Subclinical Influenza Virus A Infections in Pigs Exhibited at Agricultural Fairs, Ohio, USA, 2009–2011

Andrew S. Bowman

, Jacqueline M. Nolting, Sarah W. Nelson, and Richard D. Slemons

Author affiliations: The Ohio State University, Columbus, Ohio, USA

Abstract

Agricultural fairs are associated with bidirectional, interspecies transmission of influenza virus A between humans and pigs. We examined pigs exhibited at agricultural fairs in Ohio during 2009–2011 for signs of influenza-like illness and collected nasal swab specimens from a representative subset of these animals. Influenza virus A was recovered from pigs at 12/53 (22.6%) fairs during the 3-year sampling period. Pigs at 10/12 (83.3%) fairs from which influenza virus A was recovered did not show signs of influenza-like illness. Hemagglutinin, neuraminidase, and matrix gene combinations of the isolates were consistent with influenza virus A concurrently circulating among swine herds in the United States. Subclinical influenza virus A infections in pigs at agricultural fairs may pose a risk to human health and create challenges for passive surveillance programs for influenza virus A in swine herds.

Awareness of bidirectional zoonotic transmission of influenza virus A between pigs and humans was heightened by the emergence of the influenza A(H1N1)pdm09 virus, which resulted in an influenza pandemic among humans starting in 2009. Interspecies transmission of influenza virus A is believed to be a principal mechanism contributing to the emergence of novel influenza virus A strains that pose a threat to human and swine health (1,2). Pig respiratory tracts have receptors for swine-, human-, and avian-origin influenza virus A, which facilitates genomic reassortment among viruses from multiple host species. As a result, swine have been identified as mixing vessels for influenza virus A and a source of emergence for novel viruses (3).
For >60 years after its identification as a swine pathogen, influenza virus A circulating among North American swine was predominantly the H1N1 subtype (4). In 1998, triple-reassortant influenza virus A (H3N2), containing genes originating from swine-, human-, and avian-origin influenza virus A, was identified among swine in the United States (5). This lineage quickly became established among North American swine (6), and the 6 gene segments coding for internal proteins, including the matrix (M) gene, subsequently served as a common backbone for many new reassortant viruses appearing among pigs (7). Various subtype H1N1, H1N2, and H3N2 influenza virus A lineages continue to cocirculate and evolve among North American swine (6–9).
Swine are a source of novel and existing influenza virus A strains that infect humans (10–13). These strains pose a pandemic threat if they become capable of being transmitted efficiently from person to person and if limited protective immunity exists in the human population. Bidirectional zoonotic transmission of influenza virus A strains usually involves close contact between humans and swine. The United States has 3 major swine–human interfaces: commercial swine production, abattoirs, and agricultural fairs. Agricultural fairs are unique because they facilitate prolonged commingling of pigs from numerous sources raised under varied management programs with millions of persons who have widely disparate histories of exposure to various influenza viruses. This situation creates an environment conducive to zoonotic transmission of influenza virus A.
More persons come in contact with live swine at agricultural fairs than in any other setting in the United States, and several human cases of influenza A have been linked to swine exposure occurring at fairs. In 1988, a woman died of infection with a variant influenza virus A (H1N1) that she acquired while attending a Wisconsin fair where numerous pigs showed signs of influenza-like illness (ILI); a follow-up investigation identified more human infections (14). In Ohio, human infections with variant influenza virus A after exposure to pigs with ILI were detected at the 1988 Ohio State Fair, 2 weeks before the Wisconsin case was reported (R.D. Slemons, unpub. data), and more recently at the 2007 Huron County Fair (15).
Because of dynamic human and swine populations at fairs and the number of human influenza A cases associated with swine exposure that occurs at fairs (13–15), we hypothesized that influenza virus A infections in swine occur undetected at agricultural fairs. This study was initiated after the emergence of influenza A(H1N1)pdm09 to actively monitor the antigenic and genomic properties of influenza virus A among pigs at agricultural fairs in Ohio, with a goal of protecting the health of swine and the public.