Reverse-zoonoses of 2009 H1N1 pandemic influenza A viruses and evolution in United States swine results in viruses with zoonotic potential
The 2009 H1N1 pandemic (pdm09) lineage of influenza A virus (IAV) crosses interspecies barriers with frequent human-to-swine spillovers each year. These spillovers reassort and drift within swine populations, leading to genetically and antigenically novel IAV that represent a zoonotic threat. We qua...
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| Veröffentlicht in: | PLoS pathogens 2023-07, Vol.19 (7), p.e1011476-e1011476 |
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| creator | Markin, Alexey Ciacci Zanella, Giovana Arendsee, Zebulun W Zhang, Jianqiang Krueger, Karen M Gauger, Phillip C Vincent Baker, Amy L Anderson, Tavis K |
| description | The 2009 H1N1 pandemic (pdm09) lineage of influenza A virus (IAV) crosses interspecies barriers with frequent human-to-swine spillovers each year. These spillovers reassort and drift within swine populations, leading to genetically and antigenically novel IAV that represent a zoonotic threat. We quantified interspecies transmission of the pdm09 lineage, persistence in swine, and identified how evolution in swine impacted zoonotic risk. Human and swine pdm09 case counts between 2010 and 2020 were correlated and human pdm09 burden and circulation directly impacted the detection of pdm09 in pigs. However, there was a relative absence of pdm09 circulation in humans during the 2020-21 season that was not reflected in swine. During the 2020-21 season, most swine pdm09 detections originated from human-to-swine spillovers from the 2018-19 and 2019-20 seasons that persisted in swine. We identified contemporary swine pdm09 representatives of each persistent spillover and quantified cross-reactivity between human seasonal H1 vaccine strains and the swine strains using a panel of monovalent ferret antisera in hemagglutination inhibition (HI) assays. The swine pdm09s had variable antigenic reactivity to vaccine antisera, but each swine pdm09 clade exhibited significant reduction in cross-reactivity to one or more of the human seasonal vaccine strains. Further supporting zoonotic risk, we showed phylogenetic evidence for 17 swine-to-human transmission events of pdm09 from 2010 to 2021, 11 of which were not previously classified as variants, with each of the zoonotic cases associated with persistent circulation of pdm09 in pigs. These data demonstrate that reverse-zoonoses and evolution of pdm09 in swine results in viruses that are capable of zoonotic transmission and represent a potential pandemic threat. |
| doi_str_mv | 10.1371/journal.ppat.1011476 |
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These spillovers reassort and drift within swine populations, leading to genetically and antigenically novel IAV that represent a zoonotic threat. We quantified interspecies transmission of the pdm09 lineage, persistence in swine, and identified how evolution in swine impacted zoonotic risk. Human and swine pdm09 case counts between 2010 and 2020 were correlated and human pdm09 burden and circulation directly impacted the detection of pdm09 in pigs. However, there was a relative absence of pdm09 circulation in humans during the 2020-21 season that was not reflected in swine. During the 2020-21 season, most swine pdm09 detections originated from human-to-swine spillovers from the 2018-19 and 2019-20 seasons that persisted in swine. We identified contemporary swine pdm09 representatives of each persistent spillover and quantified cross-reactivity between human seasonal H1 vaccine strains and the swine strains using a panel of monovalent ferret antisera in hemagglutination inhibition (HI) assays. The swine pdm09s had variable antigenic reactivity to vaccine antisera, but each swine pdm09 clade exhibited significant reduction in cross-reactivity to one or more of the human seasonal vaccine strains. Further supporting zoonotic risk, we showed phylogenetic evidence for 17 swine-to-human transmission events of pdm09 from 2010 to 2021, 11 of which were not previously classified as variants, with each of the zoonotic cases associated with persistent circulation of pdm09 in pigs. These data demonstrate that reverse-zoonoses and evolution of pdm09 in swine results in viruses that are capable of zoonotic transmission and represent a potential pandemic threat.