Antigenic Distance between North American Swine and Human Seasonal H3N2 Influenza A Viruses as an Indication of Zoonotic Risk to Humans

Souza, Carine K.; Anderson, Tavis K.; Chang, Jennifer; Venkatesh, Divya; Lewis, Nicola S.; Pekosz, Andrew; Shaw-Saliba, Kathryn; Rothman, Richard E.; Chen, Kuan-Fu; Vincent, Amy L.

doi:10.1128/JVI.01374-21

Title: Antigenic Distance between North American Swine and Human Seasonal H3N2 Influenza A Viruses as an Indication of Zoonotic Risk to Humans

Journal Article · Wed Jan 26 00:00:00 EST 2022 · Journal of Virology

DOI:https://doi.org/10.1128/JVI.01374-21· OSTI ID:1983353

Souza, Carine K. ^[1];

^[1]; Chang, Jennifer ^[1]; Venkatesh, Divya ^[2]; Lewis, Nicola S. ^[2];

^[3];

^[3]; Rothman, Richard E. ^[3]; Chen, Kuan-Fu ^[4];

^[1]

US Dept. of Agriculture (USDA), Ames, IA (United States). Agricultural Research Service (ARS), National Animal Disease Center
Univ. of London, London, Hertfordshire (United Kingdom). The Royal Veterinary College
Johns Hopkins Univ., Baltimore, MD (United States)
Chang Gung Memorial Hospital at Keelung, Keelung City (Taiwan)

Human-to-swine transmission of influenza A virus (IAV) repeatedly occurs, leading to sustained transmission and increased diversity in swine; human seasonal H3N2 introductions occurred in the 1990s and 2010s and were maintained in North American swine. Swine H3N2 strains were subsequently associated with zoonotic infections, highlighting the need to understand the risk of endemic swine IAV to humans. We quantified antigenic distances between swine H3N2 and human seasonal vaccine strains from 1973 to 2014 using a panel of monovalent antisera raised in pigs in hemagglutination inhibition (HI) assays. Swine H3N2 lineages retained the closest antigenic similarity to human vaccine strains from the decade of incursion. Swine lineages from the 1990s were antigenically more similar to human vaccine strains of the mid-1990s but had substantial distance from recent human vaccine strains. In contrast, lineages from the 2010s were closer to human vaccine strains from 2011 and 2014 and the most antigenically distant from human vaccine strains prior to 2007. HI assays using ferret antisera demonstrated that swine lineages from the 1990s and 2010s had significant fold reductions compared to the homologous HI titer of the nearest pandemic preparedness candidate vaccine virus (CVV) or seasonal vaccine strain. The assessment of postinfection and postvaccination human serum cohorts demonstrated limited cross-reactivity to swine H3N2 from the 1990s, especially in older adults born before the 1970s. We identified swine strains to which humans are likely to lack population immunity or are not protected against by a current human seasonal vaccine or CVV to use in prioritizing future human CVV strain selection.

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Research Organization:: Oak Ridge Associated Universities (ORAU), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-06OR23100

OSTI ID:: 1983353

Journal Information:: Journal of Virology, Vol. 96, Issue 2; ISSN 0022-538X

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (46)

