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A human-like H1N2 influenza virus detected during an outbreak of acute respiratory disease in swine in Brazil

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Passive monitoring for detection of influenza A viruses (IAVs) in pigs has been carried out in Brazil since 2009, detecting mostly the A(H1N1)pdm09 influenza virus. Since then, outbreaks of acute respiratory disease suggestive of influenza A virus infection have been observed frequently in Brazilian pig herds. During a 2010-2011 influenza monitoring, a novel H1N2 influenza virus was detected in nursery pigs showing respiratory signs. The pathologic changes were cranioventral acute necrotizing bronchiolitis to subacute proliferative and purulent bronchointerstitial pneumonia. Lung tissue samples were positive for both influenza A virus and A(H1N1)pdm09 influenza virus based on RT-qPCR of the matrix gene. Two IAVs were isolated in SPF chicken eggs. HI analysis of both swine H1N2 influenza viruses showed reactivity to the H1δ cluster. DNA sequencing was performed for all eight viral gene segments of two virus isolates. According to the phylogenetic analysis, the HA and NA genes clustered with influenza viruses of the human lineage (H1-δ cluster, N2), whereas the six internal gene segments clustered with the A(H1N1)pdm09 group. This is the first report of a reassortant human-like H1N2 influenza virus derived from pandemic H1N1 virus causing an outbreak of respiratory disease in pigs in Brazil. The emergence of a reassortant IAV demands the close monitoring of pigs through the full-genome sequencing of virus isolates in order to enhance genetic information about IAVs circulating in pigs.

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  1. WHO (2009) Sequencing primers and protocol. Pandemic (H1N1) 2009 guidance documents

  2. Ali A, Khatri M, Wang LY, Saif YM, Lee CW (2012) Identification of swine H1N2/pandemic H1N1 reassortant influenza virus in pigs, United States. Vet Microbiol 158:60–68

    Article  CAS  PubMed  Google Scholar 

  3. Biondo N, Schaefer R, Gava D, Cantao ME, Silveira S, Mores MA, Ciacci-Zanella JR, Barcellos DE (2014) Genomic analysis of influenza A virus from captive wild boars in Brazil reveals a human-like H1N2 influenza virus. Vet Microbiol 168:34–40

    Article  CAS  PubMed  Google Scholar 

  4. Brentano L, Zanella JRC, Mores N, Piffer IA (2002) Levantamento soroepidemiológico para coronavírus respiratório e da gastroenterite transmissível e dos vírus de influenza H3N2 e H1N1 em rebanhos suínos no Brasil. Comunicado Técnico 306:1–6

  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(Pt 12):2947–2955

    CAS  PubMed  Google Scholar 

  6. Cappuccio JA, Pena L, Dibarbora M, Rimondi A, Pineyro P, Insarralde L, Quiroga MA, Machuca M, Craig MI, Olivera V, Chockalingam A, Perfumo CJ, Perez DR, Pereda A (2011) Outbreak of swine influenza in Argentina reveals a non-contemporary human H3N2 virus highly transmissible among pigs. J Gen Virol 92:2871–2878

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  7. Caron LF, Joineau MEG, Santin E, Richartz RRTB, Patricio MAC, Soccol VT (2010) Seroprevalence of H3N2 influenza A virus in pigs from Paraná (South Brazil): Interference of the animal management and climatic conditions. Virus Rev Res 15:63–73

    Google Scholar 

  8. Chan CH, Lin KL, Chan Y, Wang YL, Chi YT, Tu HL, Shieh HK, Liu WT (2006) Amplification of the entire genome of influenza A virus H1N1 and H3N2 subtypes by reverse-transcription polymerase chain reaction. J Virol Methods 136:38–43

    Article  CAS  PubMed  Google Scholar 

  9. Charoenvisal N, Keawcharoen J, Sreta D, Chaiyawong S, Nonthabenjawan N, Tantawet S, Jittimanee S, Arunorat J, Amonsin A, Thanawongnuwech R (2013) Genetic characterization of Thai swine influenza viruses after the introduction of pandemic H1N1 2009. Virus Genes 47:75–85

