Influenza A Viruses of Human Origin in Swine, Brazil - Volume 21, Number 8—August 2015 - Emerging Infectious Disease journal - CDC
Volume 21, Number 8—August 2015
Research
Influenza A Viruses of Human Origin in Swine, Brazil
On This Page
Martha I. Nelson1 , Rejane Schaefer1, Danielle Gava, Maurício Egídio Cantão, and Janice Reis Ciacci-Zanella
Abstract
The evolutionary origins of the influenza A(H1N1)pdm09 virus that caused the first outbreak of the 2009 pandemic in Mexico remain unclear, highlighting the lack of swine surveillance in Latin American countries. Although Brazil has one of the largest swine populations in the world, influenza was not thought to be endemic in Brazil’s swine until the major outbreaks of influenza A(H1N1)pdm09 in 2009. Through phylogenetic analysis of whole-genome sequences of influenza viruses of the H1N1, H1N2, and H3N2 subtypes collected in swine in Brazil during 2009–2012, we identified multiple previously uncharacterized influenza viruses of human seasonal H1N2 and H3N2 virus origin that have circulated undetected in swine for more than a decade. Viral diversity has further increased in Brazil through reassortment between co-circulating viruses, including A(H1N1)pdm09. The circulation of multiple divergent hemagglutinin lineages challenges the design of effective cross-protective vaccines and highlights the need for additional surveillance.
Influenza A viruses circulating in swine (swIAVs) are of major economic concern for the swine industry and a pandemic threat for humans. The H1N1 influenza pandemic of 2009 was associated with a virus of swine origins (1) that caused its first outbreak in humans in Mexico in early 2009 (2). However, the evolutionary origins of influenza A(H1N1)pdm09 (pH1N1) virus in swine are poorly understood, and no potential progenitor viruses have been detected in swine in any part of the world. The relatively small number of swIAVs that have been characterized in Latin America make it particularly difficult to confirm or negate the possibility of pH1N1 evolving in swine in Mexico or another Latin American country before emergence in humans.
Since 2009, transmission of pH1N1 virus from humans to pigs has been documented in numerous countries spanning 6 continents (3–13), including many countries where influenza viruses previously had not been detected in swine, such as Australia (14), Finland (15), and Cameroon (16). pH1N1 virus has been identified in swine in several Latin American countries, including Argentina (17), Brazil (18,19), Colombia (20), and Mexico (21), because of human-to-swine transmission events that have occurred since 2009. In Argentina, multiple subtypes of viruses of human seasonal virus origin also have been identified in swine (22). Although Brazil hosts one of the largest swine populations in the world (≈41 million hogs), little evidence existed of swIAV circulation in swine herds in Brazil before 2009 (23–25). Influenza virus in pigs was first detected in Brazil in 1974, and the isolated virus was closely related to the classical North American swine virus A/swine/Illinois/1/63/H1N1 (24). However, relatively little clinical illness was observed in pigs in Brazil until 2009. Since 2009, Brazil’s swine population has experienced outbreaks of pH1N1 that are associated with respiratory illness. These outbreaks have been located primarily in the country’s major swine production regions in southern, midwestern, and southeastern Brazil (Figure 1). As a result, surveillance efforts for IAVs in swine populations in Brazil have increased, revealing additional influenza virus diversity. Serum collected from swine in southeastern Brazil during January–March 2009 indicated the widespread presence of antibodies cross-reactive to multiple antigenically distinct subtypes in swine: North American classical swine H1N1 (44.4%), North American triple-reassortant swine H3N2 (23.5%), and human-like H1N1 (38.3%) (25). In southern Brazil, the seroprevalence of the H3N2 subtype was recently found to be ≈20% (23). A human-like H1N2 virus was isolated from captive wild boars (26) and from swine (27) in Brazil.