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 Rajão, Daniela S.; Walia, Rasna R.; Campbell, Brian Journal of Virology, Vol. 91, Issue 4 https://doi.org/10.1128/JVI.01763-16	journal	February 2017
Molecular and Antigenic Characterization of Triple-Reassortant H3N2 Swine Influenza Viruses Isolated from Pigs, Turkey and Quail in Canada Nfon, C.; Berhane, Y.; Zhang, S. Transboundary and Emerging Diseases, Vol. 58, Issue 5 https://doi.org/10.1111/j.1865-1682.2011.01219.x	journal	April 2011
MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform Katoh, K. Nucleic Acids Research, Vol. 30, Issue 14 https://doi.org/10.1093/nar/gkf436	journal	July 2002
Aerosol Transmission from Infected Swine to Ferrets of an H3N2 Virus Collected from an Agricultural Fair and Associated with Human Variant Infections Kaplan, Bryan S.; Kimble, J. Brian; Chang, Jennifer Journal of Virology, Vol. 94, Issue 16 https://doi.org/10.1128/JVI.01009-20	journal	July 2020
Cross-reactive and Vaccine-Induced Antibody to an Emerging Swine-Origin Variant of Influenza A Virus Subtype H3N2 (H3N2v) Skowronski, Danuta M.; Janjua, Naveed Z.; De Serres, Gaston The Journal of Infectious Diseases, Vol. 206, Issue 12 https://doi.org/10.1093/infdis/jis500	journal	October 2012
ISU FLUture: a veterinary diagnostic laboratory web-based platform to monitor the temporal genetic patterns of Influenza A virus in swine Zeller, Michael A.; Anderson, Tavis K.; Walia, Rasna W. BMC Bioinformatics, Vol. 19, Issue 1 https://doi.org/10.1186/s12859-018-2408-7	journal	November 2018
H3N2v and Other Influenza Epidemic Risk Based on Age-Specific Estimates of Sero-Protection and Contact Network Interactions Skowronski, Danuta M.; Moser, Flavia S.; Janjua, Naveed Z. PLoS ONE, Vol. 8, Issue 1 https://doi.org/10.1371/journal.pone.0054015	journal	January 2013
Introduction, Evolution, and Dissemination of Influenza A Viruses in Exhibition Swine in the United States during 2009 to 2013 Nelson, Martha I.; Stucker, Karla M.; Schobel, Seth A. Journal of Virology, Vol. 90, Issue 23 https://doi.org/10.1128/JVI.01457-16	journal	September 2016
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 Rajão, Daniela S.; Gauger, Phillip C.; Anderson, Tavis K. Journal of Virology, Vol. 89, Issue 22 https://doi.org/10.1128/JVI.01675-15	journal	August 2015
Antibody landscapes after influenza virus infection or vaccination Fonville, J. M.; Wilks, S. H.; James, S. L. Science, Vol. 346, Issue 6212 https://doi.org/10.1126/science.1256427	journal	November 2014
Neutralizing Antibodies Against Previously Encountered Influenza Virus Strains Increase over Time: A Longitudinal Analysis Miller, M. S.; Gardner, T. J.; Krammer, F. Science Translational Medicine, Vol. 5, Issue 198 https://doi.org/10.1126/scitranslmed.3006637	journal	August 2013
Serial Vaccination and the Antigenic Distance Hypothesis: Effects on Influenza Vaccine Effectiveness During A(H3N2) Epidemics in Canada, 2010–2011 to 2014–2015 Skowronski, Danuta M.; Chambers, Catharine; De Serres, Gaston The Journal of Infectious Diseases, Vol. 215, Issue 7 https://doi.org/10.1093/infdis/jix074	journal	February 2017
Impact of age and pre-existing influenza immune responses in humans receiving split inactivated influenza vaccine on the induction of the breadth of antibodies to influenza A strains Nuñez, Ivette A.; Carlock, Michael A.; Allen, James D. PLOS ONE, Vol. 12, Issue 11 https://doi.org/10.1371/journal.pone.0185666	journal	November 2017
Influenza A(H3N2) Variant Virus Outbreak at Three Fairs — Maryland, 2017 Duwell, Monique M.; Blythe, David; Radebaugh, Michael W. MMWR. Morbidity and Mortality Weekly Report, Vol. 67, Issue 42 https://doi.org/10.15585/mmwr.mm6742a1	journal	October 2018
Influenza Research Database: An integrated bioinformatics resource for influenza virus research Zhang, Yun; Aevermann, Brian D.; Anderson, Tavis K. Nucleic Acids Research, Vol. 45, Issue D1 https://doi.org/10.1093/nar/gkw857	journal	September 2016
