Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 21, Number 8—August 2015

Influenza A Viruses of Human Origin in Swine, Brazil

Martha I. Nelson1Comments to Author , Rejane Schaefer1, Danielle Gava, Maurício Egídio Cantão, and Janice Reis Ciacci-Zanella
Author affiliations: Fogarty International Center of the National Institutes of Health, Bethesda, Maryland, USA (M.I. Nelson); EMBRAPA Swine and Poultry, Concordia, Brazil (R. Schaefer, D. Gava, M.E. Cantão, J.R. Ciacci-Zanella)

Main Article

Figure 4

Phylogenetic relationships between human and swine influenza N2 segments. Time-scaled Bayesian maximum clade credibility (MCC) tree inferred for the neuraminidase (N2) sequences of 682 viruses, including 6 swine viruses from Brazil sequenced for this study, A/swine/Brazil/185-11-7/2011(H1N2), A/swine/Brazil/232-11-13/2011(H1N2), A/swine/Brazil/232-11-14/2011(H1N2), A/swine/Brazil/31-11-1/2011(H1N2), A/swine/Brazil/355-11-6/2011(H3N2), and A/swine/Brazil/365-11-7/2011(H3N2); 2 swine influenza A v

Figure 4. Phylogenetic relationships between human and swine influenza N2 segments. Time-scaled Bayesian maximum clade credibility (MCC) tree inferred for the neuraminidase (N2) sequences of 682 viruses, including 6 swine viruses from Brazil sequenced for this study, A/swine/Brazil/185-11-7/2011(H1N2), A/swine/Brazil/232-11-13/2011(H1N2), A/swine/Brazil/232-11-14/2011(H1N2), A/swine/Brazil/31-11-1/2011(H1N2), A/swine/Brazil/355-11-6/2011(H3N2), and A/swine/Brazil/365-11-7/2011(H3N2); 2 swine influenza A viruses from Brazil sequenced previously, A/wild boar/Brazil/214-11-13D/2011(H1N2) (26) and A/swine/Brazil/31-11-3/2011(H1N2) (27); 325 human seasonal N2 viruses collected globally during 1957–2013; and 350 closely related swine viruses collected globally that have been studied previously (35). Gray shading indicates branches of human seasonal influenza A(H3N2) virus origin. Branches associated with viruses from swine are shaded by country/area of origin: light blue, Argentina; dark green, Brazil; dark blue, United States; purple, Vietnam; black, Europe; red, China; pink, Korea; orange, Thailand; light green, Mexico; turquoise, Japanese swine viruses. Posterior probabilities >0.9 are included for key nodes, and the 2 clades of Brazilian swine viruses are labeled a and b (Table 1).

