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Reassortment between Swine H3N2 and 2009 Pandemic H1N1 in the United States Resulted in Influenza A Viruses with Diverse Genetic Constellations with Variable Virulence in Pigs.
J Virol 2017; 91(4)JV

Abstract

Repeated spillovers of the H1N1 pandemic virus (H1N1pdm09) from humans to pigs resulted in substantial evolution of influenza A viruses infecting swine, contributing to the genetic and antigenic diversity of influenza A viruses (IAV) currently circulating in swine. The reassortment with endemic swine viruses and maintenance of some of the H1N1pdm09 internal genes resulted in the circulation of different genomic constellations in pigs. Here, we performed a whole-genome phylogenetic analysis of 368 IAV circulating in swine from 2009 to 2016 in the United States. We identified 44 different genotypes, with the most common genotype (32.33%) containing a clade IV-A HA gene, a 2002-lineage NA gene, an M-pdm09 gene, and remaining gene segments of triple reassortant internal gene (TRIG) origin. To understand how different genetic constellations may relate to viral fitness, we compared the pathogenesis and transmission in pigs of six representative genotypes. Although all six genotypes efficiently infected pigs, they resulted in different degrees of pathology and viral shedding. These results highlight the vast H3N2 genetic diversity circulating in U.S. swine after 2009. This diversity has important implications in the control of this disease by the swine industry, as well as a potential risk for public health if swine-adapted viruses with H1N1pdm09 genes have an increased risk to humans, as occurred in the 2011-2012 and 2016 human variant H3N2v cases associated with exhibition swine.

IMPORTANCE

People continue to spread the 2009 H1N1 pandemic (H1N1pdm09) IAV to pigs, allowing H1N1pdm09 to reassort with endemic swine IAV. In this study, we determined the 8 gene combinations of swine H3N2 IAV detected from 2009 to 2016. We identified 44 different genotypes of H3N2, the majority of which contained at least one H1N1pdm09 gene segment. We compared six representative genotypes of H3N2 in pigs. All six genotypes efficiently infected pigs, but they resulted in different degrees of lung damage and viral shedding. These results highlight the vast genetic diversity of H3N2 circulating in U.S. swine after 2009, with important implications for the control of IAV for the swine industry. Because H1N1pdm09 is also highly adapted to humans, these swine viruses pose a potential risk to public health if swine-adapted viruses with H1N1pdm09 genes also have an increased risk for human infection.

Authors+Show Affiliations

Virus and Prion Diseases Research Unit, National Animal Disease Center, Agricultural Research Service, United States Department of Agriculture, Ames, Iowa, USA.Virus and Prion Diseases Research Unit, National Animal Disease Center, Agricultural Research Service, United States Department of Agriculture, Ames, Iowa, USA.Virus and Prion Diseases Research Unit, National Animal Disease Center, Agricultural Research Service, United States Department of Agriculture, Ames, Iowa, USA.Department of Veterinary Diagnostic and Production Animal Medicine, College of Veterinary Medicine, Iowa State University, Ames, Iowa, USA.Diagnostic Virology Laboratory, National Veterinary Services Laboratories, Science, Technology and Analysis Services, Veterinary Services, Animal and Plant Health Inspection Service, United States Department of Agriculture, Ames, Iowa, USA.Diagnostic Virology Laboratory, National Veterinary Services Laboratories, Science, Technology and Analysis Services, Veterinary Services, Animal and Plant Health Inspection Service, United States Department of Agriculture, Ames, Iowa, USA.Virus and Prion Diseases Research Unit, National Animal Disease Center, Agricultural Research Service, United States Department of Agriculture, Ames, Iowa, USA amy.vincent@ars.usda.gov.

Pub Type(s)

Journal Article
Research Support, N.I.H., Extramural
Research Support, U.S. Gov't, Non-P.H.S.