Antigenic and Genetic Characteristics of Swine-Origin 2009 A(H1N1) Influenza Viruses Circulating in Humans Garten, R. J.; Davis, C. T.; Russell, C. A. Science, Vol. 325, Issue 5937 https://doi.org/10.1126/science.1176225	journal	May 2009
Evolution of Novel Reassortant A/H3N2 Influenza Viruses in North American Swine and Humans, 2009–2011 Nelson, Martha I.; Vincent, Amy L.; Kitikoon, Pravina Journal of Virology, Vol. 86, Issue 16 https://doi.org/10.1128/JVI.00259-12	journal	June 2012
Pathogenesis and transmission of swine origin A(H3N2)v influenza viruses in ferrets Pearce, M. B.; Jayaraman, A.; Pappas, C. Proceedings of the National Academy of Sciences, Vol. 109, Issue 10 https://doi.org/10.1073/pnas.1119945109	journal	February 2012
Human-Origin Influenza A(H3N2) Reassortant Viruses in Swine, Southeast Mexico Nelson, Martha I.; Souza, Carine K.; Trovão, Nídia S. Emerging Infectious Diseases, Vol. 25, Issue 4 https://doi.org/10.3201/eid2504.180779	journal	April 2019
Global migration of influenza A viruses in swine Nelson, Martha I.; Viboud, Cécile; Vincent, Amy L. Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7696	journal	March 2015
ggplot2 Wickham, Hadley Use R! https://doi.org/10.1007/978-3-319-24277-4	book	January 2016
Mapping the Antigenic and Genetic Evolution of Influenza Virus Smith, D. J. Science, Vol. 305, Issue 5682 https://doi.org/10.1126/science.1097211	journal	July 2004
Influenza A(H3N2) Virus in Swine at Agricultural Fairs and Transmission to Humans, Michigan and Ohio, USA, 2016 Bowman, Andrew S.; Walia, Rasna R.; Nolting, Jacqueline M. Emerging Infectious Diseases, Vol. 23, Issue 9 https://doi.org/10.3201/eid2309.170847	journal	September 2017
Neuraminidase Receptor Binding Variants of Human Influenza A(H3N2) Viruses Resulting from Substitution of Aspartic Acid 151 in the Catalytic Site: a Role in Virus Attachment? Lin, Y. P.; Gregory, V.; Collins, P. Journal of Virology, Vol. 84, Issue 13 https://doi.org/10.1128/JVI.00458-10	journal	April 2010
Introductions and Evolution of Human-Origin Seasonal Influenza A Viruses in Multinational Swine Populations Nelson, M. I.; Wentworth, D. E.; Culhane, M. R. Journal of Virology, Vol. 88, Issue 17 https://doi.org/10.1128/JVI.01080-14	journal	June 2014
Novel vaccine concept based on back-boost effect in viral infection Kohler, Heinz Vaccine, Vol. 33, Issue 29 https://doi.org/10.1016/j.vaccine.2015.05.035	journal	June 2015
Outbreak of Variant Influenza A(H3N2) Virus in the United States Jhung, M. A.; Epperson, S.; Biggerstaff, M. Clinical Infectious Diseases, Vol. 57, Issue 12 https://doi.org/10.1093/cid/cit649	journal	September 2013
Investigation of an Outbreak of Variant Influenza A(H3N2) Virus Infection Associated With an Agricultural Fair—Ohio, August 2012 Greenbaum, Adena; Quinn, Celia; Bailer, Jennifer Journal of Infectious Diseases, Vol. 212, Issue 10 https://doi.org/10.1093/infdis/jiv269	journal	May 2015
Beyond Antigenic Match: Possible Agent-Host and Immuno-epidemiological Influences on Influenza Vaccine Effectiveness During the 2015–2016 Season in Canada Skowronski, Danuta M.; Chambers, Catharine; Sabaiduc, Suzana The Journal of Infectious Diseases, Vol. 216, Issue 12 https://doi.org/10.1093/infdis/jix526	journal	October 2017
Reverse zoonosis of influenza to swine: new perspectives on the human–animal interface Nelson, Martha I.; Vincent, Amy L. Trends in Microbiology, Vol. 23, Issue 3 https://doi.org/10.1016/j.tim.2014.12.002	journal	March 2015
Complete Genome Sequences of Two Novel Human-Like H3N2 Influenza A Viruses, A/swine/Oklahoma/65980/2017 (H3N2) and A/Swine/Oklahoma/65260/2017 (H3N2), Detected in Swine in the United States Zeller, Michael A.; Li, Ganwu; Harmon, Karen M. Microbiology Resource Announcements, Vol. 7, Issue 20 https://doi.org/10.1128/MRA.01203-18	journal	November 2018
