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Novel Reassortant Human-Like H3N2 and H3N1 Influenza A Viruses Detected in Pigs Are Virulent and Antigenically Distinct from Swine Viruses Endemic to the United States.
J Virol 2015; 89(22):11213-22JV

Abstract

Human-like swine H3 influenza A viruses (IAV) were detected by the USDA surveillance system. We characterized two novel swine human-like H3N2 and H3N1 viruses with hemagglutinin (HA) genes similar to those in human seasonal H3 strains and internal genes closely related to those of 2009 H1N1 pandemic viruses. The H3N2 neuraminidase (NA) was of the contemporary human N2 lineage, while the H3N1 NA was of the classical swine N1 lineage. Both viruses were antigenically distant from swine H3 viruses that circulate in the United States and from swine vaccine strains and also showed antigenic drift from human seasonal H3N2 viruses. Their pathogenicity and transmission in pigs were compared to those of a human H3N2 virus with a common HA ancestry. Both swine human-like H3 viruses efficiently infected pigs and were transmitted to indirect contacts, whereas the human H3N2 virus did so much less efficiently. To evaluate the role of genes from the swine isolates in their pathogenesis, reverse genetics-generated reassortants between the swine human-like H3N1 virus and the seasonal human H3N2 virus were tested in pigs. The contribution of the gene segments to virulence was complex, with the swine HA and internal genes showing effects in vivo. The experimental infections indicate that these novel H3 viruses are virulent and can sustain onward transmission in pigs, and the naturally occurring mutations in the HA were associated with antigenic divergence from H3 IAV from humans and swine. Consequently, these viruses could have a significant impact on the swine industry if they were to cause more widespread outbreaks, and the potential risk of these emerging swine IAV to humans should be considered.

IMPORTANCE

Pigs are important hosts in the evolution of influenza A viruses (IAV). Human-to-swine transmissions of IAV have resulted in the circulation of reassortant viruses containing human-origin genes in pigs, greatly contributing to the diversity of IAV in swine worldwide. New human-like H3N2 and H3N1 viruses that contain a mix of human and swine gene segments were recently detected by the USDA surveillance system. The human-like viruses efficiently infected pigs and resulted in onward airborne transmission, likely due to the multiple changes identified between human and swine H3 viruses. The human-like swine viruses are distinct from contemporary U.S. H3 swine viruses and from the strains used in swine vaccines, which could have a significant impact on the swine industry due to a lack of population immunity. Additionally, public health experts should consider an appropriate assessment of the risk of these emerging swine H3 viruses for the human population.

Authors+Show Affiliations

Virus and Prion Diseases Research Unit, National Animal Disease Center, ARS, USDA, Ames, Iowa, USA.Department of Veterinary Diagnostic and Production Animal Medicine, College of Veterinary Medicine, Iowa State University, Ames, Iowa, USA.Virus and Prion Diseases Research Unit, National Animal Disease Center, ARS, USDA, Ames, Iowa, USA.Department of Zoology, University of Cambridge, Cambridge, United Kingdom.Virus and Prion Diseases Research Unit, National Animal Disease Center, ARS, USDA, Ames, Iowa, USA.Diagnostic Virology Laboratory, National Veterinary Services Laboratories, Science, Technology and Analysis Services, Veterinary Services, APHIS, USDA, Ames, Iowa, USA.Poultry Diagnostic and Research Center, University of Georgia, Athens, Georgia, USA.Virginia-Maryland College of Veterinary Medicine, Department of Veterinary Medicine, University of Maryland, College Park, Maryland, USA.Department of Veterinary Diagnostic and Production Animal Medicine, College of Veterinary Medicine, Iowa State University, Ames, Iowa, USA.Virus and Prion Diseases Research Unit, National Animal Disease Center, ARS, USDA, Ames, Iowa, USA amy.vincent@ars.usda.gov.

