Skip to main content
SpringerLink
Log in

The genetic and antigenic diversity of avian influenza viruses isolated from domestic ducks, muscovy ducks, and chickens in northern and southern Vietnam, 2010–2012

  • Published:
Virus Genes Aims and scope Submit manuscript

Abstract

To estimate the prevalence of avian influenza virus infection in Vietnam, surveillance was conducted in domestic and wild birds from households, live-bird markets, slaughtering sites, and bird sanctuaries in Vietnam between October 2010 and October 2012. Of the 4,550 samples collected, 226 influenza A virus isolates were obtained from domestic ducks, muscovy ducks, and chickens. Of these, 25 and 22 H5N1 highly pathogenic avian influenza viruses (HPAIVs) were isolated from apparently healthy domestic ducks in live-bird markets and slaughtering sites in northern and southern Vietnam, respectively. The HA genes of H5 viruses isolated from birds in northern Vietnam phylogenetically belonged to the genetic clade 2.3.2.1 and those in southern Vietnam belonged to the genetic clade 1.1. In addition, 39 H3, 12 H4, 1 H5, 93 H6, 2 H7, 18 H9, 3 H10, and 11 H11 viruses were isolated. Phylogenetic and antigenic analyses of the H6 and H9 viruses revealed that they were closely related to the isolates obtained from domestic poultry in China. Phylogenetic analyses of internal gene segments of these isolates revealed that these viruses were circulating in both domestic and wild birds in Asia and reassortment events had occurred frequently. Therefore, it will be important to continue the surveillance and strict controls over the movement and trade of poultry and poultry products in order to eradicate H5N1 HPAIV from Asia.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. H. Kida, R. Yanagawa, Y. Matsuoka, Infect. Immun. 30, 547–553 (1980)

    PubMed  CAS  Google Scholar 

  2. H. Kida, Y. Kawaoka, C.W. Naeve, R.G. Webster, Virology 159, 109–119 (1987)

    Article  PubMed  CAS  Google Scholar 

  3. X. Xu, K. Subbarao, N.J. Cox, Y. Guo, Virology 261, 15–19 (1999)

    Article  PubMed  CAS  Google Scholar 

  4. World Organisation for Animal Health (OIE), World Animal Health Information Database (WAHID) (2013), http://www.oie.int/wahis_2/public/wahid.php/Wahidhome/Home. Accessed 12 July 2013

  5. World Health Organization (WHO), Avian influenza in humans (2013), http://www.who.int/influenza/human_animal_interface/avian_influenza/en/. Accessed 12 July 2013

  6. WHO/OIE/FAO H5N1 Evolution Working Group, Influenza Other Respir. Viruses 6, 1–5 (2012)

    Article  Google Scholar 

  7. M. Okamatsu, T. Tanaka, N. Yamamoto, Y. Sakoda, T. Sasaki, Y. Tsuda, N. Isoda, N. Kokumai, A. Takada, T. Umemura, H. Kida, Virus Genes 41, 351–357 (2010)

    Article  PubMed  CAS  Google Scholar 

  8. G. Cattoli, A. Milani, N. Temperton, B. Zecchin, A. Buratin, E. Molesti, M.M. Aly, A. Arafa, I. Capua, J. Virol. 85, 8718–8724 (2011)

    Article  PubMed  CAS  Google Scholar 

  9. C. Grund, S.M. Abdelwhab el, A.S. Arafa, M. Ziller, M.K. Hassan, M.M. Aly, H.M. Hafez, T.C. Harder, M. Beer, Vaccine 29, 5567–5573 (2011)

    Article  PubMed  CAS  Google Scholar 

  10. D.C. Nguyen, T.M. Uyeki, S. Jadhao, T. Maines, M. Shaw, Y. Matsuoka, C. Smith, T. Rowe, X. Lu, H. Hall, X. Xu, A. Balish, A. Klimov, T.M. Tumpey, D.E. Swayne, L.P. Huynh, H.K. Nghiem, H.H. Nguyen, L.T. Hoang, N.J. Cox, J.M. Katz, J. Virol. 79, 4201–4212 (2005)

