Active Surveillance for Influenza A Virus among Swine, Midwestern United States, 2009–2011

Cesar A. Corzo, Marie Culhane

, Kevin Juleen, Evelyn Stigger-Rosser, Mariette F. Ducatez, Richard J. Webby, and James F. Lowe

Author affiliations: University of Minnesota, Saint Paul, Minnesota, USA (C.A. Corzo, M. Culhane, K. Juleen); St. Jude Children’s Research Hospital, Memphis, Tennessee, USA (E. Stigger-Rosser, M.F. Ducatez, R.J. Webby); Carthage Veterinary Services, Carthage, Illinois, USA (J.F. Lowe)

Abstract

Veterinary diagnostic laboratories identify and characterize influenza A viruses primarily through passive surveillance. However, additional surveillance programs are needed. To meet this need, an active surveillance program was conducted at pig farms throughout the midwestern United States. From June 2009 through December 2011, nasal swab samples were collected monthly from among 540 groups of growing pigs and tested for influenza A virus by real-time reverse transcription PCR. Of 16,170 samples, 746 were positive for influenza A virus; of these, 18.0% were subtype H1N1, 16.0% H1N2, 7.6% H3N2, and 14.5% (H1N1)pdm09. An influenza (H3N2) and (H1N1)pdm09 virus were identified simultaneously in 8 groups. This active influenza A virus surveillance program provided quality data and increased the understanding of the current situation of circulating viruses in the midwestern US pig population.

Influenza A virus has become a major pathogen, causing epidemics of respiratory disease in humans, which not only result in increased deaths but also raise public health organization alarms regarding the need for further understanding and control of this virus (1). Additionally, the ability of the virus to cross species barriers has raised more concern over the probability of reassortment and generation of highly transmissible viruses that might pose a threat to humans (2). Despite evidence of reassortment in other species, swine have been most often labeled as the “mixing vessel” because avian- and mammalian-type receptors for influenza A virus have been found in pig tracheas, making swine a potential source of new viruses through reassortment (3,4). Because these viruses can infect humans, influenza A virus in swine should be monitored for public health reasons (5).
In the United States, influenza A virus has been present in swine for almost a century (6). Within the US pig population, 3 major subtypes of influenza A virus (H1N1, H1N2, H3N2) circulate, causing widespread respiratory disease characterized by dry coughing, sneezing, fever, anorexia, rhinorrhea, and lethargy (7). Swine influenza viruses have been monitored through seroprevalence studies. Such studies from the 1970s through the 1990s revealed that influenza virus subtypes H1N1 and H3N2 circulated in the US pig population (8–11).
At the turn of the 21st century, 2 new viruses were detected in the swine population. These viruses were the result of either double or triple reassortment between human, avian, and swine viruses (11–13). Since 1998, circulating influenza viruses in pigs have been able to change because of mutations and the propensity for influenza A virus of swine with the triple reassortant genotype to frequently reassort and generate new genotypes, therefore increasing the diversity of influenza A virus in swine (14). Virologic and seroprevalence studies have provided valuable information about influenza A virus in swine, but the epidemiology of influenza A virus in swine is not fully understood.
Newly emerged pathogens can be detected through passive or active surveillance. Passive surveillance is driven by laboratory submission of samples after outbreaks of respiratory disease, whereas active surveillance is based on purposely collecting and screening field samples regardless of clinical status. In Asia, active surveillance for influenza conducted through collection of nasal swabs at slaughter plants has reportedly detected uncommon influenza viruses (i.e., subtypes H3N1, H7N2, H9N2) in the local pig population (15–17). In the United States, similar studies, following the same sample collection method, during the early and late 1990s have been reported (10,18). However, a surveillance program that will identify and report newly emerged viruses in a timely manner is still needed (14).
Overall, studies have elucidated epidemiologic features of the virus in swine, such as the constant circulation of influenza A virus in the swine population and sporadic infections with rare subtypes. However, absence of a proactive approach leaves a gap that needs to be filled (19). Therefore, the objectives of this study were to 1) conduct an active surveillance program to better characterize the presence of influenza viruses in the swine population and 2) make live viruses available for genetic characterization, potential vaccine, and diagnostic use. Procedures and protocols used in this study were approved by the University of Minnesota Institutional Animal Care and Use Committee