Skip to main content
SpringerLink
Log in

Characterization of H3 subtype avian influenza viruses isolated from poultry in Vietnam

  • Original Paper
  • Published:
Virus Genes Aims and scope Submit manuscript

Abstract

To date, avian influenza viruses (AIVs) have persisted in domestic poultry in wet markets in East Asian countries. We have performed ongoing virus surveillance in poultry populations in Vietnam since 2011, with the goal of controlling avian influenza. Throughout this study, 110 H3 AIVs were isolated from 2760 swab samples of poultry in markets and duck farms. H3 hemagglutinin (HA) genes of the isolates were phylogenetically classified into eight groups (I–VIII). Genetic diversity was also observed in the other seven gene segments. Groups I–IV also included AIVs from wild waterbirds. The epidemic strains in poultry switched from groups I–III and VI to groups I, IV, V, and VIII around 2013. H3 AIVs in groups I and V were maintained in poultry until at least 2016, which likely accompanied their dissemination from the northern to the southern regions of Vietnam. Groups VI–VIII AIVs were antigenically distinct from the other groups. Some H3 AIV isolates had similar N6 neuraminidase and matrix genes as H5 highly pathogenic avian influenza viruses (HPAIVs). These results reveal that genetically and antigenically different H3 AIVs have been co-circulating in poultry in Vietnam. Poultry is usually reared outside in this country and is at risk of infection with wild waterbird-originating AIVs. In poultry flocks, the intruded H3 AIVs must have experienced antigenic drift/shift and genetic reassortment, which could contribute to the emergence of H5 HPAIVs with novel gene constellations.

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

Similar content being viewed by others

References

  1. Alexander DJ (1982) Ecological aspects of influenza A viruses in animals and their relationship to human influenza: a review. J R Soc Med 75:799–811

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Asha K, Kumar B (2019) Emerging influenza D virus threat: what we know so far! J Clin Med. https://doi.org/10.3390/jcm8020192

    Article  PubMed  PubMed Central  Google Scholar 

  3. Hause BM, Collin EA, Liu R, Huang B, Sheng Z, Lu W, Wang D, Nelson EA, Li F (2014) Characterization of a novel influenza virus in cattle and swine: proposal for a new genus in the orthomyxoviridae family. MBio 5:e00031

    Article  Google Scholar 

  4. Fouchier RA, Munster V, Wallensten A, Bestebroer TM, Herfst S, Smith D, Rimmelzwaan GF, Olsen B, Osterhaus AD (2005) Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J Virol 79:2814–2822

    Article  CAS  Google Scholar 

  5. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y (1992) Evolution and ecology of influenza A viruses. Microbiol Rev 56:152–179

    Article  CAS  Google Scholar 

  6. Wu Y, Wu Y, Tefsen B, Shi Y, Gao GF (2014) Bat-derived influenza-like viruses H17N10 and H18N11. Trends Microbiol 22:183–191

    Article  CAS  Google Scholar 

  7. Kida H, Kawaoka Y, Naeve CW, Webster RG (1987) Antigenic and genetic conservation of H3 influenza virus in wild ducks. Virology 159:109–119

    Article  CAS  Google Scholar 

  8. Cui H, Shi Y, Ruan T, Li X, Teng Q, Chen H, Yang J, Liu Q, Li Z (2016) Phylogenetic analysis and pathogenicity of H3 subtype avian influenza viruses isolated from live poultry markets in China. Sci Rep 6:27360

    Article  CAS  Google Scholar 

  9. Bean WJ, Schell M, Katz J, Kawaoka Y, Naeve C, Gorman O, Webster RG (1992) Evolution of the H3 influenza virus hemagglutinin from human and nonhuman hosts. J Virol 66:1129–1138

    Article  CAS  Google Scholar 

  10. Ito K, Igarashi M, Miyazaki Y, Murakami T, Iida S, Kida H, Takada A (2011) Gnarled-trunk evolutionary model of influenza A virus hemagglutinin. PLoS ONE 6:e25953

    Article  CAS  Google Scholar 

  11. Laver WG, Air GM, Webster RG (1981) Mechanism of antigenic drift in influenza virus. Amino acid sequence changes in an antigenically active region of Hong Kong (H3N2) influenza virus hemagglutinin. J Mol Biol 145:339–361