    Article  PubMed  CAS  Google Scholar 

  11. X.F. Wan, T. Nguyen, C.T. Davis, C.B. Smith, Z.M. Zhao, M. Carrel, K. Inui, H.T. Do, D.T. Mai, S. Jadhao, A. Balish, B. Shu, F. Luo, M. Emch, Y. Matsuoka, S.E. Lindstrom, N.J. Cox, C.V. Nguyen, A. Klimov, R.O. Donis, PLoS One 3, e3462 (2008)

    Article  PubMed  Google Scholar 

  12. T. Nguyen, C.T. Davis, W. Stembridge, B. Shu, A. Balish, K. Inui, H.T. Do, H.T. Ngo, X.F. Wan, M. McCarron, S.E. Lindstrom, N.J. Cox, C.V. Nguyen, A.I. Klimov, R.O. Donis, Virology 387, 250–256 (2009)

    Article  PubMed  CAS  Google Scholar 

  13. C.T. Davis, A.L. Balish, E. O’Neill, C.V. Nguyen, N.J. Cox, X. Xiyan, A. Klimov, T. Nguyen, R.O. Donis, Avian Dis. 54, 307–312 (2010)

    Article  PubMed  Google Scholar 

  14. T. Nguyen, P. Rivailler, C.T. Davis, T. Nguyen, T. Hoa do, A. Balish, N.H. Dang, J. Jones, D.T. Vui, N. Simpson, N.T. Huong, B. Shu, R. Loughlin, K. Ferdinand, S.E. Lindstrom, I.A. York, A. Klimov, R.O. Donis, Virology 432, 405–416 (2012)

    Article  PubMed  CAS  Google Scholar 

  15. H. Takakuwa, T. Yamashiro, M.Q. Le, L.S. Phuong, H. Ozaki, R. Tsunekuni, T. Usui, H. Ito, M. Morimatsu, Y. Tomioka, T. Yamaguchi, T. Ito, T. Murase, E. Ono, K. Otsuki, Prev. Vet. Med. 103, 192–200 (2012)

    Article  PubMed  Google Scholar 

  16. M.Q. Phan, W. Henry, C.B. Bui, D.H. Do, N.V. Hoang, N.T. Thu, T.T. Nguyen, T.D. Le, T.Q. Diep, K. Inui, J. Weaver, J. Carrique-Mas, Epidemiol. Infect. 1, 1–11 (2012)

    Google Scholar 

  17. K. Hotta, H. Takakuwa, Q.M. Le, S.L. Phuong, T. Murase, E. Ono, T. Ito, K. Otsuki, T. Yamashiro, Virus Res. 163, 448–453 (2012)

    Article  PubMed  CAS  Google Scholar 

  18. N. Nomura, Y. Sakoda, M. Endo, H. Yoshida, N. Yamamoto, M. Okamatsu, K. Sakurai, N.V. Hoang, L.V. Nguyen, H.D. Chu, T.N. Tien, H. Kida, Arch. Virol. 157, 247–257 (2012)

    Article  PubMed  CAS  Google Scholar 

  19. X.F. Wan, L. Dong, Y. Lan, L.P. Long, C. Xu, S. Zou, Z. Li, L. Wen, Z. Cai, W. Wang, X. Li, F. Yuan, H. Sui, Y. Zhang, J. Dong, S. Sun, Y. Gao, M. Wang, T. Bai, L. Yang, D. Li, W. Yang, H. Yu, S. Wang, Z. Feng, Y. Wang, Y. Guo, R.J. Webby, Y. Shu, J. Virol. 85, 13432–13438 (2011)

    Article  PubMed  CAS  Google Scholar 

  20. K. Huang, J. Bahl, X.H. Fan, D. Vijaykrishna, C.L. Cheung, R.J. Webby, R.G. Webster, H. Chen, G.J. Smith, J.S. Peiris, Y. Guan, J. Virol. 84, 6978–6986 (2010)