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1011476</identifier><identifier>PMID: 37498825</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animal populations ; Animals ; Antigens ; Antisera ; Biology and Life Sciences ; Complications and side effects ; Computer and Information Sciences ; Cross-reactivity ; Diagnosis ; Evolution ; Ferrets ; Genes ; Genetic diversity ; Genomes ; Health aspects ; Hemagglutination inhibition ; Hogs ; Humans ; Immune Sera ; Influenza ; Influenza A ; Influenza A virus ; Influenza A Virus, H1N1 Subtype - genetics ; Influenza, Human - epidemiology ; Medicine and health sciences ; Orthomyxoviridae Infections - epidemiology ; Orthomyxoviridae Infections - veterinary ; Pandemics ; Phylogenetics ; Phylogeny ; Population genetics ; Regression analysis ; Risk factors ; Seasons ; Strains (organisms) ; Swine ; Swine Diseases ; Swine influenza ; United States - epidemiology ; Vaccines ; Viruses ; Zoonoses ; Zoonoses - epidemiology</subject><ispartof>PLoS pathogens, 2023-07, Vol.19 (7), p.e1011476-e1011476</ispartof><rights>Copyright: This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. 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We identified contemporary swine pdm09 representatives of each persistent spillover and quantified cross-reactivity between human seasonal H1 vaccine strains and the swine strains using a panel of monovalent ferret antisera in hemagglutination inhibition (HI) assays. The swine pdm09s had variable antigenic reactivity to vaccine antisera, but each swine pdm09 clade exhibited significant reduction in cross-reactivity to one or more of the human seasonal vaccine strains. Further supporting zoonotic risk, we showed phylogenetic evidence for 17 swine-to-human transmission events of pdm09 from 2010 to 2021, 11 of which were not previously classified as variants, with each of the zoonotic cases associated with persistent circulation of pdm09 in pigs. These data demonstrate that reverse-zoonoses and evolution of pdm09 in swine results in viruses that are capable of zoonotic transmission and represent a potential pandemic threat.</description><subject>Animal populations</subject><subject>Animals</subject><subject>Antigens</subject><subject>Antisera</subject><subject>Biology and Life Sciences</subject><subject>Complications and side effects</subject><subject>Computer and Information Sciences</subject><subject>Cross-reactivity</subject><subject>Diagnosis</subject><subject>Evolution</subject><subject>Ferrets</subject><subject>Genes</subject><subject>Genetic diversity</subject><subject>Genomes</subject><subject>Health aspects</subject><subject>Hemagglutination inhibition</subject><subject>Hogs</subject><subject>Humans</subject><subject>Immune Sera</subject><subject>Influenza</subject><subject>Influenza A</subject><subject>Influenza A virus</subject><subject>Influenza A Virus, H1N1 Subtype - genetics</subject><subject>Influenza, Human - epidemiology</subject><subject>Medicine and health sciences</subject><subject>Orthomyxoviridae Infections - 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Academic</collection><collection>OSTI.GOV</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>PLoS pathogens</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Markin, Alexey</au><au>Ciacci Zanella, Giovana</au><au>Arendsee, Zebulun W</au><au>Zhang, Jianqiang</au><au>Krueger, Karen M</au><au>Gauger, Phillip C</au><au>Vincent Baker, Amy L</au><au>Anderson, Tavis K</au><au>Su, Shuo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Reverse-zoonoses of 2009 H1N1 pandemic influenza A viruses and evolution in United States swine results in viruses with zoonotic potential</atitle><jtitle>PLoS pathogens</jtitle><addtitle>PLoS Pathog</addtitle><date>2023-07-27</date><risdate>2023</risdate><volume>19</volume><issue>7</issue><spage>e1011476</spage><epage>e1011476</epage><pages>e1011476-e1011476</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>The 