Here, a phylogenetic analysis of newly sequenced influenza viruses from Brazil’s swine herds provides evidence that multiple IAVs of human seasonal virus origin have been circulating in swine for more than a decade. These particular H3N2 and H1N2 swIAV clades appear to be specific to Brazil. The co-circulation of multiple genetically diverse swIAV lineages of the H1N1, H1N2, and H3N2 subtypes introduces new challenges for the control of influenza in Brazil’s swine herds, including development of cross-protective vaccines.
Dr. Nelson is a Research Fellow at the Division of International Epidemiology and Population Studies at the Fogarty International Center, National Institutes of Health. Her primary research interests are the evolutionary dynamics of influenza viruses and other emerging pathogens.
Acknowledgments
We thank Neide L. Simon and Marisete F. Schiochet for assistance with laboratory techniques and Laboratório Multiusuários Centralizado de Genômica Funcional Aplicada à Agropecuária e Agroenergia for IAV sequencing using the Illumina platform.
This work was financially supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq process no. 578102/2008-0) and EMBRAPA. This work was supported in part by the Multinational Influenza Seasonal Mortality Study, an ongoing international collaborative effort to understand influenza epidemiology and evolution, led by the Fogarty International Center, National Institutes of Health, with funding from Office of Pandemics and Emerging Threats at the US Department of Health and Human Services.
References
- 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;325:197–201. DOIPubMed
- 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. DOIPubMed
- 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;48:3204–11. DOIPubMed
- Hofshagen M, Gjerset B, Er C. Pandemic influenza A(H1N1)v: human to pig transmission in Norway. Euro Surveill. 2009;14:1–3 .PubMed
- 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;50:1153–61 .PubMed
- Pasma T, Joseph T. Pandemic (H1N1) 2009 infection in swine herds, Manitoba, Canada. Emerg Infect Dis. 2010;16:706–8. DOIPubMed
- 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.
- 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.DOIPubMed
- 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. DOIPubMed
- 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;92:1184–8 . DOIPubMed
- 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;17:1624–9.PubMed
- 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;85:10279–85. DOIPubMed
- 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;88:10864–74. DOIPubMed
- 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;89:427–31. DOIPubMed
- 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. DOIPubMed
- 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;156:189–92. DOIPubMed
- Pereda A, Cappuccio J, Quiroga M, Baumeister E, Insarralde L, Ibar M, Pandemic (H1N1) 2009 outbreak on pig farm, Argentina. Emerg Infect Dis.2010;16:304–7. DOIPubMed
- 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.
- 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;31:761–7. DOI
- 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;04:983–90.
- 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;433:176–82. DOIPubMed
- 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;92:2871–8. DOIPubMed
- 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;15:63–73. DOI
- 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;38:13–7 .PubMed
- 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.
- 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;168:34–40. DOIPubMed
- 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;160:29–38. DOIPubMed
- 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;164:83–7. DOIPubMed
- 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;1161:277–93.PubMed
- Zhang J, Gauger PC. Isolation of swine influenza virus in cell cultures and embryonated chicken eggs. Methods Mol Biol.2014;1161:265–76.PubMed
- 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;136:38–43. DOIPubMed
- 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;146:2275–89. DOIPubMed
- 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;83:10309–13. DOIPubMed
- 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;82:596–601. DOIPubMed
- 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;88:10110–9. DOIPubMed
- Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–7. DOIPubMed
- Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics.2006;22:2688–90. DOIPubMed
- Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29:1969–73.DOIPubMed
- Suchard MA, Rambaut A. Many-core algorithms for statistical phylogenetics. Bioinformatics. 2009;25:1370–6. DOIPubMed
- Nelson MI, Gramer MR, Vincent AL, Holmes EC. Global transmission of influenza viruses from humans to swine. J Gen Virol. 2012;93:2195–203.DOIPubMed
Figures
Tables
Technical Appendix
Suggested citation for this article: Nelson MI, Schaefer R, Gava D, Cantão ME, Ciacci-Zanella JR. Influenza A viruses of human origin in swine, Brazil. Emerg Infect Dis. 2015 Aug [date cited]. http://dx.doi.org/10.3201/eid2108.141891
1These authors contributed equally to this article.
No hay comentarios:
Publicar un comentario