Acta Veterinaria Hungarica
Volume/Issue:
Volume 61: Issue 1
Emergence and characterisation of pandemic H1N1 influenza viruses in Hungarian swine herds
Authors: Ádám Bálint 1 , István Kiss 2 , Krisztián Bányai 3 , Imre Biksi 4 , Katalin Szentpáli-Gavallér 1 , Tibor Magyar 3 , István Jankovics 5 , Mónika Rózsa 5 , Bálint Szalai 5 , Mária Takács 5 , Ádám Tóth 1 , and Ádám Dán 1
View More View Less
  • 1 Central Agricultural Office Veterinary Diagnostic Directorate Tábornok u. 2 H-1149 Budapest Hungary
  • 2 CEVA PHYLAXIA Veterinary Biologicals Co. Ltd Budapest Hungary
  • 3 Hungarian Academy of Sciences Institute for Veterinary Medical Research, Centre for Agricultural Research Budapest Hungary
  • 4 Szent István University Faculty of Veterinary Science Budapest Hungary
  • 5 National Centre for Epidemiology Division of Virology Budapest Hungary
DOI:
https://doi.org/10.1556/avet.2012.059
Page Count:
125–134
Publication Date:
01 Mar 2013
Online Publication Date:
06 Dec 2012
Article Category:
Research Article
Restricted access

Purchase article

USD  $25.00

1 year subscription (Individual Only)

USD  $836.00
Purchase Online Subscription

  • Purchase article

    USD  $25.00

  • 1 year subscription (Individual Only)

    USD  $836.00

In 2010, two novel porcine H1N1 influenza viruses were isolated from pigs with influenza-like illness in Hungarian swine herds. Sequence and phylogenetic analysis of these strains revealed that they shared molecular features with the pandemic H1N1 influenza virus strains, which emerged globally during 2009. The PB2, HA and NA genes contained unique amino acid changes compared to the available new H1N1 influenza virus sequences of pig origin. Furthermore, the investigated strains could be separated with respect to parallel amino acid substitutions affecting the polymerase genes (PB2, PB1 and PA) and the nucleoprotein (NP) gene, supporting the proposed complementarities between these proteins, all required for the viral fitness. Molecular characterisation of two Hungarian human pandemic H1N1 isolates was also performed, so that we could compare contemporaneous strains of different host species origins. Shared molecular motifs in various genes of animal and human influenza strains suggested that the Hungarian porcine strains could have originated from humans through direct interspecies transmission. This study is among the few that support the natural human-to-pig transmission of the pandemic H1N1 influenza virus.

  • Abed, Y., Goyette, N. and Boivin, G. (2005): Generation and characterization of recombinant influenza A (H1N1) viruses harboring amantadine resistance mutations. Antimicrob. Agents Chemother. 49, 556–559.

    Boivin G. , 'Generation and characterization of recombinant influenza A (H1N1) viruses harboring amantadine resistance mutations ' (2005 ) 49 Antimicrob. Agents Chemother. : 556 -559.

    • Search Google Scholar

  • Bálint, Á., Metreveli, G., Widén, F., Zohari, S., Berg, M., Isaksson, M., Renstrom, L. H., Wallgren, P., Belák, S., Segall, T. and Kiss, I. (2009): The first Swedish H1N2 swine influenza virus isolate represents an uncommon reassortant. Virol. J. 6, 180.

    Kiss I. , 'The first Swedish H1N2 swine influenza virus isolate represents an uncommon reassortant ' (2009 ) 6 Virol. J. : 180 -.

    • Search Google Scholar

  • Belser, J. A., Jayaraman, A., Raman, R., Pappas, C., Zeng, H., Cox, N. J., Katz, J. M., Sasisekharan, R. and Tumpey, T. M. (2011): Effect of D222G mutation in the hemagglutinin protein on receptor binding, pathogenesis and transmissibility of the 2009 pandemic H1N1 influenza virus. PLoS One 6, e25091.

