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Virus Evol . Major change in swine influenza virus diversity in France owing to emergence and widespread dissemination of a newly introduced H1N2 1C

tetano

Editor, Senior Moderator
Virus Evol


. 2024 Dec 14;11(1):veae112.
doi: 10.1093/ve/veae112. eCollection 2025. Major change in swine influenza virus diversity in France owing to emergence and widespread dissemination of a newly introduced H1N2 1C genotype in 2020

Gautier Richard[SUP] 1 [/SUP], Séverine Hervé[SUP] 1 [/SUP], Amélie Chastagner[SUP] 1 [/SUP], Stéphane Quéguiner[SUP] 1 [/SUP], Véronique Beven[SUP] 2 [/SUP], Edouard Hirchaud[SUP] 2 [/SUP], Nicolas Barbier[SUP] 1 [/SUP], Stéphane Gorin[SUP] 1 [/SUP], Yannick Blanchard[SUP] 2 [/SUP], Gaëlle Simon[SUP] 1 [/SUP]



Affiliations
Abstract

Swine influenza A viruses (swIAVs) are a major cause of respiratory disease in pigs worldwide, presenting significant economic and health risks. These viruses can reassort, creating new strains with varying pathogenicity and cross-species transmissibility. This study aimed to monitor the genetic and antigenic evolution of swIAV in France from 2019 to 2022. Molecular subtyping revealed a marked increase in H1[SUB]av[/SUB]N2 cases from 2020 onwards, altering the previously stable subtypes' distribution. Whole-genome sequencing and phylogenetic analyses of H1[SUB]av[/SUB] (1C) strains identified 10 circulating genotypes, including 5 new genotypes. The most predominant genotype from 2020 onwards, denominated H1[SUB]av[/SUB]N2#E, was characterized by an HA-1C.2.4, an N2-Gent/84, and internal protein-encoding genes belonging to a newly defined subclade within the Eurasian avian-like (EA) lineage termed EA-DK. H1[SUB]av[/SUB]N2#E emerged in Brittany, the country's most pig-dense region, and rapidly became the most frequently detected swIAV genotype across France. This drastic change in the swIAV lineage proportions at a national scale was unprecedented, making H1[SUB]av[/SUB]N2#E a unique case for understanding swIAV evolution and spreading patterns. Phylogenetic analyses suggested an introduction of the H1[SUB]av[/SUB]N2#E genotype from a restricted source, likely originating from Denmark. It spread rapidly with low genetic diversity at the start of the epizootic in 2020, showing increasing diversification in 2021 and 2022 as the inferred population size grew and stabilized, and exhibited reassortments with other enzootic genotypes. Amino acid sequence alignments of H1[SUB]av[/SUB]N2#E antigenic sites revealed major mutations and deletions compared to commercial vaccine 1C strain (HA-1C.2.2) and previously predominant H1[SUB]av[/SUB]N1 strains (HA-1C.2.1). Antigenic cartography confirmed significant antigenic distances between H1[SUB]av[/SUB]N2#E and other 1C strains, suggesting that the new genotype has escaped the pre-existing immunity of the swine population. Epidemiologically, the H1[SUB]av[/SUB]N2#E virus exhibited epizootic hallmarks with more severe clinical outcomes compared to H1[SUB]av[/SUB]N1 viruses. These factors likely contributed to the spread of H1[SUB]av[/SUB]N2#E within the pig population. The rapid rise of H1[SUB]av[/SUB]N2#E highlighted the dynamic nature of swIAV genetic and antigenic diversity, underscoring the importance of tailored surveillance programs to support risk assessment during potential new outbreaks. It also demonstrates the need to strengthen biosecurity measures when introducing pigs into a herd, including swIAV positivity assessment followed by quarantine, and restrict the trade of swIAV-excreting live swine between European countries.

Keywords: Eurasian avian–like lineage; H1N2; epizootic; genetic diversity; surveillance; swine influenza; virus evolution.

 
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