In the JournalsPerspective

Animal markets facilitate emergence of novel influenza A viruses

Live animal markets where people and swine were in proximity represented a potential source of novel influenza A viruses and interspecies transmission, according to recently published data.

“If efficiently transmitted among humans, novel [influenza A viruses (IAVs)] might have pandemic potential, prompting the need for public health and agriculture agencies to work with community groups, market employees and market customers to develop culturally appropriate messaging about the risk for variant IAV infections in these settings,” Mary J. Choi, MD, of the CDC, and colleagues wrote in Clinical Infectious Diseases. “Encouraging seasonal flu vaccination, educating customers about prevention measures against IAV and promoting the use of [personal protective equipment] among employees is also important.”

Over 12 weeks, Choi and colleagues conducted surveillance at two live animal markets in St. Paul, Minnesota. Both markets purchased swine with unknown influenza A vaccination status from multiple supplies several times a week, the researchers wrote. The researchers collected respiratory and environmental samples and performed real-time reverse transcription PCR (rRT-PCR), viral culture and whole genome sequencing on the samples. In addition, they collected paired serum samples from employees at the start and end of surveillance.

Seventeen employees participated, and 15 employees had direct contact with swine.

Nasal swabs from 65% of these employees were positive for influenza A viruses. One employee reported being ill the week before sample collection. On multiple occasions, seven employees tested positive for influenza A viruses by rRT-PCR.

Among the employees with direct swine contact, 73% had baseline hemagglutination-inhibition antibody titers greater than or equal to 40 for swine-origin IAVs, according to Choi and colleagues. One employee, a butcher, had fourfold titer increases in both hemagglutination inhibition and microneutralization assay antibody titers to swine H1N2 and A/Mexico/4108/2009 influenza A viruses. This employee neither received the seasonal influenza vaccine during the surveillance period nor reported any influenza-like illness, the investigators wrote. Results of swine and environmental surveillance showed that influenza A viruses were cultured in 72 of 84 swine lungs, in 30 of 45 air samples from the animal holding area, and on five of 21 pen railings.

Results of whole genome sequencing on 122 influenza A isolates from the swine and the environment indicated there were multiple strains and subtype codetections involved.

“We report that multiple IAV strains and subtypes were cocirculating, identified new viral reassortants and provided evidence indicating interspecies transmission of IAV from swine to persons,” Choi and colleagues wrote.– by Colleen Owens

Disclosure: The researchers report no relevant financial disclosures.

Live animal markets where people and swine were in proximity represented a potential source of novel influenza A viruses and interspecies transmission, according to recently published data.

“If efficiently transmitted among humans, novel [influenza A viruses (IAVs)] might have pandemic potential, prompting the need for public health and agriculture agencies to work with community groups, market employees and market customers to develop culturally appropriate messaging about the risk for variant IAV infections in these settings,” Mary J. Choi, MD, of the CDC, and colleagues wrote in Clinical Infectious Diseases. “Encouraging seasonal flu vaccination, educating customers about prevention measures against IAV and promoting the use of [personal protective equipment] among employees is also important.”

Over 12 weeks, Choi and colleagues conducted surveillance at two live animal markets in St. Paul, Minnesota. Both markets purchased swine with unknown influenza A vaccination status from multiple supplies several times a week, the researchers wrote. The researchers collected respiratory and environmental samples and performed real-time reverse transcription PCR (rRT-PCR), viral culture and whole genome sequencing on the samples. In addition, they collected paired serum samples from employees at the start and end of surveillance.

Seventeen employees participated, and 15 employees had direct contact with swine.

Nasal swabs from 65% of these employees were positive for influenza A viruses. One employee reported being ill the week before sample collection. On multiple occasions, seven employees tested positive for influenza A viruses by rRT-PCR.

Among the employees with direct swine contact, 73% had baseline hemagglutination-inhibition antibody titers greater than or equal to 40 for swine-origin IAVs, according to Choi and colleagues. One employee, a butcher, had fourfold titer increases in both hemagglutination inhibition and microneutralization assay antibody titers to swine H1N2 and A/Mexico/4108/2009 influenza A viruses. This employee neither received the seasonal influenza vaccine during the surveillance period nor reported any influenza-like illness, the investigators wrote. Results of swine and environmental surveillance showed that influenza A viruses were cultured in 72 of 84 swine lungs, in 30 of 45 air samples from the animal holding area, and on five of 21 pen railings.