    Tumpey T. M. , 'Effect of D222G mutation in the hemagglutinin protein on receptor binding, pathogenesis and transmissibility of the 2009 pandemic H1N1 influenza virus ' (2011 ) 6 PLoS One : e25091 -.

    • Search Google Scholar

  • Bussey, K. A., Bousse, T. L., Desmet, E. A., Kim, B. and Takimoto, T. (2010): PB2 residue 271 plays a key role in enhanced polymerase activity of influenza A viruses in mammalian host cells. J. Virol. 84, 4395–4406.

    Takimoto T. , 'PB2 residue 271 plays a key role in enhanced polymerase activity of influenza A viruses in mammalian host cells ' (2010 ) 84 J. Virol. : 4395 -4406.

    • Search Google Scholar

  • Chen, W., Calvo, P. A., Malide, D., Gibbs, J., Schubert, U., Bacik, I., Basta, S., O’Neill, R., Schickli, J., Palese, P., Henklein, P., Bennink, J. R. and Yewdell, J. W. (2001): A novel influenza A virus mitochondrial protein that induces cell death. Nat. Med. 7, 1306–1312.

    Yewdell J. W. , 'A novel influenza A virus mitochondrial protein that induces cell death ' (2001 ) 7 Nat. Med. : 1306 -1312.

    • Search Google Scholar

  • ECDC (2009): http://www.ecdc.europa.eu/en/healthtopics/H1N1/Pages/animals_and_h1n1.aspx

  • Felsenstein, J. (2004): PHYLIP (Phylogeny Inference Package), Version 3.6. Department of Genome Sciences, University of Washington, Seattle, WA, USA.

    Felsenstein J. , '', in PHYLIP (Phylogeny Inference Package), Version 3.6. Department of Genome Sciences , (2004 ) -.

  • Gibbs, A. J., Armstrong, J. S. and Downie, J. C. (2009): From where did the 2009 ’swine-origin’ influenza A virus (H1N1) emerge? Virol. J. 6, 207.

    Downie J. C. , 'From where did the 2009 ’swine-origin’ influenza A virus (H1N1) emerge? ' (2009 ) 6 Virol. J. : 207 -.

    • Search Google Scholar

  • Guilligay, D., Tarendeau, F., Resa-Infante, P., Coloma, R., Crepin, T., Sehr, P., Lewis, J., Ruigrok, R. W., Ortin, J., Hart, D. J. and Cusack, S. (2008): The structural basis for cap binding by influenza virus polymerase subunit PB2. Nat. Struct. Mol. Biol. 15, 500–506.

    Cusack S. , 'The structural basis for cap binding by influenza virus polymerase subunit PB2 ' (2008 ) 15 Nat. Struct. Mol. Biol. : 500 -506.

    • Search Google Scholar

  • Gyarmati, P., Metreveli, G., Kecskeméti, S., Rózsa, M., Belák, S. and Kiss, I. (2009): Molecular analysis and characterization of swine and human influenza viruses isolated in Hungary in 2006–2007. Virus Genes 39, 186–192.

    Kiss I. , 'Molecular analysis and characterization of swine and human influenza viruses isolated in Hungary in 2006–2007 ' (2009 ) 39 Virus Genes : 186 -192.

    • Search Google Scholar

  • Hall, T. A. (1999): BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. Ser. 41, 95–98. In: http://www.mbio.ncsu.edu/BioEdit/bioedit.html

    Hall T. A. , 'BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT ' (1999 ) 41 Nucl. Acids Symp. Ser. : 95 -98.

    • Search Google Scholar

  • Hatta, M., Gao, P., Halfmann, P. and Kawaoka, Y. (2001): Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 293, 1840–1842.

    Kawaoka Y. , 'Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses ' (2001 ) 293 Science : 1840 -1842.

    • Search Google Scholar

  • Herfst, S., Chutinimitkul, S., Ye, J., de Wit, E., Munster, V. J., Schrauwen, E. J., Bestebroer, T. M., Jonges, M., Meijer, A., Koopmans, M., Rimmelzwaan, G. F., Osterhaus, A. D., Perez, D. R. and Fouchier, R. A. (2010): Introduction of virulence markers in PB2 of pandemic swine-origin influenza virus does not result in enhanced virulence or transmission. J. Virol. 84, 3752–3758.