    Article  CAS  PubMed  Google Scholar 

  10. Ciacci-Zanella JR, Gava D, Schaefer R, Klein CS, Silva VS, Caron L (2013) No indication of porcine reproductive and respiratory syndrome virus (PRRSV) infection in Brazilian swine herds. In: Allen D (ed) Leman Swine Conference, St. Paul RiverCentre, St. Paul, Minnesota. Veterinary Continuing Education, p 192

  11. Ciacci Zanella JR, Gava D, Schaefer R, Silveira D, Schiochet F, Simon NL, Rocha CS, Coldebella A, Silva VS, Schwarz P, Zimmermann S (2012) Prevalence of influenza viruses infection in swine herds in Brazil in 2011. In: 22nd International Pig Veterinary Society Congress, Jeju, Korea, p 412

  12. Cunha RG, Vinha VR, Passos WD (1978) Isolation of a strain of Myxovirus influenzae-A suis from swine slaughtered in Rio de Janeiro. Rev Bras Biol 38:13–17

    CAS  PubMed  Google Scholar 

  13. Dibárbora M, Cappuccio J, Olivera V, Quiroga M, Machuca M, Perfumo C, Pérez D, Pereda A (2013) Swine influenza: clinical, serological, pathological, and virological cross-sectional studies in nine farms in Argentina. Influ Respir Viruses 7:10–15

    Article  Google Scholar 

  14. Ducatez MF, Hause B, Stigger-Rosser E, Darnell D, Corzo C, Juleen K, Simonson R, Brockwell-Staats C, Rubrum A, Wang D, Webb A, Crumpton JC, Lowe J, Gramer M, Webby RJ (2011) Multiple reassortment between pandemic (H1N1) 2009 and endemic influenza viruses in pigs, United States. Emerg Infect Dis 17:1624–1629

    Article  PubMed Central  PubMed  Google Scholar 

  15. Ecco R, Lazzari AM, Guedes RMC (2009) Pneumonia enzoótica em javalis (Sus scrofa). Pesquisa Vet Brasil 29:461–468

    Article  Google Scholar 

  16. Gauger PC, Vincent AL, Loving CL, Henningson JN, Lager KM, Janke BH, Kehrli ME Jr, Roth JA (2012) Kinetics of lung lesion development and pro-inflammatory cytokine response in pigs with vaccine-associated enhanced respiratory disease induced by challenge with pandemic (2009) A/H1N1 influenza virus. Vet Pathol 49:900–912

    Article  CAS  PubMed  Google Scholar 

  17. Gava D, Ibelli AMG, Schaefer R, Ciacci-Zanella JR (2013) Multiplex PCR for simultaneous detection of five single-stranded swine DNA viruses. In: XXIV Congresso Brasileiro de Virologia, Porto Seguro, Bahia, Brazil

  18. 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  PubMed  Google Scholar 

  19. Janke BH (2000) Diagnosis of swine influenza. Swine Health Prod 8:79–83

    Google Scholar 

  20. Janke BH (2014) Influenza a virus infections in Swine: pathogenesis and diagnosis. Vet Pathol 51:410–426

    Article  CAS  PubMed  Google Scholar 

  21. Karasin AI, Carman S, Olsen CW (2006) Identification of human H1N2 and human-swine reassortant H1N2 and H1N1 influenza A viruses among pigs in Ontario, Canada (2003 to 2005). J Clin Microbiol 44:1123–1126

    Article  PubMed Central  PubMed  Google Scholar 

  22. Komadina N, McVernon J, Hall R, Leder K (2014) A historical perspective of influenza A(H1N2) virus. Emerg Infect Dis 20:6–12

    Article  PubMed Central  PubMed  Google Scholar 

  23. Lamb RAK, R M (1996) Orthomyxoviridae: the viruses and their replication. In: Fields BN, Knipe PM, Howley PM et al (ed) Fields virology. Lippincott-Raven, Philadelphia, pp 1353-1395