    Article  PubMed  CAS  Google Scholar 

  21. C.L. Cheung, D. Vijaykrishna, G.J. Smith, X.H. Fan, J.X. Zhang, J. Bahl, L. Duan, K. Huang, H. Tai, J. Wang, L.L. Poon, J.S. Peiris, H. Chen, Y. Guan, J. Virol. 81, 10402–10412 (2007)

    Article  PubMed  CAS  Google Scholar 

  22. Y. Guan, K.F. Shortridge, S. Krauss, R.G. Webster, Proc. Natl. Acad. Sci. USA 96, 9363–9367 (1999)

    Article  PubMed  CAS  Google Scholar 

  23. Y. Sun, J. Pu, Z. Jiang, T. Guan, Y. Xia, Q. Xu, L. Liu, B. Ma, F. Tian, E.G. Brown, J. Liu, Vet. Microbiol. 146, 215–225 (2010)

    Article  PubMed  CAS  Google Scholar 

  24. Y.J. Lee, J.Y. Shin, M.S. Song, Y.M. Lee, J.G. Choi, E.K. Lee, O.M. Jeong, H.W. Sung, J.H. Kim, Y.K. Kwon, J.H. Kwon, C.J. Kim, R.J. Webby, R.G. Webster, Y.K. Choi, Virology 359, 313–323 (2007)

    Article  PubMed  CAS  Google Scholar 

  25. H. Yoshida, Y. Sakoda, M. Endo, M. Motoshima, F. Yoshino, N. Yamamoto, M. Okamatsu, T. Soejima, S. Senba, H. Kanda, H. Kida, J. Vet. Med. Sci. 73, 753–758 (2011)

    Article  PubMed  CAS  Google Scholar 

  26. World Organisation for Animal Health (OIE), Manual of diagnostic Tests and Vaccines for Terrestrial Animal 2012, (2012), http://www.oie.int/en/international-standard-setting/terrestrial-manual/access-online/. Accessed 12 July 2013

  27. H. Kida, R. Yanagawa, Zentralbl Bakteriol Orig A 244, 135–143 (1979)

    PubMed  CAS  Google Scholar 

  28. K. Soda, H. Ozaki, Y. Sakoda, N. Isoda, Y. Haraguchi, S. Sakabe, N. Kuboki, N. Kishida, A. Takada, H. Kida, Arch. Virol. 153, 2041–2048 (2008)

    Article  PubMed  CAS  Google Scholar 

  29. M. Gilbert, L. Jambal, W.B. Karesh, A. Fine, E. Shiilegdamba, P. Dulam, R. Sodnomdarjaa, K. Ganzorig, D. Batchuluun, N. Tseveenmyadag, P. Bolortuya, C.J. Cardona, C.Y. Leung, J.S. Peiris, E. Spackman, D.E. Swayne, D.O. Joly, PLoS One 7, e44097 (2012)

    Article  PubMed  CAS  Google Scholar 

  30. Y. Han, G. Hou, W. Jiang, C. Han, S. Liu, J. Chen, J. Li, P. Zhang, B. Huang, Y. Liu, PLoS One 7, e33092 (2012)

    Article  PubMed  CAS  Google Scholar 

  31. Y. Sakoda, H. Ito, Y. Uchida, M. Okamatsu, N. Yamamoto, K. Soda, N. Nomura, S. Kuribayashi, S. Shichinohe, Y. Sunden, T. Umemura, T. Usui, H. Ozaki, T. Yamaguchi, T. Murase, T. Ito, T. Saito, A. Takada, H. Kida, J. Gen. Virol. 93, 541–550 (2012)

    Article  PubMed  CAS  Google Scholar 

  32. K. Huang, H. Zhu, X. Fan, J. Wang, C.L. Cheung, L. Duan, W. Hong, Y. Liu, L. Li, D.K. Smith, H. Chen, R.G. Webster, R.J. Webby, M. Peiris, Y. Guan, J. Virol. 86, 6075–6083 (2012)

    Article  PubMed  CAS  Google Scholar 

  33. K.S. Li, K.M. Xu, J.S. Peiris, L.L. Poon, K.Z. Yu, K.Y. Yuen, K.F. Shortridge, R.G. Webster, Y. Guan, J. Virol. 77, 6988–6994 (2003)