Main Article

  1. Garten  RJ, Davis  CT, Russell  CA, Shu  B, Lindstrom  S, Balish  A, Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science. 2009;325:197201. DOIPubMedGoogle Scholar
  2. Chowell  G, Echevarría-Zuno  S, Viboud  C, Simonsen  L, Tamerius  J, Miller  MA, Characterizing the epidemiology of the 2009 influenza A/H1N1 pandemic in Mexico. PLoS Med. 2011;8:e1000436. DOIPubMedGoogle Scholar
  3. Song  MS, Lee  JH, Pascua  PNQ, Baek  YH, Kwon  H, Park  KJ, Evidence of human-to-swine transmission of the pandemic (H1N1) 2009 influenza virus in South Korea. J Clin Microbiol. 2010;48:320411. DOIPubMedGoogle Scholar
  4. Hofshagen  M, Gjerset  B, Er  C. Pandemic influenza A(H1N1)v: human to pig transmission in Norway. Euro Surveill. 2009;14:13 .PubMedGoogle Scholar
  5. Howden  KJ, Brockhoff  EJ, Caya  FD, McLeod  LJ, Lavoie  M, Ing  JD. An investigation into human pandemic influenza virus (H1N1) 2009 on an Alberta swine farm. Can Vet J. 2009;50:115361 .PubMedGoogle Scholar
  6. Pasma  T, Joseph  T. Pandemic (H1N1) 2009 infection in swine herds, Manitoba, Canada. Emerg Infect Dis. 2010;16:7068. DOIPubMedGoogle Scholar
  7. Trevennec  K, Leger  L, Lyazrhi  F, Baudon  E, Cheung  CY, Roger  F, Transmission of pandemic influenza H1N1 (2009) in Vietnamese swine in 2009–2010. Influenza Other Respir Viruses. 2012;6:348–57.
  8. Kim  SH, Moon  OK, Lee  KK, Song  YK, Yeo  CI, Bae  CW, Outbreak of pandemic influenza (H1N1) 2009 in pigs in Korea. Vet Rec. 2011;169:155. DOIPubMedGoogle Scholar
  9. Vijaykrishna  D, Poon  LLM, Zhu  HC, Ma  SK, Li  OTW, Cheung  CL, Reassortment of pandemic H1N1/2009 influenza A virus in swine. Science. 2010;328:1529. DOIPubMedGoogle Scholar
  10. Starick  E, Lange  E, Fereidouni  S, Bunzenthal  C, Höveler  R, Kuczka  A, Reassorted pandemic (H1N1) 2009 influenza A virus discovered from pigs in Germany. J Gen Virol. 2011;92:11848 . DOIPubMedGoogle Scholar
  11. Ducatez  MF, Hause  B, Stigger-Rosser  E, Darnell  D, Corzo  C, Juleen  K, Multiple reassortment between pandemic (H1N1) 2009 and endemic influenza viruses in pigs, United States. Emerg Infect Dis. 2011;17:16249.PubMedGoogle Scholar
  12. Lam  TTY, Zhu  H, Wang  J, Smith  DK, Holmes  EC, Webster  RG, Reassortment events among swine influenza A viruses in China: implications for the origin of the 2009 influenza pandemic. J Virol. 2011;85:1027985. DOIPubMedGoogle Scholar
  13. Liang  H, Lam  TTY, Fan  X, Chen  X, Zeng  Y, Zhou  J, Expansion of genotypic diversity and establishment of 2009 H1N1 pandemic-origin internal genes in pigs in China. J Virol. 2014;88:1086474. DOIPubMedGoogle Scholar
  14. Holyoake  PK, Kirkland  PD, Davis  RJ, Arzey  KE, Watson  J, Lunt  RA, The first identified case of pandemic H1N1 influenza in pigs in Australia. Aust Vet J. 2011;89:42731. DOIPubMedGoogle Scholar
  15. Nokireki  T, Laine  T, London  L, Ikonen  N, Huovilainen  A. The first detection of influenza in the Finnish pig population: a retrospective study. Acta Vet Scand. 2013;55:69. DOIPubMedGoogle Scholar
  16. Njabo  KY, Fuller  TL, Chasar  A, Pollinger  JP, Cattoli  G, Terregino  C, Pandemic A/H1N1/2009 influenza virus in swine, Cameroon, 2010. Vet Microbiol. 2012;156:18992. DOIPubMedGoogle Scholar
  17. Pereda  A, Cappuccio  J, Quiroga  M, Baumeister  E, Insarralde  L, Ibar  M, Pandemic (H1N1) 2009 outbreak on pig farm, Argentina. Emerg Infect Dis. 2010;16:3047. DOIPubMedGoogle Scholar
  18. Rajão  DS, Costa  AT, Brasil  BS, Del Puerto  HL, Oliveira  FG, Alves  F, Genetic characterization of influenza virus circulating in Brazilian pigs during 2009 and 2010 reveals a high prevalence of the pandemic H1N1 subtype. Influenza Other Respir Viruses. 2013;7:783–90.
  19. Schaefer  R, Zanella  JRC, Brentano  L, Vincent  AL, Ritterbusch  GA, Silveira  S, Isolation and characterization of a pandemic H1N1 influenza virus in pigs in Brazil. Pesqui Vet Bras. 2011;31:7617. DOIGoogle Scholar
  20. Ramirez-Nieto  GC, Rojas  CAD, Alfonso  VJ, Correa  JJ, Galvis  JD. First isolation and identification of H1N1 swine influenza viruses in Colombian pig farms. Health (Irvine Calif). 2012;04:98390.