    Article  CAS  Google Scholar 

  12. Anthony SJ, St Leger JA, Pugliares K, Ip HS, Chan JM, Carpenter ZW, Navarrete-Macias I, Sanchez-Leon M, Saliki JT, Pedersen J, Karesh W, Daszak P, Rabadan R, Rowles T, Lipkin WI (2012) Emergence of fatal avian influenza in New England harbor seals. MBio 3:e00166

    Article  CAS  Google Scholar 

  13. Crawford PC, Dubovi EJ, Castleman WL, Stephenson I, Gibbs EP, Chen L, Smith C, Hill RC, Ferro P, Pompey J, Bright RA, Medina MJ, Johnson CM, Olsen CW, Cox NJ, Klimov AI, Katz JM, Donis RO (2005) Transmission of equine influenza virus to dogs. Science 310:482–485

    Article  CAS  Google Scholar 

  14. Guo Y, Wang M, Kawaoka Y, Gorman O, Ito T, Saito T, Webster RG (1992) Characterization of a new avian-like influenza A virus from horses in China. Virology 188:245–255

    Article  CAS  Google Scholar 

  15. Olsen CW (2002) The emergence of novel swine influenza viruses in North America. Virus Res 85:199–210

    Article  CAS  Google Scholar 

  16. Takemae N, Parchariyanon S, Damrongwatanapokin S, Uchida Y, Ruttanapumma R, Watanabe C, Yamaguchi S, Saito T (2008) Genetic diversity of swine influenza viruses isolated from pigs during 2000 to 2005 in Thailand. Influenza Other Respir Viruses 2:181–189

    Article  Google Scholar 

  17. Campitelli L, Fabiani C, Puzelli S, Fioretti A, Foni E, De Marco A, Krauss S, Webster RG, Donatelli I (2002) H3N2 influenza viruses from domestic chickens in Italy: an increasing role for chickens in the ecology of influenza? J Gen Virol 83:413–420

    Article  CAS  Google Scholar 

  18. Choi YK, Seo SH, Kim JA, Webby RJ, Webster RG (2005) Avian influenza viruses in Korean live poultry markets and their pathogenic potential. Virology 332:529–537

    Article  CAS  Google Scholar 

  19. Liu M, He S, Walker D, Zhou N, Perez DR, Mo B, Li F, Huang X, Webster RG, Webby RJ (2003) The influenza virus gene pool in a poultry market in South central china. Virology 305:267–275

    Article  CAS  Google Scholar 

  20. Pu J, Zhang GZ, Ma JH, Xia YJ, Liu QF, Jiang ZL, Wang Z, Brown EG, Tian FL, Liu JH (2009) Serologic evidence of prevalent avian H3 subtype influenza virus infection in chickens. Avian Dis 53:198–204

    Article  Google Scholar 

  21. Choi JG, Kang HM, Kim MC, Paek MR, Kim HR, Kim BS, Kwon JH, Kim JH, Lee YJ (2012) Genetic relationship of H3 subtype avian influenza viruses isolated from domestic ducks and wild birds in Korea and their pathogenic potential in chickens and ducks. Vet Microbiol 155:147–157

    Article  CAS  Google Scholar 

  22. Li X, Yang J, Liu B, Jia Y, Guo J, Gao X, Weng S, Yang M, Wang L, Wang LF, Cui J, Chen H, Zhu Q (2016) Co-circulation of H5N6, H3N2, H3N8, and emergence of novel reassortant H3N6 in a local community in Hunan Province in China. Sci Rep 6:25549

    Article  CAS  Google Scholar 

  23. Brooks-Moizer F, Roberton SI, Edmunds K, Bell D (2009) Avian influenza H5N1 and the wild bird trade in Hanoi Vietnam. Ecol Soc. https://doi.org/10.5751/ES-02760-140128

    Article  Google Scholar 

  24. Nguyen LT, Firestone SM, Stevenson MA, Young ND, Sims LD, Chu DH, Nguyen TN, Van Nguyen L, Le Thanh T, Van Nguyen H, Nguyen HN, Tien TN, Nguyen TD, Tran BN, Matsuno K, Okamatsu M, Kida H, Sakoda Y (2019) A systematic study towards evolutionary and epidemiological dynamics of currently predominant H5 highly pathogenic avian influenza viruses in Vietnam. Sci Rep 9:7723