    Article  PubMed  CAS  Google Scholar 

  34. P.Q. Minh, R.S. Morris, B. Schauer, M. Stevenson, J. Benschop, H.V. Nam, R. Jackson, Prev. Vet. Med. 89, 16–24 (2009)

    Article  PubMed  Google Scholar 

  35. H. Chen, Rev. Sci. Tech. 28, 267–274 (2009)

    PubMed  CAS  Google Scholar 

  36. C.W. Lee, D.A. Senne, D.L. Suarez, J. Virol. 78, 8372–8381 (2004)

    Article  PubMed  CAS  Google Scholar 

  37. Y.K. Choi, S.H. Seo, J.A. Kim, R.J. Webby, R.G. Webster, Virology 332, 529–537 (2005)

    Article  PubMed  CAS  Google Scholar 

  38. J.G. Choi, H.M. Kang, M.C. Kim, M.R. Paek, H.R. Kim, B.S. Kim, J.H. Kwon, J.H. Kim, Y.J. Lee, Vet. Microbiol. 155, 147–157 (2012)

    Article  PubMed  CAS  Google Scholar 

  39. H.J. Moon, M.S. Song, D.J. Cruz, K.J. Park, P.N. Pascua, J.H. Lee, Y.H. Baek, D.H. Choi, Y.K. Choi, C.J. Kim, Arch. Virol. 155, 229–241 (2010)

    Article  PubMed  CAS  Google Scholar 

  40. P.S. Chin, E. Hoffmann, R. Webby, R.G. Webster, Y. Guan, M. Peiris, K.F. Shortridge, J. Virol. 76, 507–516 (2002)

    Article  PubMed  CAS  Google Scholar 

  41. N. Kishida, Y. Sakoda, M. Eto, Y. Sunaga, H. Kida, Arch. Virol. 149, 2095–2104 (2004)

    Article  PubMed  CAS  Google Scholar 

  42. M. Haghighat-Jahromi, K. Asasi, H. Nili, H. Dadras, A.H. Shooshtari, Arch. Virol. 153, 651–655 (2008)

    Article  PubMed  CAS  Google Scholar 

  43. J. Liu, K. Okazaki, H. Ozaki, Y. Sakoda, Q. Wu, F. Chen, H. Kida, Avian Pathol. 32, 551–560 (2003)

    Article  PubMed  CAS  Google Scholar 

  44. M. Liu, S. He, D. Walker, N. Zhou, D.R. Perez, B. Mo, F. Li, X. Huang, R.G. Webster, R.J. Webby, Virology 305, 267–275 (2003)

    Article  PubMed  CAS  Google Scholar 

  45. G. Fournie, J. Guitian, S. Desvaux, P. Mangtani, S. Ly, V.C. Cong, S. San, H. Dung do, D. Holl, D.U. Pfeiffer, S. Vong, A.C. Ghani, PLoS One 7, e37986 (2012)

    Article  PubMed  CAS  Google Scholar 

  46. G. Fournie, F.J. Guitian, P. Mangtani, A.C. Ghani, J. R. Soc. Interface 8, 1079–1089 (2011)

    Article  PubMed  CAS  Google Scholar 

  47. Y.H. Leung, E.H. Lau, L.J. Zhang, Y. Guan, B.J. Cowling, J.S. Peiris, Emerg. Infect. Dis. 18, 1339–1341 (2012)

    Article  PubMed  Google Scholar 

  48. N. Kishida, Y. Sakoda, N. Isoda, K. Matsuda, M. Eto, Y. Sunaga, T. Umemura, H. Kida, Arch. Virol. 150, 1383–1392 (2005)

    Article  PubMed  CAS  Google Scholar 

  49. M. Kajihara, K. Matsuno, E. Simulundu, M. Muramatsu, O. Noyori, R. Manzoor, E. Nakayama, M. Igarashi, D. Tomabechi, R. Yoshida, M. Okamatsu, Y. Sakoda, K. Ito, H. Kida, A. Takada, Jpn. J. Vet. Res. 59, 89–100 (2011)

