{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,22]],"date-time":"2026-09-22T10:49:59Z","timestamp":1790074199781,"version":"4.0.1"},"reference-count":34,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2024,12,16]],"date-time":"2024-12-16T00:00:00Z","timestamp":1734307200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell. Infect. Microbiol."],"abstract":"<jats:p>Swine influenza virus (SIV) is a highly contagious pathogen that poses significant economic challenges to the swine industry and carries zoonotic potential, underscoring the need for vigilant surveillance. In this study, we performed a comprehensive genetic and molecular analysis of H3N2 SIV isolates obtained from 372 swine samples collected in Shandong Province, China. Phylogenetic analysis revealed two distinct genotypes. The surface genes of both genotypes clustered with the human-like H3N2 lineage, while the internal genes of one genotype clustered with the 2009 pandemic H1N1 (pdm\/09) lineage. In the second genotype, the NS gene clustered with the classical swine (CS) H1N1 lineage, while the remaining internal genes clustered with pdm\/09, suggesting stable integration of pdm\/09 gene segments into H3N2 SIV. Homology analysis showed over 96% genetic similarity between the isolates and reference strains from China and Brazil, suggesting potential transmission through swine trade or human movement. Molecular characterization identified amino acid substitutions in the HA protein (190D, 226I, and 228S), potentially enhancing the virus\u2019s affinity for human-like receptors, thereby increasing the zoonotic risk. Key mutations in the PB2 (271A, 591R), PA (336M, 356R, 409N), and M2 (S31N) proteins, along with novel drug resistance mutations, indicate the potential for enhanced virulence and drug resistance in these isolates. Moreover, glycosylation site analysis revealed four differences, and antigenic site analysis showed 13 differences between the HA proteins of the isolates and the WHO-recommended vaccine strain A\/Cambodia\/E0826360\/2020 for the 2021\u20132022 season, which may reduce vaccine efficacy. Serological analysis revealed that 11 out of the tested serum samples were positive for H3N2 antibodies, resulting in an overall positivity rate of 0.42%. These findings emphasize the urgent need for strengthened SIV surveillance in China to monitor the risk of human transmission and ensure better preparedness for future influenza outbreaks.<\/jats:p>","DOI":"10.3389\/fcimb.2024.1517023","type":"journal-article","created":{"date-parts":[[2024,12,15]],"date-time":"2024-12-15T19:10:12Z","timestamp":1734289812000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":8,"title":["Two genotypes of H3N2 swine influenza viruses identified in pigs from Shandong Province, China"],"prefix":"10.3389","volume":"14","author":[{"given":"Yuzhong","family":"Zhao","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lebin","family":"Han","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haotian","family":"Sang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pingping","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yanmeng","family":"Hou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yihong","family":"Xiao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2024,12,16]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"a038737","DOI":"10.1101\/cshperspect.a038737","article-title":"Swine influenza A viruses and the tangled relationship with humans","volume":"11","author":"Anderson","year":"2021","journal-title":"Cold Spring Harb. Perspect. Med."},{"key":"B2","doi-asserted-by":"publisher","first-page":"1195","DOI":"10.1007\/s11250-015-0848-x","article-title":"Molecular characterization of H9N2 avian influenza viruses isolated from vaccinated broiler chickens in northeast Iran","volume":"47","author":"Bahari","year":"2015","journal-title":"Trop. Anim. Health Prod"},{"key":"B3","doi-asserted-by":"publisher","first-page":"1472","DOI":"10.3201\/eid2009.131082","article-title":"Swine-to-human transmission of influenza A(H3N2) virus at agricultural fairs, Ohio, USA, 2012","volume":"20","author":"Bowman","year":"2014","journal-title":"Emerg. Infect. Dis."},{"key":"B4","doi-asserted-by":"publisher","first-page":"503","DOI":"10.1006\/viro.1993.1155","article-title":"Genetic reassortment between avian and human influenza A viruses in Italian pigs","volume":"193","author":"Castrucci","year":"1993","journal-title":"Virology"},{"key":"B5","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pmed.1001399","article-title":"Using routine surveillance data to estimate the epidemic potential of emerging zoonoses: Application to the emergence of US swine origin influenza A H3N2v virus","volume":"10","author":"Cauchemez","year":"2013","journal-title":"PloS Med."