Skip to main content

Advertisement

SpringerLink
Log in

Antigenic variation of H1N1, H1N2 and H3N2 swine influenza viruses in Japan and Vietnam

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

The antigenicity of the influenza A virus hemagglutinin is responsible for vaccine efficacy in protecting pigs against swine influenza virus (SIV) infection. However, the antigenicity of SIV strains currently circulating in Japan and Vietnam has not been well characterized. We examined the antigenicity of classical H1 SIVs, pandemic A(H1N1)2009 (A(H1N1)pdm09) viruses, and seasonal human-lineage SIVs isolated in Japan and Vietnam. A hemagglutination inhibition (HI) assay was used to determine antigenic differences that differentiate the recent Japanese H1N2 and H3N2 SIVs from the H1N1 and H3N2 domestic vaccine strains. Minor antigenic variation between pig A(H1N1)pdm09 viruses was evident by HI assay using 13 mAbs raised against homologous virus. A Vietnamese H1N2 SIV, whose H1 gene originated from a human strain in the mid-2000s, reacted poorly with post-infection ferret serum against human vaccine strains from 2000-2010. These results provide useful information for selection of optimal strains for SIV vaccine production.

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.

Fig. 1

Similar content being viewed by others

References

  1. Olsen CW, Brown IH, Easterday BC, Van Reeth K (2006) Swine influenza. In: Straw DJ, Zimmerman JJ, d’Alaaire S, Taylor DJ (eds) Diseases of swine, 9th edn. Blackwell Publishing, Oxford, pp 469–482

    Google Scholar 

  2. Bennett R, Ijpelaar J (2005) Updated estimates of the costs associated with thirty four endemic livestock diseases in Great Britain: A note. J Agr Econ 56(1):135–144. doi:10.1111/j.1477-9552.2005.tb00126.x

    Article  Google Scholar 

  3. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y (1992) Evolution and ecology of influenza A viruses. Microbiol Rev 56(1):152–179. doi:0146-0749/92/010152-28$02.00/0

    PubMed  CAS  Google Scholar 

  4. Scholtissek C, Burger H, Bachmann PA, Hannoun C (1983) Genetic relatedness of hemagglutinins of the H1 subtype of influenza a viruses isolated from swine and birds. Virology 129(2):521–523. doi:10.1016/0042-6822(83)90194-0

    Article  PubMed  CAS  Google Scholar 

  5. Brown IH, Harris PA, McCauley JW, Alexander DJ (1998) Multiple genetic reassortment of avian and human influenza A viruses in European pigs, resulting in the emergence of an H1N2 virus of novel genotype. J Gen Virol 79(12):2947–2955

    PubMed  CAS  Google Scholar 

  6. Webby RJ, Swenson SL, Krauss SL, Gerrish PJ, Goyal SM, Webster RG (2000) Evolution of swine H3N2 influenza viruses in the United States. J Virol 74(18):8243–8251. doi:10.1128/jvi.74.18.8243-8251.2000

    Article  PubMed  CAS  Google Scholar 

  7. Vijaykrishna D, Poon LLM, Zhu HC, Ma SK, Li OTW, Cheung CL, Smith GJD, Peiris JSM, Guan Y (2010) Reassortment of pandemic H1N1/2009 influenza A virus in swine. Science 328(5985):1529. doi:10.1126/science.1189132

    Article  PubMed  CAS  Google Scholar 

  8. Howden KJ, Brockhoff EJ, Caya FD, McLeod LJ, Lavoie M, Ing JD, Bystrom JM, Alexandersen S, Pasick JM, Berhane Y, Morrison ME, Keenliside JM, Laurendeau S, Rohonczy EB (2009) An investigation into human pandemic influenza virus (H1N1) 2009 on an Alberta swine farm. Can Vet J 50(11):1153–1161

    PubMed  Google Scholar 

  9. Starick E, Lange E, Grund C, Grosse Beilage E, Dohring S, Maas A, Noe T, Beer M, Harder TC (2012) Reassortants of pandemic influenza A virus H1N1/2009 and endemic porcine HxN2 viruses emerge in swine populations in Germany. J Gen Virol 93:1658–1663. doi:10.1099/vir.0.042648-0