    Fouchier R. A. , 'Introduction of virulence markers in PB2 of pandemic swine-origin influenza virus does not result in enhanced virulence or transmission ' (2010 ) 84 J. Virol. : 3752 -3758.

    • Search Google Scholar

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

    Perez D. R. , 'Universal primer set for the full-length amplification of all influenza A viruses ' (2001 ) 146 Arch. Virol. : 2275 -2289.

    • Search Google Scholar

  • Hurt, A. C., Leang, S. K., Speers, D. J., Barr, I. G. and Maurer-Stroh, S. (2012): Mutations I117V and I117M and oseltamivir sensitivity of pandemic (H1N1) 2009 viruses. Emerg. Infect. Dis. 18, 109–112.

    Maurer-Stroh S. , 'Mutations I117V and I117M and oseltamivir sensitivity of pandemic (H1N1) 2009 viruses ' (2012 ) 18 Emerg. Infect. Dis. : 109 -112.

    • Search Google Scholar

  • Kiss, I., Gyarmati, P., Zohari, S., Wilbe Ramsay, K., Metreveli, G., Weiss, E., Brytting, M., Stivers, M., Lindström, S., Lundkvist, A., Nemirov, K., Thorén, P., Berg, M., Czifra, Gy. and Belák, S. (2008): Molecular characterization of highly pathogenic H5N1 avian influenza viruses isolated in Sweden in 2006. Virol. J. 5, 113.

    Belák S. , 'Molecular characterization of highly pathogenic H5N1 avian influenza viruses isolated in Sweden in 2006 ' (2008 ) 5 Virol. J. : 113 -.

    • Search Google Scholar

  • Li, O. T., Barr, I., Leung, C. Y., Chen, H., Guan, Y., Peiris, J. S. and Poon, L. L. (2007): Reliable universal RT-PCR assays for studying influenza polymerase subunit gene sequences from all 16 haemagglutinin subtypes. J. Virol. Meth. 142, 218–222.

    Poon L. L. , 'Reliable universal RT-PCR assays for studying influenza polymerase subunit gene sequences from all 16 haemagglutinin subtypes ' (2007 ) 142 J. Virol. Meth. : 218 -222.

    • Search Google Scholar

  • Lu, J., Rowley, T., Garten, R. and Donis, R. O. (2007): FluGenome: a web tool for genotyping influenza A virus. Nucl. Acids Res. 35 (Web Server Issue), W275–W279.

    Donis R. O. , 'FluGenome: a web tool for genotyping influenza A virus ' (2007 ) 35 Nucl. Acids Res. : W275 -W279.

    • Search Google Scholar

  • Matrosovich, M., Tuzikov, A., Bovin, N., Gambaryan, A., Klimov, A., Castrucci, M. R., Donatelli, I. and Kawaoka, Y. (2000): Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals. J. Virol. 74, 8502–8512.

    Kawaoka Y. , 'Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals ' (2000 ) 74 J. Virol. : 8502 -8512.

    • Search Google Scholar

  • Mehle, A. and Doudna, J. A. (2009): Adaptive strategies of the influenza virus polymerase for replication in humans. Proc. Natl Acad. Sci. USA 106, 21312–21316.

    Doudna J. A. , 'Adaptive strategies of the influenza virus polymerase for replication in humans ' (2009 ) 106 Proc. Natl Acad. Sci. USA : 21312 -21316.

    • Search Google Scholar

  • Metreveli, G., Emmoth, E., Zohari, S., Bálint, Á., Widén, F., Muradrasoli, S., Wallgren, P., Belák, S., Leblanc, N., Berg, M. and Kiss, I. (2011): Comparison of two H1N2 swine influenza A viruses from disease outbreaks in pigs in Sweden during 2009 and 2010. Virus Genes 42, 236–244.