},{"key":"B6","doi-asserted-by":"publisher","first-page":"1068","DOI":"10.1016\/j.bios.2010.08.060","article-title":"Detection of swine-origin influenza A (H1N1) viruses using a localized surface plasmon coupled fluorescence fiber-optic biosensor","volume":"26","author":"Chang","year":"2010","journal-title":"Biosens Bioelect."},{"key":"B7","doi-asserted-by":"publisher","first-page":"47","DOI":"10.3390\/v14010047","article-title":"Genetic variability among swine influenza viruses in Italy: Data analysis of the period 2017\u20132020","volume":"14","author":"Chiapponi","year":"2021","journal-title":"Viruses"},{"key":"B8","doi-asserted-by":"publisher","first-page":"1755","DOI":"10.1093\/molbev\/msq317","article-title":"Charting the host adaptation of influenza viruses","volume":"28","author":"dos Reis","year":"2011","journal-title":"Mol Biol Evol."},{"key":"B9","doi-asserted-by":"publisher","first-page":"2375","DOI":"10.1128\/JVI.06824-11","article-title":"Emergence and dissemination of a swine H3N2 reassortant influenza virus with 2009 pandemic H1N1 genes in pigs in China","volume":"86","author":"Fan","year":"2012","journal-title":"J. Virol."},{"key":"B10","doi-asserted-by":"publisher","first-page":"571","DOI":"10.1016\/j.tips.2013.08.003","article-title":"Structural and energetic analysis of drug inhibition of the influenza A M2 proton channel","volume":"34","author":"Gu","year":"2013","journal-title":"Trends Pharmacol. Sci."},{"key":"B11","doi-asserted-by":"publisher","first-page":"40","DOI":"10.16437\/j.cnki.1007-5038.2020.12.008","article-title":"Genetic analysis and virulence of H7N9 influenza A viruses isolated from chickens and humans in mice","volume":"41","author":"Guo","year":"2020","journal-title":"Prog. Vet. Med."},{"key":"B12","doi-asserted-by":"publisher","first-page":"85","DOI":"10.1038\/s41426-018-0088-z","article-title":"Novel triple-reassortant influenza viruses in pigs, Guangxi, China","volume":"7","author":"He","year":"2018","journal-title":"Emerg. Microbes Infect."},{"key":"B13","doi-asserted-by":"publisher","first-page":"121","DOI":"10.2147\/IDR.S105473","article-title":"Drug resistance in influenza A virus: The epidemiology and management","volume":"10","author":"Hussain","year":"2017","journal-title":"Infect. Drug Resist."},{"key":"B14","doi-asserted-by":"publisher","first-page":"307","DOI":"10.1016\/S0166-3542(02)00053-0","article-title":"The H274Y mutation in the influenza A\/H1N1 neuraminidase active site following oseltamivir phosphate treatment leaves virus severely compromised both in vitro and in vivo","volume":"55","author":"Ives","year":"2002","journal-title":"Antiviral Res."},{"key":"B15","doi-asserted-by":"publisher","first-page":"1703","DOI":"10.1093\/cid\/cit649","article-title":"Outbreak of variant influenza A(H3N2) virus in the United States","volume":"57","author":"Jhung","year":"2013","journal-title":"Clin. Infect. Dis."},{"key":"B16","doi-asserted-by":"publisher","first-page":"10864","DOI":"10.1128\/JVI.01327-14","article-title":"Expansion of genotypic diversity and establishment of 2009 H1N1 pandemic-origin internal genes in pigs in China","volume":"88","author":"Liang","year":"2014","journal-title":"J. Virol."},{"key":"B17","doi-asserted-by":"publisher","first-page":"174","DOI":"10.1016\/j.jinf.2019.04.015","article-title":"A human infection with a novel reassortant H3N2 swine virus in China","volume":"79","author":"Lu","year":"2019","journal-title":"J. Infect."},{"key":"B18","doi-asserted-by":"publisher","first-page":"2831","DOI":"10.1128\/JVI.03355-14","article-title":"Pathogenicity and transmissibility of novel reassortant H3N2 influenza viruses with 2009 pandemic H1N1 genes in pigs","volume":"89","author":"Ma","year":"2015","journal-title":"J. Virol."},{"key":"B19","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1016\/j.chom.2008.06.007","article-title":"An inhibitory activity in human cells restricts the function of an avian-like influenza virus polymerase","volume":"4","author":"Mehle","year":"2008","journal-title":"Cell Host Microbe"},{"key":"B20","doi-asserted-by":"publisher","first-page":"931","DOI":"10.1038\/nature08157","article-title":"Emergence and pandemic potential of swine-origin H1N1 influenza virus","volume":"459","author":"Neumann","year":"2009","journal-title":"Nature"},{"key":"B21","doi-asserted-by":"publisher","first-page":"1157","DOI":"10.15585\/mmwr.mm6542a1","article-title":"Outbreak of influenza A(H3N2) variant virus infections among persons attending agricultural fairs housing infected swine - Michigan and Ohio, July-August 2016","volume":"65","author":"Schicker","year":"2016","journal-title":"MMWR Morb Mortal Wkly Rep."