    Article  PubMed  CAS  Google Scholar 

  10. Fan X, Zhu H, Zhou B, Smith DK, Chen X, Lam TTY, Poon LLM, Peiris M, Guan Y (2012) Emergence and dissemination of a swine H3N2 reassortant influenza virus with 2009 pandemic H1N1 genes in pigs in China. J Virol 86(4):2375–2378. doi:10.1128/jvi.06824-11

    Article  PubMed  CAS  Google Scholar 

  11. Sugimura T, Yonemochi H, Ogawa T, Tanaka Y, Kumagai T (1980) Isolation of a recombinant influenza virus (Hsw 1 N2) from swine in Japan. Arch Virol 66(3):271–274. doi:10.1007/BF01314741

    Article  PubMed  CAS  Google Scholar 

  12. Nerome K, Sakamoto S, Yano N, Yamamoto T, Kobayashi S, Webster RG, Oya A (1983) Antigenic characteristics and genome composition of a naturally occurring recombinant influenza virus isolated from a pig in Japan. J Gen Virol 64(12):2611–2620. doi:10.1099/0022-1317-64-12-2611

    Article  PubMed  CAS  Google Scholar 

  13. Saito T, Suzuki H, Maeda K, Inai K, Takemae N, Uchida Y (2006) Tsunemitsu H (2008) Molecular characterization of an H1N2 swine influenza virus isolated in Miyazaki, Japan, in. J Vet Med Sci 70(4):423–427. doi:10.1292/jvms.70.423

    Article  Google Scholar 

  14. Saito T, Takemae N, Uchida Y, Hiromoto Y, Hayashi T (2010) Evolutional analysis of swine influenza virus in Japan. Paper presented at the XIV International Conference on Negative Strand Viruses, Brugge, Belgium, pp 20–25

    Google Scholar 

  15. Ngo LT, Hiromoto Y, Pham V, Le HT, Nguyen HT, Le VT, Takemae N, Saito T (201) Isolation of novel triple-reassortant swine H3N2 influenza viruses possessing the hemagglutinin and neuraminidase genes of a seasonal influenza virus in Vietnam in 2010. Influenza Other Respi Viruses 6(1):6–10. doi:10.1111/j.1750-2659.2011.00267.x

    Article  Google Scholar 

  16. Ma W, Richt AJ (2010) Swine influenza vaccines: current status and future perspectives. Anim Health Res Rev 11:81–96. doi:10.1017/S146625231000006X

    Article  PubMed  Google Scholar 

  17. Van Reeth K, Brown I, Essen S, Pensaert M (2004) Genetic relationships, serological cross-reaction and cross-protection between H1N2 and other influenza A virus subtypes endemic in European pigs. Virus Res 103(1–2):115–124. doi:10.1016/j.virusres.2004.02.023

    Article  PubMed  Google Scholar 

  18. Van Reeth K, De Clercq S, Pensaert M (2001) Lack of cross-protection between European H1N1 and H1N2 swine influenza viruses. Int Congr 1219:341–345. doi:10.1016/S0531-5131(01)00345-4

    Article  Google Scholar 

  19. Daidoji T, Koma T, Du A, Yang C-S, Ueda M, Ikuta K, Nakaya T (2008) H5N1 avian influenza virus induces apoptotic cell death in mammalian airway epithelial cells. J Virol 82(22):11294–11307. doi:10.1128/jvi.01192-08

    Article  PubMed  CAS  Google Scholar 

  20. Takemae N, Parchariyanon S, Ruttanapumma R, Hiromoto Y, Hayashi T, Uchida Y, Saito T (2011) Swine influenza virus infection in different age groups of pigs in farrow-to-finish farms in Thailand. Virol J 8(1):537. doi:10.1186/1743-422X-8-537

