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To thwart the next pandemic, ‘swientists’ hunt for flu viruses at U.S. hog shows | Science

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A version of this story appeared in Science, Vol 378, Issue 6618.Download PDF

Des Moines, Iowa—At 4:30 a.m. on 16 June, the last morning of the National Swine Registry’s Exposition, a weeklong hog show at the Iowa State Fairgrounds, Andrew Bowman and his team began winding through massive, open-air barns housing some 2000 pigs. Large fans blew across the pens to cool the pigs and ease the pungent ammonia stench of urine and feces. But Bowman, a swine veterinarian at Ohio State University (OSU), Columbus, and his group of nine vet students and research assistants were more interested in pig sounds than their smells.

“You hear the cougher?” asked Bowman, carrying a blue pail filled with supplies. “There’s somebody over in there that has the barking cough.”

When Bowman found the noisy culprit, he reached into his pail, opened a packet holding a fresh eight-ply gauze cloth, leaned over the rail of the pen, and wiped each nostril on the pig’s snout. As he likes to say, “I’m a professional pig nose picker.” He put the snot-filled rag into a test tube and sealed the cap.

Pigs inflected with influenza virus often have a distinctive barking cough.Andrew Bowman

Bowman and his team were hunting for a most unwelcome guest at the Exposition: influenza virus. Not all coughing pigs are infected, but Bowman’s work over the past decade has shown a “flu break” in even a few animals at a show like this can quickly spread the virus far and wide. As the best pigs fan out from the Exposition and other “jackpot shows” to competitions at the 2000 county and state fairs that take place across the United States through the early fall, they can carry flu with them. With about 150 million people visiting those events, the virus has plenty of opportunities to jump to humans, sickening people with flu outside its typical winter season.

Since 2010, the Centers for Disease Control and Prevention (CDC) has recorded nearly 500 human infections with those “variant viruses”—a term the pork industry prefers to the older, better known “swine flu.” (Researchers say this surely undercounts the actual number because standard flu tests cannot detect an infection with a variant virus.) Most infections fizzle out without further person-to-person spread, possibly because humans have substantial immunity to similar flu viruses. But if a pig virus emerged that did spread readily in people, it could spark a pandemic. “It’s about as real as any zoonotic threat,” says Martha Nelson, an evolutionary biologist at the National Institutes of Health (NIH) who has collaborated with Bowman for 7 years.

A researcher leans over the gate of a pig pen to reach a pig's snout with one hand. He's wearing navy blue short-sleeved coveralls and blue nitrile gloves. A second researcher crouches in front of the pen to watch, and a pig in the neighboring pen sniffs at the divider. Many more pens are visible in the background.
Andrew Bowman (top) shows colleague Martha Nelson his pig snout swabbing prowess as they gather samples to test for flu at the Exposition, a show in Des Moines, Iowa.J. Cohen/Science

It has happened before. Nelson, who works at NIH’s National Center for Biotechnology Information and also studies highly lethal avian influenzas, was part of a team that found persuasive evidence that the 2009 flu pandemic, which infected hundreds of millions of people worldwide, began when a new flu virus jumped from commercial pigs on farms in central Mexico. Although many epidemiologists think viruses from birds touched off the 20th century’s three influenza pandemics—including the infamous one that began in 1918 and killed about 50 million people—some argue pigs could have been a key intermediary between birds and humans in each one. “While people want to downplay it, I think the risk is much greater for swine-to-human influenza pandemics than it is for avian,” says Gregory Gray, an epidemiologist at the University of Texas Medical Branch.

Fears about the next flu pandemic usually focus on Asia, where markets sell live poultry and exotic animals such as palm civets, raccoon dogs, and bamboo rats. “If we sit here and talk about the live-animal markets in China or East Asia, you say, ‘Oh we’d never do that in the U.S.,’” Bowman notes. But U.S. hog shows, where handlers—often children—tend, groom, and even sleep with their charges pose a similar risk, he says. “I mean, is it really that different?”