Pub Type(s)

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

Language

eng

PubMed ID

26311895

Citation

Rajão, Daniela S., et al. "Novel Reassortant Human-Like H3N2 and H3N1 Influenza a Viruses Detected in Pigs Are Virulent and Antigenically Distinct From Swine Viruses Endemic to the United States." Journal of Virology, vol. 89, no. 22, 2015, pp. 11213-22.
Rajão DS, Gauger PC, Anderson TK, et al. Novel Reassortant Human-Like H3N2 and H3N1 Influenza A Viruses Detected in Pigs Are Virulent and Antigenically Distinct from Swine Viruses Endemic to the United States. J Virol. 2015;89(22):11213-22.
Rajão, D. S., Gauger, P. C., Anderson, T. K., Lewis, N. S., Abente, E. J., Killian, M. L., ... Vincent, A. L. (2015). Novel Reassortant Human-Like H3N2 and H3N1 Influenza A Viruses Detected in Pigs Are Virulent and Antigenically Distinct from Swine Viruses Endemic to the United States. Journal of Virology, 89(22), pp. 11213-22. doi:10.1128/JVI.01675-15.
Rajão DS, et al. Novel Reassortant Human-Like H3N2 and H3N1 Influenza a Viruses Detected in Pigs Are Virulent and Antigenically Distinct From Swine Viruses Endemic to the United States. J Virol. 2015;89(22):11213-22. PubMed PMID: 26311895.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Novel Reassortant Human-Like H3N2 and H3N1 Influenza A Viruses Detected in Pigs Are Virulent and Antigenically Distinct from Swine Viruses Endemic to the United States. AU - Rajão,Daniela S, AU - Gauger,Phillip C, AU - Anderson,Tavis K, AU - Lewis,Nicola S, AU - Abente,Eugenio J, AU - Killian,Mary Lea, AU - Perez,Daniel R, AU - Sutton,Troy C, AU - Zhang,Jianqiang, AU - Vincent,Amy L, Y1 - 2015/08/26/ PY - 2015/06/30/received PY - 2015/08/19/accepted PY - 2015/8/28/entrez PY - 2015/8/28/pubmed PY - 2016/1/30/medline SP - 11213 EP - 22 JF - Journal of virology JO - J. Virol. VL - 89 IS - 22 N2 - UNLABELLED: Human-like swine H3 influenza A viruses (IAV) were detected by the USDA surveillance system. We characterized two novel swine human-like H3N2 and H3N1 viruses with hemagglutinin (HA) genes similar to those in human seasonal H3 strains and internal genes closely related to those of 2009 H1N1 pandemic viruses. The H3N2 neuraminidase (NA) was of the contemporary human N2 lineage, while the H3N1 NA was of the classical swine N1 lineage. Both viruses were antigenically distant from swine H3 viruses that circulate in the United States and from swine vaccine strains and also showed antigenic drift from human seasonal H3N2 viruses. Their pathogenicity and transmission in pigs were compared to those of a human H3N2 virus with a common HA ancestry. Both swine human-like H3 viruses efficiently infected pigs and were transmitted to indirect contacts, whereas the human H3N2 virus did so much less efficiently. To evaluate the role of genes from the swine isolates in their pathogenesis, reverse genetics-generated reassortants between the swine human-like H3N1 virus and the seasonal human H3N2 virus were tested in pigs. The contribution of the gene segments to virulence was complex, with the swine HA and internal genes showing effects in vivo. The experimental infections indicate that these novel H3 viruses are virulent and can sustain onward transmission in pigs, and the naturally occurring mutations in the HA were associated with antigenic divergence from H3 IAV from humans and swine. Consequently, these viruses could have a significant impact on the swine industry if they were to cause more widespread outbreaks, and the potential risk of these emerging swine IAV to humans should be considered. IMPORTANCE: Pigs are important hosts in the evolution of influenza A viruses (IAV). Human-to-swine transmissions of IAV have resulted in the circulation of reassortant viruses containing human-origin genes in pigs, greatly contributing to the diversity of IAV in swine worldwide. New human-like H3N2 and H3N1 viruses that contain a mix of human and swine gene segments were recently detected by the USDA surveillance system. The human-like viruses efficiently infected pigs and resulted in onward airborne transmission, likely due to the multiple changes identified between human and swine H3 viruses. The human-like swine viruses are distinct from contemporary U.S. H3 swine viruses and from the strains used in swine vaccines, which could have a significant impact on the swine industry due to a lack of population immunity. Additionally, public health experts should consider an appropriate assessment of the risk of these emerging swine H3 viruses for the human population. SN - 1098-5514 UR - https://www.unboundmedicine.com/medline/citation/26311895/Novel_Reassortant_Human_Like_H3N2_and_H3N1_Influenza_A_Viruses_Detected_in_Pigs_Are_Virulent_and_Antigenically_Distinct_from_Swine_Viruses_Endemic_to_the_United_States_ L2 - http://jvi.asm.org/cgi/pmidlookup?view=long&pmid=26311895 DB - PRIME DP - Unbound Medicine ER -