Breeding pig transport drives the dispersal of swine influenza A virus across Europe

Abstract

Pigs serve as reservoirs of former human influenza A virus (IAV) H1N1 and H3N2 lineages and act as mixing vessels for diverse strains, facilitating the emergence of novel IAVs. Understanding the spread and evolution of swine IAVs (swIAVs) is therefore crucial to assess the risk of strains with zoonotic potential emerging. This study uses a phylogeographic framework to investigate the predictors of swIAV dispersal across Europe. All publicly available swIAV genomic sequences were retrieved and subsampled for the ten largest European pig-producing countries. Discrete phylogeographic reconstructions were conducted for H1, H3, N1, N2 encoding genes and all internal gene segments. Our analyses indicate that viral dispersal predominantly occurred from north-western to southern and eastern Europe, with frequent long-distance transitions between non-adjacent countries. We also extended the discrete phylogeographical analyses with generalized linear models to test the association between viral movement and potential predictors, such as live pig trade, pork trade, pig densities, farm sizes, or the geographic distance between key pig production zones. We find that breeding pig trade is the only consistently well-supported predictor of between-country transition events, whereas pork trade and geographic distance were not supported. This highlights that farms importing breeding pigs from multiple countries could act as hotspots for reassortment of diverse swIAV strains. Strengthening external biosecurity on farms with emphasis on quarantining breeding pigs, limiting long-distance transport, and implementing a One Health surveillance system for earlier detection of emerging strains, could help curb the rapid spread and evolution of swIAV in Europe. Author summaryInfluenza A viruses that originally came from humans are now circulating in pigs. This is a public health concern because these viruses continue to evolve in pigs and may eventually return to humans in new forms that could cause more severe disease. To better prevent this risk, we need to understand the dispersal dynamics of influenza viruses infecting pigs. For this purpose, we retrieved all publicly available European swine influenza A virus genomic sequences. Using this genomic dataset, we reconstructed how the virus has spread across Europe and investigated the external factors that may have driven the spread. Our results indicate that swine influenza A viruses frequently spread between European countries, in particular from north-western to southern and eastern Europe, and that the trade of pigs intended for breeding is strongly associated with these patterns of spread. Consequently, measures such as quarantining of breeding pigs, could help preventing swine influenza variants from spreading between and becoming established in new regions. We also find major gaps in available genomic data from several European countries. We therefore recommend stronger European surveillance programs that include monitoring influenza viruses in both animals and humans to improve early detection of new emerging viral variants.