  21. Escalera-Zamudio  M, Cobián-Güemes  G, de los Dolores Soto-del Río  M, Isa  P, Sánchez-Betancourt  I, Parissi-Crivelli  A, Characterization of an influenza A virus in Mexican swine that is related to the A/H1N1/2009 pandemic clade. Virology. 2012;433:17682. DOIPubMedGoogle Scholar
  22. Cappuccio  JA, Pena  L, Dibárbora  M, Rimondi  A, Piñeyro  P, Insarralde  L, Outbreak of swine influenza in Argentina reveals a non-contemporary human H3N2 virus highly transmissible among pigs. J Gen Virol. 2011;92:28718. DOIPubMedGoogle Scholar
  23. Caron  LF, Joineau  MEG, Santin  E, Richartz  RRTB, Patricio  MAC, Soccol  VT. Seroprevalence of H3N2 influenza A virus in pigs from Paraná (South Brazil): interference of the animal management and climatic conditions. Virus Rev Res. 2010;15:6373. DOIGoogle Scholar
  24. Cunha  RG, Vinha  VR, Passos  WD. Isolation of a strain of myxovirus influenzae-A suis from swine slaughtered in Rio de Janeiro. Rev Bras Biol. 1978;38:137 .PubMedGoogle Scholar
  25. Rajão  DS, Alves  F, Del Puerto  HL, Braz  GF, Oliveira  FG, Ciacci-Zanella  JR, Serological evidence of swine influenza in Brazil. Influenza Other Respir Viruses. 2013;7:109–12.
  26. Biondo  N, Schaefer  R, Gava  D, Cantão  ME, Silveira  S, Mores  MAZ, Genomic analysis of influenza A virus from captive wild boars in Brazil reveals a human-like H1N2 influenza virus. Vet Microbiol. 2014;168:3440. DOIPubMedGoogle Scholar
  27. Schaefer  R, Rech  RR, Gava  D, Cantão  ME, Silva  MC, Silveira  S. CZJ. A human-like H1N2 influenza virus detected during an outbreak of acute respiratory disease in swine in Brazil. Arch Virol. 2015;160:2938. DOIPubMedGoogle Scholar
  28. Lorusso  A, Faaberg  KS, Killian  ML, Koster  L, Vincent  AL. One-step real-time RT-PCR for pandemic influenza A virus (H1N1) 2009 matrix gene detection in swine samples. J Virol Methods. 2010;164:837. DOIPubMedGoogle Scholar
  29. Zhang  J, Harmon  KM. RNA extraction from swine samples and detection of influenza A virus in swine by real-time RT-PCR. Methods Mol Biol. 2014;1161:27793.PubMedGoogle Scholar
  30. Zhang  J, Gauger  PC. Isolation of swine influenza virus in cell cultures and embryonated chicken eggs. Methods Mol Biol. 2014;1161:26576.PubMedGoogle Scholar
  31. Chan  C-H, Lin  K-L, Chan  Y, Wang  Y-L, Chi  Y-T, Tu  H-L, Amplification of the entire genome of influenza A virus H1N1 and H3N2 subtypes by reverse-transcription polymerase chain reaction. J Virol Methods. 2006;136:3843. DOIPubMedGoogle Scholar
  32. Hoffmann  E, Stech  J, Guan  Y, Webster  RG, Perez  DR. Universal primer set for the full-length amplification of all influenza A viruses. Arch Virol. 2001;146:227589. DOIPubMedGoogle Scholar
  33. Zhou  B, Donnelly  ME, Scholes  DT, St George  K, Hatta  M, Kawaoka  Y, Single-reaction genomic amplification accelerates sequencing and vaccine production for classical and Swine origin human influenza a viruses. J Virol. 2009;83:1030913. DOIPubMedGoogle Scholar
  34. Bao  Y, Bolotov  P, Dernovoy  D, Kiryutin  B, Zaslavsky  L, Tatusova  T, The influenza virus resource at the National Center for Biotechnology Information. J Virol. 2008;82:596601. DOIPubMedGoogle Scholar
  35. Nelson  MI, Wentworth  DE, Culhane  MR, Vincent  AL, Viboud  C, LaPointe  MP, Introductions and evolution of human-origin seasonal influenza A viruses in multinational swine populations. J Virol. 2014;88:101109. DOIPubMedGoogle Scholar
  36. Edgar  RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:17927. DOIPubMedGoogle Scholar
  37. Stamatakis  A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22:268890. DOIPubMedGoogle Scholar
  38. Drummond  AJ, Suchard  MA, Xie  D, Rambaut  A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29:196973. DOIPubMedGoogle Scholar
  39. Suchard  MA, Rambaut  A. Many-core algorithms for statistical phylogenetics. Bioinformatics. 2009;25:13706. DOIPubMedGoogle Scholar
  40. Nelson  MI, Gramer  MR, Vincent  AL, Holmes  EC. Global transmission of influenza viruses from humans to swine. J Gen Virol. 2012;93:2195203. DOIPubMedGoogle Scholar

Main Article

1These authors contributed equally to this article.

Page created: July 14, 2015
Page updated: July 14, 2015
Page reviewed: July 14, 2015
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.