  24. Lorusso A, Faaberg KS, Killian ML, Koster L, Vincent AL (2010) One-step real-time RT-PCR for pandemic influenza A virus (H1N1) 2009 matrix gene detection in swine samples. J Virol Methods 164:83–87

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Lorusso A, Vincent AL, Gramer ME, Lager KM, Ciacci-Zanella JR (2013) Contemporary epidemiology of North American lineage triple reassortant influenza A viruses in pigs. Curr Top Microbiol Immunol 370:113–132

    PubMed  Google Scholar 

  27. Luna LG, Armed Forces Institute of Pathology (US), Armed Forces Institute of Pathology (US) (1968) Manual of histologic staining methods of the Armed Forces Institute of Pathology, 3d edn. Blakiston Division, New York

  28. Moreno A, Di Trani L, Faccini S, Vaccari G, Nigrelli D, Boniotti MB, Falcone E, Boni A, Chiaponni C, Sozzi E, Cordioli P (2010) Novel H1N2 swine influenza reassortant strain in pigs derived from the pandemic H1N1/2009 virus. Vet Microbiol 149(3–4):472–477

  29. Nfon CK, Berhane Y, Hisanaga T, Zhang SZ, Handel K, Kehler H, Labrecque O, Lewis NS, Vincent AL, Copps J, Alexandersen S, Pasick J (2011) Characterization of H1N1 swine influenza viruses circulating in Canadian pigs in 2009. J Virol 85:8667–8679

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  30. Nicholson TL, Kukielka D, Vincent AL, Brockmeier SL, Miller LC, Faaberg KS (2011) Utility of a panviral microarray for detection of swine respiratory viruses in clinical samples. J Clin Microbiol 49:1542–1548

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Pereda A, Cappuccio J, Quiroga MA, Baumeister E, Insarralde L, Ibar M, Sanguinetti R, Cannilla ML, Franzese D, Escobar Cabrera OE, Craig MI, Rimondi A, Machuca M, Debenedetti RT, Zenobi C, Barral L, Balzano R, Capalbo S, Risso A, Perfumo CJ (2010) Pandemic (H1N1) 2009 outbreak on pig farm, Argentina. Emerg Infect Dis 16:304–307

    Article  PubMed  Google Scholar 

  32. Pereda A, Rimondi A, Cappuccio J, Sanguinetti R, Angel M, Ye J, Sutton T, Dibarbora M, Olivera V, Craig MI, Quiroga M, Machuca M, Ferrero A, Perfumo C, Perez DR (2011) Evidence of reassortment of pandemic H1N1 influenza virus in swine in Argentina: are we facing the expansion of potential epicenters of influenza emergence? Influenza Other Respi Viruses 5:409–412

    Article  PubMed Central  Google Scholar 

  33. Rajão DS, Costa AT, Brasil BS, Del Puerto HL, Oliveira FG, Alves F, Braz GF, Reis JK, Guedes RM, Lobato ZI, Leite RC (2012) Genetic characterization of influenza virus circulating in Brazilian pigs during 2009 and 2010 reveals a high prevalence of the pandemic H1N1 subtype. Influenza Other Respi Viruses 7(5):783–790

  34. Rajao DS, Alves F, Del Puerto HL, Braz GF, Oliveira FG, Ciacci-Zanella JR, Schaefer R, dos Reis JK, Guedes RM, Lobato ZI, Leite RC (2013) Serological evidence of swine influenza in Brazil. Influenza and other respiratory viruses 7:109–112

    Article  PubMed  Google Scholar 

  35. Schaefer R, Zanella JRC, Brentano L, Vincent AL, Ritterbusch GA, Silveira S, Caron L, Mores N (2011) Isolation and characterization of a pandemic H1N1 influenza virus in pigs in Brazil. Pesquisa Vet Brasil 31:761–767

