Multiple introductions of #equine #influenza virus into the #UK resulted in widespread #outbreaks and #lineage #replacement

Abstract

Influenza A viruses (IAVs) are prime examples of emerging viruses in humans and animals. IAV circulation in domestic animals poses a pandemic risk as it provides new opportunities for zoonotic infections. The recent emergence of H5N1 IAV in cows and subsequent spread over multiple states within the USA, together with reports of spillover infections in humans, cats and mice highlight this issue. The horse is a domestic animal in which an avian-origin IAV lineage has been circulating for >60 years. In 2018/19, a Florida Clade 1 (FC1) virus triggered one of the largest epizootics recorded in the UK, which led to the replacement of the Equine Influenza Virus (EIV) Florida Clade 2 (FC2) lineage that had been circulating in the country since 2003. We integrated geographical, epidemiological, and virus genetic data to determine the virological and ecological factors leading to this epizootic. By combining newly-sequenced EIV complete genomes derived from UK outbreaks with existing genomic and epidemiological information, we reconstructed the nationwide viral spread and analysed the global evolution of EIV. We show that there was a single EIV FC1 introduction from the USA into Europe, and multiple independent virus introductions from Europe to the UK. At the UK level, three English regions (East, West Midlands, and North-West) were the main sources of virus during the epizootic, and the number of affected premises together with the number of horses in the local area were found as key predictors of viral spread within the country. At the global level, phylogeographic analysis evidenced a source-sink model for intercontinental EIV migration, with a source population evolving in the USA and directly or indirectly seeding viral lineages into sink populations in other continents. Our results provide insight on the underlying factors that influence IAV spread in domestic animals.

Author summary

Influenza causes significant disease burden in animals, including wild birds, sea lions, pigs, horses, dogs, and more recently, cows. Outbreaks and epizootics of influenza in agricultural species are a threat to food security and the economy whereas in wild animals they could affect biodiversity and conservation efforts. Given the zoonotic nature of influenza viruses and the high levels of contact between domestic animals and humans, animal influenza is also a public health concern. Here, we combined geographical, epidemiological, and virus sequence data to determine key factors that led to one of the largest epizootics of equine influenza in the United Kingdom in decades. We show that an American equine influenza virus lineage was introduced into Europe and replaced the virus lineage that had been circulating in the United Kingdom for nearly 20 years. We also analysed a global dataset of virus genomes and propose a model of equine influenza virus intercontinental migration, in which USA is the main source of viruses to other countries. Our results provide important information concerning the basic principles of influenza virus circulation in animal populations. This is central to devise effective measures of disease control that would increase animal health while reducing zoonotic risk.

Source: PLoS Pathogens, https://journals.plos.org/plospathogens/article?id=10.1371/journal.ppat.1013227

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