    Article  PubMed  Google Scholar 

  21. 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 Respi Viruses 2(5):181–189. doi:10.1111/j.1750-2659.2008.00062.x

    Article  PubMed  Google Scholar 

  22. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp 41:95–98

    CAS  Google Scholar 

  23. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739. doi:10.1093/molbev/msr121

    Article  PubMed  CAS  Google Scholar 

  24. Igarashi M, Ito K, Yoshida R, Tomabechi D, Kida H, Takada A (2010) Predicting the Antigenic Structure of the Pandemic (H1N1) 2009 Influenza Virus Hemagglutinin. PLoS ONE 5(1):e8553. doi:10.1371/journal.pone.0008553

    Article  PubMed  Google Scholar 

  25. Wiley DC, Skehel JJ (1987) The Structure and Function of the Hemagglutinin Membrane Glycoprotein of Influenza Virus. Annu Rev Biochem 56(1):365–394. doi:10.1146/annurev.bi.56.070187.002053

    Article  PubMed  CAS  Google Scholar 

  26. Loeffen WLA, Stockhofe N, Weesendorp E, van Zoelen-Bos D, Heutink R, Quak S, Goovaerts D, Heldens JGM, Maas R, Moormann RJ, Koch G (2011) Efficacy of a pandemic (H1N1) 2009 virus vaccine in pigs against the pandemic influenza virus is superior to commercially available swine influenza vaccines. Vet Microbiol 152(3–4):304–314. doi:10.1016/j.vetmic.2011.05.027

    Article  PubMed  CAS  Google Scholar 

  27. Romagosa A, Allerson M, Gramer M, Joo HS, Deen J, Detmer S, Torremorell M (2011) Vaccination of influenza a virus decreases transmission rates in pigs. Vet Res 42:120. doi:10.1186/1297-9716-42-120

    Article  PubMed  CAS  Google Scholar 

  28. Vincent AL, Lager KM, Janke BH, Gramer MR, Richt JA (2008) Failure of protection and enhanced pneumonia with a US H1N2 swine influenza virus in pigs vaccinated with an inactivated classical swine H1N1 vaccine. Vet Microbiol 126(4):310–323. doi:10.1016/j.vetmic.2007.07.011

    Article  PubMed  CAS  Google Scholar 

  29. de Jong JC, van Nieuwstadt AP, Kimman TG, Loeffen WLA, Bestebroer TM, Bijlsma K, Verweij C, Osterhaus ADME, Claas ECJ (1999) Antigenic drift in swine influenza H3 haemagglutinins with implications for vaccination policy. Vaccine 17(11–12):1321–1328. doi:10.1016/S0264-410X(98)00392-2

    PubMed  Google Scholar 

  30. de Jong JC, Smith DJ, Lapedes AS, Donatelli I, Campitelli L, Barigazzi G, Van Reeth K, Jones TC, Rimmelzwaan GF, Osterhaus ADME, Fouchier RAM (2007) Antigenic and Genetic Evolution of Swine Influenza A (H3N2) Viruses in Europe. J Virol 81(8):4315–4322. doi:10.1128/jvi.02458-06

    Article  PubMed  Google Scholar 

  31. Heinen PP, van Nieuwstadt AP, de Boer-Luijtze EA, Bianchi ATJ (2001) Analysis of the quality of protection induced by a porcine influenza A vaccine to challenge with an H3N2 virus. Vet Immunol Immunopathol 82(1–2):39–56. doi:10.1016/s0165-2427(01)00342-7

    Article  PubMed  CAS  Google Scholar 

  32. Van Reeth K, Van Gucht S, Pensaert M (2003) Investigations of the efficacy of European H1N1- and H3N2-based swine influenza vaccines against the novel H1N2 subtype. Vet Rec 153(1):9–13. doi:10.1136/vr.153.1.9

    Article  PubMed  Google Scholar 

  33. Kyriakis CS, Gramer MR, Barbé F, Van Doorsselaere J, Van Reeth K (2010) Efficacy of commercial swine influenza vaccines against challenge with a recent European H1N1 field isolate. Vet Microbiol 144(1–2):67–74. doi:10.1016/j.vetmic.2009.12.039

