The emergence in humans of the A(H1N1)pdm09 influenza virus, a complex reassortant virus of swine origin, highlighted the importance of worldwide influenza virus surveillance in swine. To date, large-scale surveillance studies have been reported for southern China and North America, but such data has not yet been described for Europe. We report the first large-scale genomic characterization of 290 swine influenza viruses collected from 14 European countries between 2009 and 2013. 23 distinct genotypes were identified, with the seven most common comprising 82% of the incidence. Contrasting epidemiological dynamics were observed for two of these genotypes, H1_huN2 and H3N2, with the former showing multiple long-lived geographically-isolated lineages, whilst the latter had short-lived geographically-diffuse lineages. At least 32 human-swine transmission events have resulted in A(H1N1)pdm09 becoming established at a mean frequency of 8% across European countries. Notably, swine in the UK have largely had a replacement of the endemic Eurasian ´avian-like´ genotypes with A(H1N1)pdm09-derived genotypes. The high number of reassortant genotypes observed in European swine, combined with the identification of a genotype similar to the A(H3N2)v in North America, underlines the importance of continued swine surveillance in Europe for the purposes of public health. This study further reveals that the emergence and drivers of virus evolution in swine differ at a global level.

IMPORTANCE:

The influenza A(H1N1)pdm09 virus contains a reassortant genome with segments derived from separate virus lineages that evolved in different regions of world. In particular its neuraminidase and matrix segments were derived from the Eurasian ´avian-like´ lineage that emerged in European swine in the 1970s. However, while large-scale genomic characterization of swine has been reported for southern China and North America, no equivalent study has yet been reported for Europe. Surveillance of swine herds across Europe between 2009 and 2013 revealed that the A(H1N1)pdm09 virus is established in European swine, increasing the number of circulating lineages in the region and increasing the possibility of the emergence of a genotype with human pandemic-potential. It also has implications for veterinary health, making prevention through vaccination more challenging. The identification of a genotype similar to the A(H3N2)v, causing zoonoses at North American agricultural fairs, underlines the importance of continued genomic characterization in European swine.