Archives of Virology

, Volume 164, Issue 2, pp 457–472 | Cite as

Genetic and antigenic dynamics of influenza A viruses of swine on pig farms in Thailand

  • Junki Mine
  • Haruka Abe
  • Sujira Parchariyanon
  • Prakit Boonpornprasert
  • Namfon Ubonyaem
  • Bandit Nuansrichay
  • Nobuhiro Takemae
  • Taichiro Tanikawa
  • Ryota Tsunekuni
  • Yuko Uchida
  • Takehiko SaitoEmail author
Original Article


Surveillance studies of influenza A virus of swine (IAV-S) have accumulated information regarding IAVs-S circulating in Thailand, but how IAVs-S evolve within a farm remains unclear. In the present study, we isolated 82 A(H1N1)pdm09 and 87 H3N2 viruses from four farms from 2011 through 2017. We then phylogenetically and antigenically analyzed the isolates to elucidate their evolution within each farm. Phylogenetic analysis demonstrated multiple introductions of A(H1N1)pdm09 viruses that resembled epidemic A(H1N1)pdm09 strains in humans in Thailand, and they reassorted with H3N2 viruses as well as other A(H1N1)pdm09 viruses. Antigenic analysis revealed that the viruses had acquired antigenic diversity either by accumulating substitutions in the hemagglutinin protein or through the introduction of IAV-S strains with different antigenicity. Our results, obtained through continuous longitudinal surveillance, revealed that IAV-S can be maintained on a pig farm over several years through the generation of antigenic diversity due to the accumulation of mutations, introduction of new strains, and reassortment events.



All antisera raised against human H3N2 viruses, the homologous inactivated antigens, and A/Narita/1/2009 were kindly provided by the National Institute of Infectious Diseases, Japan; A/California/04/2009 was kindly provided by the Centers for Disease Control and Prevention, USA. We thank the staff of the National Institute of Animal Health, Thailand, for arranging and supporting our collection of pig swab samples in Thailand. All of the analyses involving the BEAST software package were conducted by using the supercomputer of AFFRIT, MAFF, Japan. The current research was supported by the Japan Initiative for Global Research Network on Infectious Diseases (J-GRID) from the Ministry of Education, Culture, Sports, Science, and Technology in Japan and by the Japan Agency for Medical Research and Development (AMED) under grant number JP18fm0108008.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Ethics statement

This article does not contain any studies involving human participants or live animals that were performed by any of the authors.

Supplementary material

705_2018_4091_MOESM1_ESM.pptx (85 kb)
Supplementary material 1 (PPTX 85 kb)
705_2018_4091_MOESM2_ESM.pptx (584 kb)
Fig. S1 Detail of a maximum-likelihood phylogenetic tree of isolates from this study that display H1 HA genes and those originating from A(H1N1)pdm09 viruses between 2009 and 2013. IAVs isolated in 2009 and 2010 are shown in light blue; those isolated in 2011 and 2012 are in dark blue. Genetic groups 3.3.2a, 3.3.2b, and 3.3.2c are all shown in green. Bootstrap values at the root of each genetic group are indicated by red squares. Fig. S2 Detail of a maximum-likelihood phylogenetic tree of the H3 HA genes displayed by the H3N2 isolates, human-like a and human-like b clusters, in this study. The genetic group human-like a is in green, and human-like b is in yellow. Bootstrap values at the root of each genetic group are indicated by red squares. Fig. S3 Maximum-likelihood phylogenetic tree (a) and MCC phylogenetic tree (b) of the N2 NA genes displayed by the H3N2 isolates in this study. The genetic group human-like a is in green. In (a), bootstrap values at the root of each genetic group are indicated by red squares. Strain names of isolates from farms B, C, D, and O are shown in red, orange, blue, and purple, respectively in (b). Fig. S4. Maximum-likelihood phylogenetic tree (a), MCC phylogenetic trees (b–d), and part of the maximum-likelihood phylogenetic tree (e) of the PB1 genes of the isolates in this study. IAVs-S isolated in 2009 and 2010 are shown in lines colored with light blue; those from 2011 and 2012 are in dark blue; isolates from 2013 and 2014 are pink; and those from 2015 and 2016 are red. The genetic groups 3.3.2a, 3.3.2b, and 3.3.2c are all in green. Bootstrap values of the root of each genetic group are indicated by red squares (a). The genetic groups 3.3.2a, 3.3.2b, and 3.3.2c are colored light red (b), pink (c), and blue (d), respectively. Strain names of isolates from farms B, C, D, and O are shown in red, orange, blue, and purple, respectively. Gray boxes indicate the divergence time estimated using BEAST. The genetic group 3.3.2c of PB1 genes is colored in light blue (e). Fig. S5 Part of the maximum-likelihood phylogenetic tree of the MP genes, including the isolates in this study. The genetic group 3.3.2c of MP genes is in light blue. Fig. S6 Maximum-likelihood phylogenetic tree (a), detail of the maximum-likelihood phylogenetic tree (b), and MCC phylogenetic trees (c) of NP genes, including the isolates in this study. IAVs isolated in 2009 and 2010 are shown in lines colored with light blue; those of 2011 and 2012 are in dark blue; viruses from 2013 and 2014 are in pink; and those of 2015 and 2016 are red. In (a), the genetic groups 3.3.2ab and 3.3.2c are both green. In (b), the genetic group 3.3.2c of NP genes is light blue. In (c), the genetic group 3.3.2ab is colored bright purple. Strain names of isolates from farms B, C, D, and O are shown in red, orange, blue, and purple, respectively. (PPTX 584 kb)


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Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  • Junki Mine
    • 1
    • 2
  • Haruka Abe
    • 1
    • 2
  • Sujira Parchariyanon
    • 3
  • Prakit Boonpornprasert
    • 3
  • Namfon Ubonyaem
    • 3
  • Bandit Nuansrichay
    • 3
  • Nobuhiro Takemae
    • 1
    • 2
  • Taichiro Tanikawa
    • 1
    • 2
  • Ryota Tsunekuni
    • 1
    • 2
  • Yuko Uchida
    • 1
    • 2
  • Takehiko Saito
    • 1
    • 2
    Email author
  1. 1.Division of Transboundary DiseasesNational Institute of Animal Health, National Agriculture and Food Research Organization (NARO)TsukubaJapan
  2. 2.Thailand-Japan Zoonotic Diseases Collaboration CenterBangkokThailand
  3. 3.National Institute of Animal HealthBangkokThailand

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