},{"key":"B22","doi-asserted-by":"publisher","first-page":"S24","DOI":"10.1086\/jid.1997.176.issue-s1","article-title":"Effects of glycosylation on the properties and functions of influenza virus hemagglutinin","author":"Schulze","year":"1997","journal-title":"J. Infect. Dis."},{"key":"B23","doi-asserted-by":"publisher","first-page":"251","DOI":"10.1099\/0022-1317-44-1-251","article-title":"Further studies of the antigenic properties of H3N2 strains of influenza A isolated from swine in South East Asia","volume":"44","author":"Shortridge","year":"1979","journal-title":"J. Gen. Virol."},{"key":"B24","doi-asserted-by":"publisher","first-page":"1454","DOI":"10.1126\/science.867041","article-title":"Persistence of Hong Kong influenza virus variants in pigs","volume":"196","author":"Shortridge","year":"1977","journal-title":"Science"},{"key":"B25","doi-asserted-by":"publisher","first-page":"213","DOI":"10.1016\/j.cell.2013.05.052","article-title":"Lipidomic profiling of influenza infection identifies mediators that induce and resolve inflammation","volume":"154","author":"Tam","year":"2013","journal-title":"Cell"},{"key":"B26","doi-asserted-by":"crossref","first-page":"590","DOI":"10.1111\/j.1439-0450.1976.tb00697.x","article-title":"Serological evidence and isolation of a virus closely related to the human A\/Hong Kong\/68 (H3N2) strain in swine populations in CzechoSlovakia in 1969\u20131972","volume":"23","author":"T\u0169mov\u00e1","year":"1976","journal-title":"Zentralbl Veterinarmed B"},{"key":"B27","doi-asserted-by":"publisher","first-page":"2063","DOI":"10.1093\/molbev\/mss095","article-title":"Detecting patches of protein sites of influenza A viruses under positive selection","volume":"29","author":"Tusche","year":"2012","journal-title":"Mol. Biol. Evol."},{"key":"B28","doi-asserted-by":"publisher","first-page":"4","DOI":"10.1111\/zph.2014.61.issue-1","article-title":"Review of influenza A virus in swine worldwide: A call for increased surveillance and research","volume":"61","author":"Vincent","year":"2014","journal-title":"Zoonoses Public Health"},{"key":"B29","doi-asserted-by":"publisher","first-page":"152","DOI":"10.1128\/mr.56.1.152-179.1992","article-title":"Evolution and ecology of influenza A viruses","volume":"56","author":"Webster","year":"1992","journal-title":"Microbiol Rev."},{"key":"B30","doi-asserted-by":"publisher","first-page":"224","DOI":"10.1016\/j.vetmic.2014.11.031","article-title":"Two different genotypes of H1N2 swine influenza virus isolated in northern China and their pathogenicity in animals","volume":"175","author":"Yang","year":"2015","journal-title":"Vet Microbiol."},{"key":"B31","doi-asserted-by":"publisher","first-page":"40","DOI":"10.19958\/j.cnki.cn31-2031\/s.20210611.002","article-title":"Isolation, identification and pathogenicity in mice of A H1N1 subtype swine influenza virus","volume":"31","author":"Zhang","year":"2023","journal-title":"Chinese J. Animal Infectious Dis."},{"key":"B32","first-page":"1693","article-title":"Phylogenetic and molecular characterization of H1N1 influenza A viruses from pigs in China","volume":"67","author":"Zhao","year":"2020","journal-title":"Transbound Emerg. Dis."},{"key":"B33","doi-asserted-by":"publisher","first-page":"194","DOI":"10.19958\/j.cnki.cn31-2031\/s.20210826.002","article-title":"Key amino acid sites affecting the pathogenicity and transmission of swine influenza virus","volume":"31","author":"Zhao","year":"2023","journal-title":"Chinese J. Animal Infectious Dis."},{"key":"B34","doi-asserted-by":"publisher","first-page":"8851","DOI":"10.1128\/JVI.73","article-title":"Genetic reassortment of avian, swine, and human influenza A viruses in American pigs","volume":"73","author":"Zhou","year":"1999","journal-title":"J Virol."}],"container-title":["Frontiers in Cellular and Infection Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2024.1517023\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,1,2]],"date-time":"2025-01-02T09:15:12Z","timestamp":1735809312000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2024.1517023\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,12,16]]},"references-count":34,"alternative-id":["10.3389\/fcimb.2024.1517023"],"URL":"https:\/\/doi.org\/10.3389\/fcimb.2024.1517023","relation":{},"ISSN":["2235-2988"],"issn-type":[{"value":"2235-2988","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,12,16]]},"article-number":"1517023"}}