    Kiss I. , 'Comparison of two H1N2 swine influenza A viruses from disease outbreaks in pigs in Sweden during 2009 and 2010 ' (2011 ) 42 Virus Genes : 236 -244.

    • Search Google Scholar

  • OIE (2008): Manual of Diagnostic Tests and Vaccines for Terrestrial Animals. Sixth edition. Office International des Epizooties, Paris, France.

    '', in Manual of Diagnostic Tests and Vaccines for Terrestrial Animals , (2008 ) -.

  • Ramakrishnan, M. A., Gramer, M. R., Goyal, S. M. and Sreevatsan, S. (2009): A Serine12Stop mutation in PB1-F2 of the 2009 pandemic (H1N1) influenza A: a possible reason for its enhanced transmission and pathogenicity to humans. J. Vet. Sci. 10, 349–351.

    Sreevatsan S. , 'A Serine12Stop mutation in PB1-F2 of the 2009 pandemic (H1N1) influenza A: a possible reason for its enhanced transmission and pathogenicity to humans ' (2009 ) 10 J. Vet. Sci. : 349 -351.

    • Search Google Scholar

  • Shinya, K., Hamm, S., Hatta, M., Ito, H., Ito, T. and Kawaoka, Y. (2004): PB2 amino acid at position 627 affects replicative efficiency, but not cell tropism, of Hong Kong H5N1 influenza A viruses in mice. Virology 320, 258–266.

    Kawaoka Y. , 'PB2 amino acid at position 627 affects replicative efficiency, but not cell tropism, of Hong Kong H5N1 influenza A viruses in mice ' (2004 ) 320 Virology : 258 -266.

    • Search Google Scholar

  • Smith, G. J., Vijaykrishna, D., Bahl, J., Lycett, S. J., Worobey, M., Pybus, O. G., Ma, S. K., Cheung, C. L., Raghwani, J., Bhatt, S., Peiris, J. S., Guan, Y. and Rambaut, A. (2009): Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459, 1122–1125.

    Rambaut A. , 'Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic ' (2009 ) 459 Nature : 1122 -1125.

    • Search Google Scholar

  • Squires, B., Macken, C., Garcia-Sastre, A., Godbole, S., Noronha, J., Hunt, V., Chang, R., Larsen, C. N., Klem, E., Biersack, K. and Scheuermann, R. H. (2008): BioHealthBase: informatics support in the elucidation of influenza virus host pathogen interactions and virulence. Nucl. Acids Res. 36, D497–D503.

    Scheuermann R. H. , 'BioHealthBase: informatics support in the elucidation of influenza virus host pathogen interactions and virulence ' (2008 ) 36 Nucl. Acids Res. : D497 -D503.

    • Search Google Scholar

  • Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007): MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596–1599.

    Kumar S. , 'MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0 ' (2007 ) 24 Mol. Biol. Evol. : 1596 -1599.

    • Search Google Scholar

  • WHO (2009): World now at the start of 2009 influenza pandemic. http://www.who.int/mediacentre/news/statements/2009/h1n1_pandemic_phase6_20090611/en/index.html

  • Zell, R., Krumbholz, A., Eitner, A., Krieg, R., Halbhuber, K. J. and Wutzler, P. (2007): Prevalence of PB1-F2 of influenza A viruses. J. Gen. Virol. 88, 536–546.

    Wutzler P. , 'Prevalence of PB1-F2 of influenza A viruses ' (2007 ) 88 J. Gen. Virol. : 536 -546.

    • Search Google Scholar
Cover Acta Veterinaria Hungarica
Acta Veterinaria Hungarica
Print ISSN:
0236-6290
Online ISSN:
1588-2705
Keywords:
Interspecies transmission; reverse zoonosis; porcine; human; Hungary

Monthly Content Usage

Abstract Views Full Text Views PDF Downloads
Sep 2020 3 0 0
Oct 2020 9 0 0
Nov 2020 1 1 0
Dec 2020 1 0 0
Jan 2021 4 0 0
Feb 2021 9 0 0
Mar 2021 7 0 0