Ecological drivers of evolution of swine influenza in the United States: a review

Abstract

Influenza A viruses (IAVs) pose a major public health threat due to their wide host range and pandemic potential. Pigs have been proposed as "mixing vessels" for avian, swine, and human IAVs, significantly contributing to influenza ecology. In the United States, IAVs are enzootic in commercial swine farming operations, with numerous genetic and antigenic IAV variants having emerged in the past two decades. However, the dynamics of intensive swine farming systems and their interactions with ecological factors influencing IAV evolution have not been systematically analysed. This review examines the evolution of swine IAVs in commercial farms, highlighting the role of multilevel ecological factors. A total of 61 articles published after 2000 were reviewed, with most studies conducted after 2009 in Midwestern US, followed by Southeast and South-central US. The findings reveal that ecological factors at multiple spatial scales, such as regional transportation networks, interconnectedness of swine operations, farm environments, and presence of high-density, low-genetic diversity herds, can facilitate virus transmission and enhance virus evolution. Additionally, interactions at various interfaces, such as between commercial swine and feral swine, humans, or wild birds contribute to the increase in genetic diversity of swine IAVs. The review underscores the need for comprehensive studies and improved data collection to better understand the ecological dynamics influencing swine IAV evolution. This understanding is crucial for mitigating disease burden in swine production and reducing the risk of zoonotic influenza outbreaks.

Keywords: H1N1; H3N2; Influenza A virus; commercial swine farm; ecology; evolution; swine Influenza virus.

Figure 1.

A typical commercial swine operation infrastructure. The operation begins with Great-Grand-Parents (GGP), genetically selected pigs that produce Grand-Parents (GP), who in turn breed parent pigs destined to replenish the population in Sow-Farms (SF). Male pigs are usually sent directly from weaning to Wean-to-Finish (WF) farms, while females are transferred to Gilt-Development-Units (GDU). The most suitable gilts from GDUs are then moved to SF, although some systems may place them in a replacement farm before their final transfer to SF. The farming practices vary across different systems, but the typical pathways post-farrowing at SF include: (i) from Nursery to Finisher farm, (ii) from Nursery to Nursery-to-Grower and then to Grower-to-Finish farm, and (iii) directly from SF to Wean-to-Finish (WF) farm. The figure was generated using Biorender and adapted from Hatuwal et al. [14].

Figure 2.

Flow diagram for article selection: out of 122 screened articles, 61 articles were considered eligible for inclusion into the scoping review. In addition to duplicates, other 61 records were excluded on a case-by-case basis.