    Article  PubMed  CAS  Google Scholar 

  34. Webster RG, Thomas TL (1993) Efficacy of equine influenza vaccines for protection against A/Equine/Jilin/89 (H3N8) — A new equine influenza virus. Vaccine 11(10):987–993. doi:10.1016/0264-410x(93)90122-e

    Article  PubMed  CAS  Google Scholar 

  35. Richt JA, Lager KM, Janke BH, Woods RD, Webster RG, Webby RJ (2003) Pathogenic and antigenic properties of phylogenetically distinct reassortant H3N2 swine influenza viruses cocirculating in the United States. J Clin Microbiol 41(7):3198–3205. doi:10.1128/jcm.41.7.3198-3205.2003

    Article  PubMed  Google Scholar 

  36. Gramer MR, Lee JH, Choi YK, Goyal SM, Joo HS (2007) Serologic and genetic characterization of North American H3N2 swine influenza A viruses. Can J Vet Res 71(3):201–206

    PubMed  CAS  Google Scholar 

  37. Nelson M, Gramer M, Vincent A, Holmes EC (2012) Global transmission of influenza viruses from humans to swine. J Gen Virol 93(10):2195–2203. doi:10.1099/vir.0.044974-0

    Article  PubMed  CAS  Google Scholar 

  38. Vincent AL, Ciacci-Zanella JR, Lorusso A, Gauger PC, Zanella EL, Kehrli ME Jr, Janke BH, Lager KM (2010) Efficacy of inactivated swine influenza virus vaccines against the 2009 A/H1N1 influenza virus in pigs. Vaccine 28(15):2782–2787. doi:10.1016/j.vaccine.2010.01.049

    Article  PubMed  CAS  Google Scholar 

  39. Lorusso A, Vincent AL, Harland ML, Alt D, Bayles DO, Swenson SL, Gramer MR, Russell CA, Smith DJ, Lager KM (2008) Lewis NS (2011) Genetic and antigenic characterization of H1 influenza viruses from United States swine from. J Gen Virol 92(4):919–930. doi:10.1099/vir.0.027557-0

    Article  Google Scholar 

  40. Matsuu A, Uchida Y, Takemae N, MawatariI T, Yoneyama S, Kasai T, Nakamura R, Eto M (2012) Saito T (2012) Genetic characterization of swine influenza viruses isolated in Japan between 2009 and. Microbiol Immunol 56(11):792–803. doi:10.1111/j.1348-0421.2012.00501.x

    Article  PubMed  CAS  Google Scholar 

  41. Lee C, Kang B, Kim H, Park S, Park B, Jung K, Song D (2008) Phylogenetic analysis of swine influenza viruses recently isolated in Korea. Virus Genes 37(2):168–176. doi:10.1007/s11262-008-0251-z

    Article  PubMed  CAS  Google Scholar 

  42. Ministry of Agriculture Forestry and Fisheries, Japan (2011) STATISTICAL YEARBOOK OF MINISTRY OF AGRICULTURE, FORESTRY AND FISHERIES. http://www.maff.go.jp/j/tokei/kouhyou/tikusan/index.html. Accessed 2012/11/19

  43. National Veterinary Assay Laboratory (2012) http://www.maff.go.jp/nval/kentei_kensa/index.html. Accessed 2012/11/16

  44. Van Reeth K, Labarque G, Clercq SD, Pensaert M (2001) Efficacy of vaccination of pigs with different H1N1 swine influenza viruses using a recent challenge strain and different parameters of protection. Vaccine 19(31):4479–4486. doi:10.1016/s0264-410x(01)00206-7

