Our findings highlight the limitations of relying on visual examination for ILI to identify pigs infected with influenza virus A at agricultural fairs. Subclinical influenza virus A infections predominated among the pigs we tested, with subclinical infections detected among pigs at 10/53 (18.9%) participating fairs during 2009–2011. These findings may explain the frequency of variant influenza virus A infections among humans who have only been exposed to apparently healthy swine at fairs.
Agricultural fairs are often the face of agriculture to the general public. The International Association of Fairs and Expositions estimates annual attendance at fairs in North America to be 150 million persons (The Association, pers. comm.). Agricultural fairs have been occurring in the United States since 1811 (23
) and are special community events with a strong tradition and history of celebrating agricultural heritage and achievement (24
). As the agricultural workforce has decreased to <2% of the US population (25
), fairs have added educational programs to showcase advancements in food production systems in an effort to maintain attendance (26
) and meet societal needs. These much-needed educational efforts often provide an opportunity for attendees to have direct contact with all facets of agriculture, including pork production. Many of these persons would not otherwise have any exposure to swine and the pathogens they harbor, so their close contact with pigs at fairs may play multiple roles in the transmission of influenza A viruses: they may pass human-origin influenza virus A to swine, leading to novel reassortant viruses; they may serve as early sentinels by becoming infected first with a novel swine-origin influenza A virus; or they may disseminate a novel swine-origin influenza virus A in their local communities (27
The long duration of many agricultural fairs (3–10 days) is distinctly different than other swine concentration points or commingling events (i.e., abattoirs, markets, auctions, or shows), where interactions are limited to hours. In addition to their long duration, agricultural fairs also enable the comingling of pigs from multiple locations and various production systems (backyard to intensive commercial) at 1 site. Exhibition swine are commonly a unique population of noncommercial swine, reared by the use of management practices that differ greatly from standard commercial swine production practices (28
). These pigs likely have varying levels of immunity to influenza virus A and may bring a variety of influenza virus A strains with them to the fair, where the viruses can spread to other pigs, possibly reassort, and potentially transmit to humans.
Swine-to-human transmission of influenza virus A has been sporadically reported worldwide (11
), but the true incidence of this transmission is unknown. The Centers for Disease Control and Prevention reported that 36 humans were infected with variant influenza virus A in the United States during December 2005–April 2012 (29
). Of these cases, 15 occurred after July 2011, and 6 cases, all involving infection with influenza A (H3N2) viruses containing the M gene from the influenza A(H1N1)pdm09 virus (H3N2v), were associated with exposure to swine at agricultural fairs. However, none of the implicated fairs reported signs of ILI in the pigs, and influenza virus A could not be isolated from the pigs that were suspected to be the sources because of delays and lack of the availability of the pigs. Nonetheless, it is possible that subclinical influenza infections in pigs at these swine–human interfaces played a key role in zoonotic infections.
The increased swine–human exposure occurring at agricultural fairs may also facilitate human-origin influenza A virus transmission to swine. The earliest reports of introductions of the influenza A(H1N1)pdm09 virus into the US swine herd occurred at the state fairs in Minnesota and South Dakota (30
). Human-to-swine transmission is credited as a primary source of the genetic diversity seen in currently circulating swine influenza virus strains (32
). Human-to-swine transmission of influenza virus A can be economically devastating for the pork industry because of decreased domestic sales, restrictions imposed by export partners, and production losses due to disease. Agricultural fairs may provide a conduit to introduce human-origin influenza virus A into the US swine herd.
No human cases of variant influenza A associated with any of the agricultural fairs included in this study were reported, even though influenza A (H3N2) viruses containing the M gene from the influenza A(H1N1)pdm09 virus were recovered from pigs at 6 of the participating fairs in 2011. However, the number of confirmed H3N2v cases dramatically increased during the summer of 2012, with most cases epidemiologically linked to swine exposure occurring at agricultural fairs (35
The HA, NA, and M gene combinations of the influenza virus A isolates recovered from 155/1,073 (14.4%) sampled pigs were consistent with influenza virus A concurrently circulating in the US swine population (37
). The high frequency of virus isolation from the pigs at the 12 fairs at which influenza virus A was found is likely due to sample collection occurring at the end of the exhibition period, ≈5–7 days after arrival, which probably coincided with peak viral shedding in the swine population.
A limitation of the study is that extrapolating the findings to other Ohio fairs and fairs in other states may not be possible because of the selection bias and inherent variability among agricultural fairs. Although the fairs where influenza virus A was recovered were diverse regarding the predetermined selection criteria (data not shown), the participating fairs were included in the study because they were ranked relatively high among Ohio fairs within >1 selection category. Expanded surveillance efforts for agricultural fairs are underway to more accurately estimate the true prevalence of influenza virus A infections among swine at agricultural fairs in Ohio. Recognized risk factors and accurate prevalence estimates are needed to lay the foundation for studies investigating potential interventions to decrease the probability of swine-to-human and human-to-swine transmission of influenza virus A at agricultural fairs.
The subclinical influenza virus A infections identified in this study would not be detected by the current national swine influenza virus surveillance program (39
), which is passive and focuses on swine showing signs of ILI and on reacting to reports of variant influenza A cases in humans (39
). Thus, subclinical influenza virus A infections among pigs are likely underreported. This passive surveillance strategy does not adequately describe the breadth of influenza virus A circulating in swine because it does not identify less virulent strains of influenza virus A (40
) and does not collect metadata on host, environmental, and agent factors that affect severity of illness. Therefore, to accurately capture the risk influenza virus A in swine populations presents to swine and public health, surveillance efforts should include healthy and clinically ill pigs.
Reducing bidirectional zoonotic transmission of influenza virus A between pigs and humans is crucial to agriculture and biomedicial science. Unfortunately, little scientific evidence exists on which to base changes in policies and management practices to reduce the risk for interspecies transmission of influenza virus A between pigs and humans. This investigation highlights the need for additional studies to quantify the risk for interspecies influenza A virus transmission at fairs and to evaluate interventions to mitigate the risk.
Potential strategies to mitigate the risk for intra- and interspecies transmission of influenza virus A at fairs on the swine side of the human-swine interface include shortening the swine exhibition period, preventing interfair movement of pigs, and vaccinating exhibition swine for appropriate influenza A viruses. Recommendations have previously been made for mitigating risk on the human side of the human–swine interface (www.cdc.gov/flu/swineflu
). Expanded risk assessments at agricultural fairs will provide animal and public health officials with scientific data that will enable them to make appropriate decisions to protect animal and public health while still furthering appreciation and understanding of agriculture and ensuring our future food security.