Language

eng

PubMed ID

27928015

Citation

Rajão, Daniela S., et al. "Reassortment Between Swine H3N2 and 2009 Pandemic H1N1 in the United States Resulted in Influenza a Viruses With Diverse Genetic Constellations With Variable Virulence in Pigs." Journal of Virology, vol. 91, no. 4, 2017.
Rajão DS, Walia RR, Campbell B, et al. Reassortment between Swine H3N2 and 2009 Pandemic H1N1 in the United States Resulted in Influenza A Viruses with Diverse Genetic Constellations with Variable Virulence in Pigs. J Virol. 2017;91(4).
Rajão, D. S., Walia, R. R., Campbell, B., Gauger, P. C., Janas-Martindale, A., Killian, M. L., & Vincent, A. L. (2017). Reassortment between Swine H3N2 and 2009 Pandemic H1N1 in the United States Resulted in Influenza A Viruses with Diverse Genetic Constellations with Variable Virulence in Pigs. Journal of Virology, 91(4), doi:10.1128/JVI.01763-16.
Rajão DS, et al. Reassortment Between Swine H3N2 and 2009 Pandemic H1N1 in the United States Resulted in Influenza a Viruses With Diverse Genetic Constellations With Variable Virulence in Pigs. J Virol. 2017 02 15;91(4) PubMed PMID: 27928015.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Reassortment between Swine H3N2 and 2009 Pandemic H1N1 in the United States Resulted in Influenza A Viruses with Diverse Genetic Constellations with Variable Virulence in Pigs. AU - Rajão,Daniela S, AU - Walia,Rasna R, AU - Campbell,Brian, AU - Gauger,Phillip C, AU - Janas-Martindale,Alicia, AU - Killian,Mary Lea, AU - Vincent,Amy L, Y1 - 2017/01/31/ PY - 2016/09/06/received PY - 2016/12/01/accepted PY - 2016/12/9/pubmed PY - 2017/5/16/medline PY - 2016/12/9/entrez KW - H3N2 KW - genotypes KW - influenza KW - pandemic KW - swine JF - Journal of virology JO - J. Virol. VL - 91 IS - 4 N2 - : Repeated spillovers of the H1N1 pandemic virus (H1N1pdm09) from humans to pigs resulted in substantial evolution of influenza A viruses infecting swine, contributing to the genetic and antigenic diversity of influenza A viruses (IAV) currently circulating in swine. The reassortment with endemic swine viruses and maintenance of some of the H1N1pdm09 internal genes resulted in the circulation of different genomic constellations in pigs. Here, we performed a whole-genome phylogenetic analysis of 368 IAV circulating in swine from 2009 to 2016 in the United States. We identified 44 different genotypes, with the most common genotype (32.33%) containing a clade IV-A HA gene, a 2002-lineage NA gene, an M-pdm09 gene, and remaining gene segments of triple reassortant internal gene (TRIG) origin. To understand how different genetic constellations may relate to viral fitness, we compared the pathogenesis and transmission in pigs of six representative genotypes. Although all six genotypes efficiently infected pigs, they resulted in different degrees of pathology and viral shedding. These results highlight the vast H3N2 genetic diversity circulating in U.S. swine after 2009. This diversity has important implications in the control of this disease by the swine industry, as well as a potential risk for public health if swine-adapted viruses with H1N1pdm09 genes have an increased risk to humans, as occurred in the 2011-2012 and 2016 human variant H3N2v cases associated with exhibition swine. IMPORTANCE: People continue to spread the 2009 H1N1 pandemic (H1N1pdm09) IAV to pigs, allowing H1N1pdm09 to reassort with endemic swine IAV. In this study, we determined the 8 gene combinations of swine H3N2 IAV detected from 2009 to 2016. We identified 44 different genotypes of H3N2, the majority of which contained at least one H1N1pdm09 gene segment. We compared six representative genotypes of H3N2 in pigs. All six genotypes efficiently infected pigs, but they resulted in different degrees of lung damage and viral shedding. These results highlight the vast genetic diversity of H3N2 circulating in U.S. swine after 2009, with important implications for the control of IAV for the swine industry. Because H1N1pdm09 is also highly adapted to humans, these swine viruses pose a potential risk to public health if swine-adapted viruses with H1N1pdm09 genes also have an increased risk for human infection. SN - 1098-5514 UR - https://www.unboundmedicine.com/medline/citation/27928015/Reassortment_between_Swine_H3N2_and_2009_Pandemic_H1N1_in_the_United_States_Resulted_in_Influenza_A_Viruses_with_Diverse_Genetic_Constellations_with_Variable_Virulence_in_Pigs_ L2 - https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/27928015/ DB - PRIME DP - Unbound Medicine ER -