    PubMed  Google Scholar 

  50. Y. Sakoda, S. Sugar, D. Batchluun, T.O. Erdene-Ochir, M. Okamatsu, N. Isoda, K. Soda, H. Takakuwa, Y. Tsuda, N. Yamamoto, N. Kishida, K. Matsuno, E. Nakayama, M. Kajihara, A. Yokoyama, A. Takada, R. Sodnomdarjaa, H. Kida, Virology 406, 88–94 (2010)

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Drs. Luk S. M. Geraldine and Y. Guan for providing viruses. We are grateful for the support of the Programme on Surveillance of Wild Birds and Domestic Animals along Migratory Flyways under the OIE/JTF Project for Strengthening HPAI Control in Asia. This work was partially supported by J-GRID, the Japan Initiative for Global Research Network on Infectious Diseases of the Ministry of Education, Culture, Sports, Science and Technology of Japan. This work was also partially supported by the Japan Science and Technology Agency Basic Research Programs. We are grateful for the support of the Global Center of Excellence Program of Hokkaido University.

Author information

Authors and Affiliations

  1. Laboratory of Microbiology, Department of Disease Control, Graduate School of Veterinary Medicine, Hokkaido University, Kita 18 Nishi 9, Kita-ku, Sapporo, 060-0818, Japan

    Masatoshi Okamatsu, Tatsuya Nishi, Naoki Nomura, Naoki Yamamoto, Yoshihiro Sakoda & Hiroshi Kida

  2. OIE Regional Representation for Asia and the Pacific, The University of Tokyo, Food Science Building 5F, 1-1-1 Yayoi, Bunkyo-ku, Tokyo, 113-8657, Japan

    Kenji Sakurai

  3. Ministry of Agriculture and Rural Development, 15/78 Giaiphong, Phuongmai, Dongda, Hanoi, Vietnam

    Huy Duc Chu, Long Pham Thanh, Long Van Nguyen, Nam Van Hoang & Tien Ngoc Tien

  4. Research Center for Zoonosis Control, Hokkaido University, Kita 20 Nishi 10, Kita-ku, Sapporo, 001-0020, Japan

    Reiko Yoshida, Ayato Takada & Hiroshi Kida

Authors
  1. Masatoshi Okamatsu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tatsuya Nishi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Naoki Nomura
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Naoki Yamamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yoshihiro Sakoda
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kenji Sakurai
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Huy Duc Chu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Long Pham Thanh
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Long Van Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Nam Van Hoang
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Tien Ngoc Tien
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Reiko Yoshida
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Ayato Takada
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Hiroshi Kida
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hiroshi Kida.

Electronic supplementary material

Below is the link to the electronic supplementary material.

11262_2013_954_MOESM1_ESM.pptx

Phylogenetic trees for the PB2, PB1, PA, NP, M, and NS genes of influenza viruses. Nucleotides 1,652–1,895 (244 bp) of PB2, 1,363–1,610 (248 bp) of PB1, 1,190–1,446 (257 bp) of PA, 1,188–1,434 (247 bp) of NP, 52–666 (615 bp) of M, and 46–284 (239 bp) of NS were used for ML phylogenetic analysis. Horizontal distances are proportional to the minimum number of nucleotide differences required to join nodes and sequences. Numbers at each node indicate the confidence level in a bootstrap analysis with 1,000 replications. Representative viruses isolated in the present study are marked by black circle (North) or triangle (South) and the representative of each sublineage are shown in bold. Supplementary material 1 (PPTX 166 kb)

Supplementary material 2 (XLS 77 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Okamatsu, M., Nishi, T., Nomura, N. et al. The genetic and antigenic diversity of avian influenza viruses isolated from domestic ducks, muscovy ducks, and chickens in northern and southern Vietnam, 2010–2012. Virus Genes 47, 317–329 (2013). https://doi.org/10.1007/s11262-013-0954-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11262-013-0954-7

Keywords

Search

Navigation