The global antigenic diversity of swine influenza A viruses Lewis, Nicola S.; Russell, Colin A.; Langat, Pinky eLife, Vol. 5 https://doi.org/10.7554/eLife.12217	journal	April 2016
Antigenic and genetic evolution of contemporary swine H1 influenza viruses in the United States Rajao, Daniela S.; Anderson, Tavis K.; Kitikoon, Pravina Virology, Vol. 518 https://doi.org/10.1016/j.virol.2018.02.006	journal	May 2018
Sex-specific effects of age and body mass index on antibody responses to seasonal influenza vaccines in healthcare workers Kuo, Helen; Shapiro, Janna R.; Dhakal, Santosh Vaccine, Vol. 40, Issue 11 https://doi.org/10.1016/j.vaccine.2021.02.047	journal	March 2022
Genotype patterns of contemporary reassorted H3N2 virus in US swine Kitikoon, P.; Nelson, M. I.; Killian, M. L. Journal of General Virology, Vol. 94, Issue Pt_6 https://doi.org/10.1099/vir.0.51839-0	journal	May 2013
Antigenic evolution of H3N2 influenza A viruses in swine in the United States from 2012 to 2016 Bolton, Marcus J.; Abente, Eugenio J.; Venkatesh, Divya Influenza and Other Respiratory Viruses, Vol. 13, Issue 1 https://doi.org/10.1111/irv.12610	journal	October 2018
Human Mobility Networks, Travel Restrictions, and the Global Spread of 2009 H1N1 Pandemic Bajardi, Paolo; Poletto, Chiara; Ramasco, Jose J. PLoS ONE, Vol. 6, Issue 1 https://doi.org/10.1371/journal.pone.0016591	journal	January 2011
Childhood immune imprinting to influenza A shapes birth year-specific risk during seasonal H1N1 and H3N2 epidemics Gostic, Katelyn M.; Bridge, Rebecca; Brady, Shane PLOS Pathogens, Vol. 15, Issue 12 https://doi.org/10.1371/journal.ppat.1008109	journal	December 2019
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
Substitutions near the Hemagglutinin Receptor-Binding Site Determine the Antigenic Evolution of Influenza A H3N2 Viruses in U.S. Swine Lewis, N. S.; Anderson, T. K.; Kitikoon, P. Journal of Virology, Vol. 88, Issue 9 https://doi.org/10.1128/JVI.03805-13	journal	February 2014
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt Molecular Biology and Evolution, Vol. 32, Issue 1 https://doi.org/10.1093/molbev/msu300	journal	November 2014
Differential Antibody Recognition of H3N2 Vaccine and Seasonal Influenza Virus Strains Based on Age, Vaccine Status, and Sex in the 2017–2018 Season Ursin, Rebecca L.; Liu, Hsuan; Powell, Harrison R. The Journal of Infectious Diseases, Vol. 222, Issue 8 https://doi.org/10.1093/infdis/jiaa289	journal	June 2020
Swine Influenza A Viruses and the Tangled Relationship with Humans Anderson, Tavis K.; Chang, Jennifer; Arendsee, Zebulun W. Cold Spring Harbor Perspectives in Medicine, Vol. 11, Issue 3 https://doi.org/10.1101/cshperspect.a038737	journal	January 2020
Pathogenesis and Transmission of Genetically Diverse Swine-Origin H3N2 Variant Influenza A Viruses from Multiple Lineages Isolated in the United States, 2011–2016 Sun, Xiangjie; Pulit-Penaloza, Joanna A.; Belser, Jessica A. Journal of Virology, Vol. 92, Issue 16 https://doi.org/10.1128/JVI.00665-18	journal	August 2018
Use of Influenza Risk Assessment Tool for Prepandemic Preparedness Burke, Stephen A.; Trock, Susan C. Emerging Infectious Diseases, Vol. 24, Issue 3 https://doi.org/10.3201/eid2403.171852	journal	March 2018
Paradoxical clade- and age-specific vaccine effectiveness during the 2018/19 influenza A(H3N2) epidemic in Canada: potential imprint-regulated effect of vaccine (I-REV) Skowronski, Danuta M.; Sabaiduc, Suzana; Leir, Siobhan Eurosurveillance, Vol. 24, Issue 46 https://doi.org/10.2807/1560-7917.ES.2019.24.46.1900585	journal	November 2019

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Title: Antigenic Distance between North American Swine and Human Seasonal H3N2 Influenza A Viruses as an Indication of Zoonotic Risk to Humans

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