2009 H1N1 pandemic (pdm09) lineage of influenza A virus (IAV) crosses interspecies barriers with frequent human-to-swine spillovers each year. These spillovers reassort and drift within swine populations, leading to genetically and antigenically novel IAV that represent a zoonotic threat. We quantified interspecies transmission of the pdm09 lineage, persistence in swine, and identified how evolution in swine impacted zoonotic risk. Human and swine pdm09 case counts between 2010 and 2020 were correlated and human pdm09 burden and circulation directly impacted the detection of pdm09 in pigs. However, there was a relative absence of pdm09 circulation in humans during the 2020-21 season that was not reflected in swine. During the 2020-21 season, most swine pdm09 detections originated from human-to-swine spillovers from the 2018-19 and 2019-20 seasons that persisted in swine. We identified contemporary swine pdm09 representatives of each persistent spillover and quantified cross-reactivity between human seasonal H1 vaccine strains and the swine strains using a panel of monovalent ferret antisera in hemagglutination inhibition (HI) assays. The swine pdm09s had variable antigenic reactivity to vaccine antisera, but each swine pdm09 clade exhibited significant reduction in cross-reactivity to one or more of the human seasonal vaccine strains. Further supporting zoonotic risk, we showed phylogenetic evidence for 17 swine-to-human transmission events of pdm09 from 2010 to 2021, 11 of which were not previously classified as variants, with each of the zoonotic cases associated with persistent circulation of pdm09 in pigs. These data demonstrate that reverse-zoonoses and evolution of pdm09 in swine results in viruses that are capable of zoonotic transmission and represent a potential pandemic threat.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>37498825</pmid><doi>10.1371/journal.ppat.1011476</doi><tpages>e1011476</tpages><orcidid>https://orcid.org/0000-0002-3138-5535</orcidid><orcidid>https://orcid.org/0000000231385535</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1553-7374 |
| ispartof | PLoS pathogens, 2023-07, Vol.19 (7), p.e1011476-e1011476 |
| issn | 1553-7374 1553-7366 1553-7374 |
| language | eng |
| recordid | cdi_plos_journals_2851954389 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central Open Access; Public Library of Science (PLoS); PubMed Central |
| subjects | Animal populations Animals Antigens Antisera Biology and Life Sciences Complications and side effects Computer and Information Sciences Cross-reactivity Diagnosis Evolution Ferrets Genes Genetic diversity Genomes Health aspects Hemagglutination inhibition Hogs Humans Immune Sera Influenza Influenza A Influenza A virus Influenza A Virus, H1N1 Subtype - genetics Influenza, Human - epidemiology Medicine and health sciences Orthomyxoviridae Infections - epidemiology Orthomyxoviridae Infections - veterinary Pandemics Phylogenetics Phylogeny Population genetics Regression analysis Risk factors Seasons Strains (organisms) Swine Swine Diseases Swine influenza United States - epidemiology Vaccines Viruses Zoonoses Zoonoses - epidemiology |
| title | Reverse-zoonoses of 2009 H1N1 pandemic influenza A viruses and evolution in United States swine results in viruses with zoonotic potential |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-18T11%3A48%3A32IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Reverse-zoonoses%20of%202009%20H1N1%20pandemic%20influenza%20A%20viruses%20and%20evolution%20in%20United%20States%20swine%20results%20in%20viruses%20with%20zoonotic%20potential&rft.jtitle=PLoS%20pathogens&rft.au=Markin,%20Alexey&rft.date=2023-07-27&rft.volume=19&rft.issue=7&rft.spage=e1011476&rft.epage=e1011476&rft.pages=e1011476-e1011476&rft.issn=1553-7374&rft.eissn=1553-7374&rft_id=info:doi/10.1371/journal.ppat.1011476&rft_dat=%3Cgale_plos_%3EA759349361%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2851954389&rft_id=info:pmid/37498825&rft_galeid=A759349361&rfr_iscdi=true |