    Article  Google Scholar 

  25. Chu DH, Okamatsu M, Matsuno K, Hiono T, Ogasawara K, Nguyen LT, Van Nguyen L, Nguyen TN, Nguyen TT, Van Pham D, Nguyen DH, Nguyen TD, To TL, Van Nguyen H, Kida H, Sakoda Y (2016) Genetic and antigenic characterization of H5, H6 and H9 avian influenza viruses circulating in live bird markets with intervention in the center part of Vietnam. Vet Microbiol 192:194–203

    Article  Google Scholar 

  26. Kim KI, Choi JG, Kang HM, To TL, Nguyen TD, Song BM, Hong MS, Choi KS, Kye SJ, Kim JY, Lee HS, Lee YJ (2013) Geographical distribution of low pathogenic avian influenza viruses of domestic poultry in Vietnam and their genetic relevance with Asian isolates. Poult Sci 92:2012–2023

    Article  Google Scholar 

  27. Okamatsu M, Nishi T, Nomura N, Yamamoto N, Sakoda Y, Sakurai K, Chu HD, Thanh LP, Van Nguyen L, Van Hoang N, Tien TN, Yoshida R, Takada A, Kida H (2013) 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

    Article  CAS  Google Scholar 

  28. Takakuwa H, Yamashiro T, Le MQ, Phuong LS, Ozaki H, Tsunekuni R, Usui T, Ito H, Morimatsu M, Tomioka Y, Yamaguchi T, Ito T, Murase T, Ono E, Otsuki K (2012) Molecular epidemiology of avian influenza viruses circulating among healthy poultry flocks in farms in northern Vietnam. Prev Vet Med 103:192–200

    Article  Google Scholar 

  29. Kida H, Yangawa R (1979) Isolation and characterization of influenza a viruses from wild free-flying ducks in Hokkaido, Japan. Zentralbl Bakteriol [Orig A] 244:135–143

    CAS  Google Scholar 

  30. Lee MS, Chang PC, Shien JH, Cheng MC, Shieh HK (2001) Identification and subtyping of avian influenza viruses by reverse transcription-PCR. J Virol Methods 97:13–22

    Article  CAS  Google Scholar 

  31. Tsukamoto K, Ashizawa H, Nakanishi K, Kaji N, Suzuki K, Okamatsu M, Yamaguchi S, Mase M (2008) Subtyping of avian influenza viruses H1 to H15 on the basis of hemagglutinin genes by PCR assay and molecular determination of pathogenic potential. J Clin Microbiol 46:3048–3055

    Article  CAS  Google Scholar 

  32. Tsukamoto K, Ashizawa T, Nakanishi K, Kaji N, Suzuki K, Shishido M, Okamatsu M, Mase M (2009) Use of reverse transcriptase PCR to subtype N1 to N9 neuraminidase genes of avian influenza viruses. J Clin Microbiol 47:2301–2303

    Article  CAS  Google Scholar 

  33. Hoffmann E, Stech J, Guan Y, Webster RG, Perez DR (2001) Universal primer set for the full-length amplification of all influenza A viruses. Arch Virol 146:2275–2289

    Article  CAS  Google Scholar 

  34. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  Google Scholar 

  35. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  Google Scholar 

  36. Underwood PA (1982) Mapping of antigenic changes in the haemagglutinin of Hong Kong influenza (H3N2) strains using a large panel of monoclonal antibodies. J Gen Virol 62(Pt 1):153–169

    Article  CAS  Google Scholar 

  37. Tian H, Zhou S, Dong L, Van Boeckel TP, Cui Y, Newman SH, Takekawa JY, Prosser DJ, Xiao X, Wu Y, Cazelles B, Huang S, Yang R, Grenfell BT, Xu B (2015) Avian influenza H5N1 viral and bird migration networks in Asia. Proc Natl Acad Sci USA 112:172–177

    Article  CAS  Google Scholar 

  38. Koehler AV, Pearce JM, Flint PL, Franson JC, Ip HS (2008) Genetic evidence of intercontinental movement of avian influenza in a migratory bird: the northern pintail (Anas acuta). Mol Ecol 17:4754–4762