Results of whole genome sequencing on 122 influenza A isolates from the swine and the environment indicated there were multiple strains and subtype codetections involved.

“We report that multiple IAV strains and subtypes were cocirculating, identified new viral reassortants and provided evidence indicating interspecies transmission of IAV from swine to persons,” Choi and colleagues wrote.– by Colleen Owens

Disclosure: The researchers report no relevant financial disclosures.

    Perspective
    Gregory C. Gray

    Gregory C. Gray

    In their pioneering study, Choi and colleagues have clearly demonstrated that the two live animal markets they studied in Minnesota are hot spots for influenza A virus transmission and likely sources for novel virus generation. The prevalence of influenza A they found in pigs, people and environmental samples was remarkably high. Especially alarming was the high prevalence (67%) of virus detected in air samples. If these viruses are freely moving in air in such settings, our understanding of swine barn biosecurity has been severely undermined. While it is clear there is a transmission risk in these markets, what about the risk in the farms from which these pigs came? This study reminds us of how a powerful, interdisciplinary One Health approach can shed new light on what has likely been an old problem the world over, namely influenza A transmission between humans and pigs. 

    Other recent reports have demonstrated efficient movement of influenza A viruses between pigs and man through modern agriculture methods and pig shows at state and county fairs. One wonders what other pig-human interactions may play roles in the ecology of influenza A. For instance, how frequently are U.S. swine workers sharing influenza A virus infections with pigs? Are influenza A viruses crossing species during the movement of pigs across state lines to the Midwest finishing farms? Are pork processing plant workers at risk for novel influenza virus infection? What human behaviors and animal husbandry practices have the strongest association with influenza A aerosolization?

    As we cannot feed the growing world’s population without modern agribusiness meat productivity, the pork industry and public health officials have to find new ways to work together. Jointly, they need to answer numerous questions before they can design effective interventions to reduce the risk for novel virus generation and cross-species transmission. However, the highly integrated U.S. pork industry is not as willing to permit researchers access to their industry domains as compared with the live animal market owners in the subject study. This reticence to conduct One Health studies of their industry environments may one day harm the U.S. pork industry as similar resistance has recently harmed the U.S. poultry industry. In devastating discoveries that poultry biosecurity was not sufficient, the U.S. poultry industry has recently experienced the worst outbreak of highly pathogenic avian influenza virus infections in recent years. During the period of December 2014 to July, highly pathogenic avian H5N2 influenza strains have struck birds in 21 states leading to the destruction of 48 million birds, causing billions of dollars of industry losses.

    While it is likely relatively easy to design interventions for the small live animal markets in the U.S. — and already biosecurity interventions are likely reducing cross-species influenza A transmission at state and county fairs — the greater concern should be focused upon the pork industry. How can we bring modern pork production and public health officials to the same table such that both will benefit from each other’s professional expertise in an interdisciplinary One Health way to protect the health of humans and pigs?

    For more information:

    Bowman AS, et al. Emerg Infect Dis. 2012;doi:10.3201/eid1812.121116.

    Forgie SE, et al. Clin Infect Dis. 2011;doi:10.1093/cid/ciq030.

    Jhung MA, et al. Clin Infect Dis. 2013;doi:10.1093/cid/cit649.

    Nelson MI, et al. Emerg Infect Dis 2015;doi:10.3201/eid2108.141891.

    Nelson MI, et al. J Infect Dis. 2015;doi:10.1093/infdis/jiv399.

    Nelson MI, et al. J Virol. 2015;doi:10.1128/JVI.00459-15.

    Nelson MI, et al. J Virol. 2014;doi:10.1128/JVI.01080-14.

    Nelson MI, et al. Nat Commun. 2015;doi:10.1038/ncomms7696.

    Nelson MI, et al. Trends Microbiol 2015;doi:10.1016/j.tim.2014.12.002.

    • Gregory C. Gray, MD, MPH, FIDSA
    • Professor Division of infectious diseases, Global Health Institute and Nicholas School of the Environment Duke University

    Disclosures: Gray reports no relevant financial disclosures.