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank Drs. Y.-K. Choi, Chungbuk National University, Republic of Korea; N. Cox, Centers for Disease Control and Prevention, USA; H. Kida and Y. Sakoda, Hokkaido University, Japan; K. V. Reeth, Ghent University, Belgium; and R. Saito, Niigata University, Japan, for providing viruses; Drs. M. Tashiro and T. Odagiri, National Institute of Infectious Diseases, Japan, for providing a virus, post-infection ferret sera against human vaccine strains and homologous inactivated antigens; and the staffs of the Sub-Department of Animal Health of Ba Ria Vung Tau, Binh Duong, Nam Dinh, and Tien Giang provinces in Vietnam for coordinating and supporting pig swab collection in Vietnam. This work was supported in part by a program of the Japan Initiative for Global Research Network on Infectious Diseases (J-GRID) of the Ministry of Education, Culture, Sports, Science, and Technology (MEXT) of Japan, and by a grant from the Zoonoses Control Project of the Ministry of Agriculture, Forestry and Fisheries of Japan.

Author information

Authors and Affiliations

  1. Thailand-Japan Zoonotic Diseases Collaboration Center, Kasetklang, Chatuchak, Bangkok, 10900, Thailand

    Nobuhiro Takemae, Yasuaki Hiromoto, Yuko Uchida, Tsuyoshi Hayashi, Aya Matsuu & Takehiko Saito

  2. Viral Disease and Epidemiology Research Division, National Institute of Animal Health, National Agriculture and Food Research Organization (NARO), 3-1-5 Kannondai, Tsukuba, Ibaraki, 305-0856, Japan

    Nobuhiro Takemae, Yasuaki Hiromoto, Yuko Uchida, Tsuyoshi Hayashi, Aya Matsuu & Takehiko Saito

  3. National Centre for Veterinary Diagnostics, 11/78 Giai Phong, Phuong Mai, Dong Da, Hanoi, Vietnam

    Tung Nguyen, Hoa Thi Do & Dang Hoang Nguyen

  4. Center for Veterinary Diagnostics, Regional Animal Health Office No. 6, 521/ 1 Hoang Van Thu St., Ward 4, Tan Binh District, Ho Chi Minh City, Vietnam

    Long Thanh Ngo, Vu Phong Pham, Vu Tri Le & Hung Van Vo

  5. Influenza Virus Research Center, National Institute of Infectious Diseases, 4-7-1 Gakuen, Musashi-Murayama, Tokyo, 208-0011, Japan

    Tsutomu Kageyama

  6. Nagano Environmental Conservation Research Institute, 1978 Amorikomemura, Nagano, Nagano, 380-0944, Japan

    Shizuko Kasuo

  7. Saitama Institute of Public Health, 639-1 Kamiokubo, Sakura-ku, Saitama, Saitama, 338-0824, Japan

    Shinichi Shimada

  8. Ehime Prefectural Institute of Public Health and Environmental Science, 8-234 Sanbancho, Matsuyama, Ehime, 790-0003, Japan

    Yasutaka Yamashita

  9. Osaka City Institute of Public Health and Environmental Sciences, 8-34 Tojocho, Tennouji-ku, Osaka, Osaka, 543-0026, Japan

    Kaoru Goto & Hideyuki Kubo

  10. The United Graduate School of Veterinary Sciences, Gifu University, 1-1 Yanagido, Gifu, Gifu, 501-1193, Japan

    Takehiko Saito

Authors
  1. Nobuhiro Takemae
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tung Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Long Thanh Ngo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yasuaki Hiromoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yuko Uchida
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Vu Phong Pham
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tsutomu Kageyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shizuko Kasuo
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Shinichi Shimada
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Yasutaka Yamashita
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Kaoru Goto
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Hideyuki Kubo
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Vu Tri Le
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Hung Van Vo
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Hoa Thi Do
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Dang Hoang Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Tsuyoshi Hayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Aya Matsuu
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Takehiko Saito
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Takehiko Saito.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Takemae, N., Nguyen, T., Ngo, L.T. et al. Antigenic variation of H1N1, H1N2 and H3N2 swine influenza viruses in Japan and Vietnam. Arch Virol 158, 859–876 (2013). https://doi.org/10.1007/s00705-013-1616-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-013-1616-8

Keywords

Search

Navigation