    Article  Google Scholar 

  39. Si Y, Skidmore AK, Wang T, de Boer WF, Debba P, Toxopeus AG, Li L, Prins HH (2009) Spatio-temporal dynamics of global H5N1 outbreaks match bird migration patterns. Geospat Health 4:65–78

    Article  Google Scholar 

  40. Zost SJ, Parkhouse K, Gumina ME, Kim K, Diaz Perez S, Wilson PC, Treanor JJ, Sant AJ, Cobey S, Hensley SE (2017) Contemporary H3N2 influenza viruses have a glycosylation site that alters binding of antibodies elicited by egg-adapted vaccine strains. Proc Natl Acad Sci USA 114:12578–12583

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This was a collaborative research effort between the National Institute of Hygiene and Epidemiology (Vietnam), Nagasaki University (Japan), and Tottori University (Japan). This research was supported by AMED under Grant Number JP19fm0108001 (Japan Initiative for Global Research Network on Infectious Diseases (J-GRID)), and in part by a grant from MEXT for the Joint Research Program of the Research Center for Zoonosis Control, Hokkaido University, Japan.

Author information

Authors and Affiliations

  1. Department of Joint Veterinary Medicine, Faculty of Agriculture, Tottori University, 4-101 Koyama-Minami, Tottori, 680-8553, Japan

    Kosuke Soda, Mina Kashiwabara, Hiroshi Ito & Toshihiro Ito

  2. Faculty of Agriculture, Avian Zoonosis Research Center, Tottori University, 4-101 Koyama-Minami, Tottori, 680-8553, Japan

    Kosuke Soda, Hiroshi Ito & Toshihiro Ito

  3. Vietnam Research Station, Nagasaki University, c/o National Institute of Hygiene and Epidemiology, No. 1 Yersin Street, Hanoi, Vietnam

    Kozue Miura

  4. Department of Virology, National Institute of Hygiene and Epidemiology, No. 1 Yersin Street, Hanoi, Vietnam

    Trang T. H. Ung, Hang L. K. Nguyen & Mai Q. Le

Authors
  1. Kosuke Soda
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mina Kashiwabara
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kozue Miura
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Trang T. H. Ung
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hang L. K. Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hiroshi Ito
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mai Q. Le
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Toshihiro Ito
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

KS (first author) was responsible for the conception and design of the study, the acquisition, collation, and interpretation of the data, and the writing of the submitted article. MK was involved in the phylogenic/antigenic analyses and the animal infection experiment. KH, TTHU., and HLKN performed the virus surveillance and isolation study. HI, MQL, and TI (corresponding author) were involved in the coordination of the study, the import formality (Vietnam to Japan), and the submission process.

Corresponding author

Correspondence to Toshihiro Ito.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Edited by Simon D. Scott.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 10 kb)

Supplementary file2 (PDF 110 kb)

Fig. S1 Phylogenetic trees of the N2 NA (A), N3 NA (B), N8 NA (C), PB2 (D), PB1 (E), PA (F), NP (G), and NS (H) gene segments of H3 AIV. The H3 virus isolates in our surveillance in Vietnam are shown in red. Wildfowl-originating viruses and H5 HPAIVs are shown in green and blue, respectively. The compressed taxa on the tree are shown by the italicized common denominators. The reference strains used for antigenic analysis in the present study are marked with filled circles. The partial sequences of each segment indicated in Table S1 were used for the analysis. Horizontal distances are proportional to the minimum number of nucleotide differences required to join the nodes and sequences. Numbers at the nodes indicate confidence levels in a bootstrap analysis with 1,000 replications. Bootstrap values of more than 60% are shown at each branch. The strains together with the virus isolates sharing a distinct common node [shown via asterisks (*)] were assumed to be within the same group.

Fig. S2 Alignment of the deduced H3 HA amino acid sequences of the strains used for antigenic analysis (H3 HA numbering). Group numbers are based on the H3 HA gene phylogeny (Fig. 1A). Amino acids constituting five antigenic sites (A—E) are boxed. Amino acid residues different from those in the group I LBM48 strain are shown in red.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Soda, K., Kashiwabara, M., Miura, K. et al. Characterization of H3 subtype avian influenza viruses isolated from poultry in Vietnam. Virus Genes 56, 712–723 (2020). https://doi.org/10.1007/s11262-020-01797-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11262-020-01797-7

Keywords

Search

Navigation