ, Krauss  S, Senne  DA, Mo  IP, Lo  KS, Xiong  XP, Characterization of the pathogenicity of members of the newly established H9N2 influenza virus lineages in Asia. Virology. 2000;267:279–88 and. DOIPubMedGoogle Scholar
  20. Li  KS, Xu  KM, Peiris  JS, Poon  LL, Yu  KZ, Yuen  KY, Characterization of H9 subtype influenza viruses from the ducks of southern China: a candidate for the next influenza pandemic in humans? J Virol. 2003;77:6988–94 and. DOIPubMedGoogle Scholar
  21. Ahmed  SS, Ersboll  AK, Biswas  PK, Christensen  JP, Hannan  AS, Toft  N. Ecological determinants of highly pathogenic avian influenza (H5N1) outbreaks in Bangladesh. PLoS ONE. 2012;7:e33938 and. DOIPubMedGoogle Scholar
  22. International Centre for Diarrhoeal Disease Research. Bangladesh. Backyard poultry raising practices in Bangladesh. Health and Science Bulletin (ICDDR,B). 2012 [cited 2012 Nov 26]. http://www.icddrb.org/what-we-do/publications/cat_view/52-publications/10042-icddrb-periodicals/10048-health-and-science-bulletin-bangla-and-english/14138-vol-10-no-3-english-2012/14144-backyard-poultry-raising-practices-in-bangladesh-implications-for-risk-of-avian-influenza-infection-in-humans
  23. World Health Organization. Cumulative number of confirmed human cases of avian influenza A(H5N1) [cited 2012 Nov 26]. http://www.who.int/influenza/human_animal_ interface/H5N1_cumulative_table_archives/en/index.htmlExternal
  24. Mondal  SP, Tardif-Douglin  D, Ryan-Silva  R, Magnani  R. Controlling highly pathogenic avian influenza, Bangladesh. Emerg Infect Dis. 2012;18:2083–5 and. DOIPubMedGoogle Scholar
  25. Dolberg  F. Poultry sector country review: Bangladesh. Food and Agricultural Organization of the United Nations. 2009 [cited 2012 Nov 26]. ftp://ftp.fao.org/docrep/fao/011/ai319e/ai319e00.pdf
  26. Negovetich  NJ, Feeroz  MM, Jones-Engel  L, Walker  D, Alam  SM, Hasan  K, Live bird markets of Bangladesh: H9N2 viruses and the near absence of highly pathogenic H5N1 influenza. PLoS ONE. 2011;6:e19311 and. DOIPubMedGoogle Scholar
  27. Palmer  DFDW, Coleman  MT, Schild  GC. Advanced laboratory techniques for influenza diagnosis. Immunology series no. 6. Atlanta: Centers for Disease Control, US Department of Health, Education and Welfare; 1975.
  28. 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;99:8950–5 and. DOIPubMedGoogle Scholar
  29. 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;146:2275–89 and. DOIPubMedGoogle Scholar
  30. Guindon  S, Dufayard  JF, Lefort  V, Anisimova  M, Hordijk  W, Gascuel  O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59:307–21 and. DOIPubMedGoogle Scholar
  31. Gupta  R, Jung  E, Brunak  S. Prediction of N-glycosylation sites in human proteins [cited 2012 Nov 26]. http://www.cbs.dtu.dk/services/NetNGlyc/
  32. Baigent  SJ, McCauley  JW. Influenza type A in humans, mammals and birds: determinants of virus virulence, host-range and interspecies transmission. Bioessays. 2003;25:657–71 and. DOIPubMedGoogle Scholar
  33. 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;81:5181–91 and. DOIPubMedGoogle Scholar
  34. Wan  H, Sorrell  EM, Song  H, Hossain  MJ, Ramirez-Nieto  G, Monne  I, Replication and transmission of H9N2 influenza viruses in ferrets: evaluation of pandemic potential. PLoS ONE. 2008;3:e2923 and. DOIPubMedGoogle Scholar
  35. Matrosovich  M, Zhou  N, Kawaoka  Y, Webster  R. The surface glycoproteins of H5 influenza viruses isolated from humans, chickens, and wild aquatic birds have distinguishable properties. J Virol. 1999;73:1146–55 .PubMedGoogle Scholar
  36. Chen  GW, Chang  SC, Mok  CK, Lo  YL, Kung  YN, Huang  JH, Genomic signatures of human versus avian influenza A viruses. Emerg Infect Dis. 2006;12:1353–60 and. DOIPubMedGoogle Scholar
  37. Jackson  D, Hossain  MJ, Hickman  D, Perez  DR, Lamb  RA. A new influenza virus virulence determinant: the NS1 protein four C-terminal residues modulate pathogenicity. Proc Natl Acad Sci U S A. 2008;105:4381–6 and. DOIPubMedGoogle Scholar
  38. Abbas  MA, Spackman  E, Swayne  DE, Ahmed  Z, Sarmento  L, Siddique  N, Sequence and phylogenetic analysis of H7N3 avian influenza viruses isolated from poultry in Pakistan 1995–2004. Virol J. 2010;7:137 and. DOIPubMedGoogle Scholar
  39. Kageyama  T, Fujisaki  S, Takashita  E, Xu  H, Yamada  S, Uchida  Y, Genetic analysis of novel avian A(H7N9) influenza viruses isolated from patients in China, February to April 2013. Euro Surveill. 2013;18:20453.PubMedGoogle Scholar
  40. Gao  R, Cao  B, Hu  Y, Feng  Z, Wang  D, Hu  W, Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med. 2013;368:1888–97 and. DOIPubMedGoogle Scholar

Main Article

Page created: August 20, 2013
Page updated: August 20, 2013
Page reviewed: August 20, 2013
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.
file_external