    Article  Google Scholar 

  36. Silva MC, Rech RR, Gava D, Kuchiishi SS, Schaefer R, Ciacci-Zanella JR (2013) Porcine respiratory disease complex in Southern Brazil: pathogens and associated histopathology In: ACVP and ASVCP Annual Meeting, Montreal, Canada

  37. Spackman E, Suarez DL (2008) Type A influenza virus detection and quantitation by real-time RT-PCR. Methods Mol Biol 436:19–26

    CAS  PubMed  Google Scholar 

  38. 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

    Article  CAS  PubMed  Google Scholar 

  39. 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 28:2731–2739

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  40. Thacker EL, Thacker BJ, Janke BH (2001) Interaction between Mycoplasma hyopneumoniae and swine influenza virus. J Clin Microbiol 39:2525–2530

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Van Reeth K, Brown IH, Olsen CW (2012) Influenza virus. In: Zimmerman JJ, Karriker LA, Ramirez A, Schwartz KJ, Stevenson GW (eds) Diseases of Swine, 10th edn. Iowa State University Press, Ames, pp 557–571

  42. Vijaykrishna D, Poon LL, Zhu HC, Ma SK, Li OT, Cheung CL, Smith GJ, Peiris JS, Guan Y (2010) Reassortment of pandemic H1N1/2009 influenza A virus in swine. Science 328:1529

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  43. Vincent AL, Ma W, Lager KM, Janke BH, Richt JA (2008) Swine influenza viruses a North American perspective. Adv Virus Res 72:127–154

    Article  CAS  PubMed  Google Scholar 

  44. Vincent AL, Ma W, Lager KM, Gramer MR, Richt JA, Janke BH (2009) Characterization of a newly emerged genetic cluster of H1N1 and H1N2 swine influenza virus in the United States. Virus Genes 39:176–185

  45. Vincent AL, Wong F, Ciacci-Zanella JR, Pasick J, Van Reeth K, Peiris M, Gramer M, Webby R, Donis R, Swenson S, Parchariyanon S, Saito T, Awada L (2011) OFFLU Surveillance for Influenza in Pigs meeting, 6–7 April 2011, OIE Headquarters, Paris

  46. Vincent LL, Janke BH, Paul PS, Halbur PG (1997) A monoclonal-antibody-based immunohistochemical method for the detection of swine influenza virus in formalin-fixed, paraffin-embedded tissues. J Vet Diagn Invest 9:191–195

    Article  CAS  PubMed  Google Scholar 

  47. Weingartl HM, Berhane Y, Hisanaga T, Neufeld J, Kehler H, Emburry-Hyatt C, Hooper-McGreevy K, Kasloff S, Dalman B, Bystrom J, Alexandersen S, Li Y, Pasick J (2010) Genetic and pathobiologic characterization of pandemic H1N1 2009 influenza viruses from a naturally infected swine herd. J Virol 84:2245–2256

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  48. Zhou B, Donnelly ME, Scholes DT, St George K, Hatta M, Kawaoka Y, Wentworth DE (2009) Single-reaction genomic amplification accelerates sequencing and vaccine production for classical and Swine origin human influenza a viruses. J Virol 83:10309–10313

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  49. Zhou NN, Senne DA, Landgraf JS, Swenson SL, Erickson G, Rossow K, Liu L, Yoon K, Krauss S, Webster RG (1999) Genetic reassortment of avian, swine, and human influenza A viruses in American pigs. J Virol 73:8851–8856

    CAS  PubMed Central  PubMed  Google Scholar 

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This study was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq Process no. 578102/2008-0, Brazil) and EMBRAPA. The authors acknowledge Francieli Ianiski, Marisete F. Schiochet and Neide L. Simon for technical assistance, and Rafael Becker (DVM) for collecting biological samples from pigs. SS has a scholarship from CNPq.

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Correspondence to Rejane Schaefer.

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Schaefer, R., Rech, R.R., Gava, D. et al. A human-like H1N2 influenza virus detected during an outbreak of acute respiratory disease in swine in Brazil. Arch Virol 160, 29–38 (2015).

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