To assess that risk, Bowman and his co-workers have become regulars at shows and fairs across the country. Winning the trust of sometimes-wary organizers and contestants, the researchers have visited about 1000 events and collected samples from some 40,000 pigs, analyzing them for clues to how novel flu viruses spread through the show circuit and shuttle between pigs and people. From their two dozen studies, “We’ve learned a lot about how swine influenza circulates in that particular niche,” says virologist Richard Webby of St. Jude Children’s Research Hospital.

Bowman and Nelson are also devising simple steps that could protect both pigs and people, including testing show entrants and limiting contact between swine and people. “Our goal is to try and figure out how we can make small tweaks in the whole system that will have outsized, downstream effects,” Nelson says.

Pigs have a special place in the ecology of influenza. Two types of influenza virus, A and B, sicken humans, killing up to 650,000 people worldwide in a bad year. Influenza B viruses only circulate in people, but type A can infect many species. Waterfowl harbor the most diversity, with 16 varieties of one surface protein, hemagglutinin, and nine of another, neuraminidase, leading researchers to conclude waterfowl are the main influenza A reservoir. The seasonal influenza A viruses that routinely infect humans today are restricted to variations of the H1N1 and H3N2 subtypes. But other type A viruses regularly spread to poultry, horses, dogs—and pigs.

As the virus circulates, it changes, constantly presenting new challenges to the immune system. One source of change is its highly mutable RNA genome, allowing “drifts” during each round of viral replication. But flu has another maneuver that speeds its own evolution. The viral RNA is broken into eight segments that can be swapped between related subtypes. So if one type A virus finds its way into a human cell already infected with another, their two genomes can mix when they replicate. This reassortment, or “shift,” creates viral progeny with RNA segments from both strains.

Drift forces vaccine developers to roll out a new vaccine each year to combat the spread of seasonal flu. When shifted viruses emerge from an animal reservoir, the changes sometimes greatly enhance transmission and increase immune evasion—and can even spark a pandemic. “Flu is an acrobat,” Nelson says. “You have to think in eight dimensions.”

Researcher Martha Nelson kneels next to a pig pen, resting her crossed arms on one knee. A black and pink pig has pushed its snout through the bars of the gate beside her. Nelson's face is turned toward the pig and she is smiling widely.
Despite studying the evolution of influenza viruses from pigs and other animals for many years, Martha Nelson hadn’t attended a pig show until this year.J. Cohen/Science

Pigs are a major venue for those acrobatics. When infecting pigs, avian viruses can reassort with viruses already in the swine that more readily infect people. The result can be a novel strain, foreign to the human immune system, that is more apt to spread in people than the original bird virus.

Just such a cascade of trouble began in 1979, when an avian H1N1 virus journeyed from wild ducks to pigs in Europe. Decades later, some of its genes were found in the H1N1 that triggered the 2009 pandemic after jumping from Mexican pigs to humans around March 2009.

Just 5 months after what was dubbed pH1N1 surfaced, nasal swabs of show pigs at the Minnesota State Fair underscored the threat of cross-species transmission by showing 12% of the animals had the virus: This time, humans had infected the pigs. When then–Secretary of Agriculture Tom Vilsack reported the infection of pigs at the show, pork prices plummeted. “The industry was very angry at us,” says Gray, who then was with the University of Florida and led the study. “We were just doing science, but it got political real fast.”

The risk that a flu virus with pandemic potential finds its way to humans via pigs infected by birds remains as real as ever. But massive commercial farms raising hogs by the thousands may not be the biggest threat. On large farms in the United States and many other countries, biocontainment measures limit contact between people and pigs, says James Lowe, a swine vet at the University of Illinois, Urbana-Champaign, who studies influenza in commercial pig herds. Instead he worries about shows like the Exposition, where young handlers compete for belt buckles, banners, and ribbons for having raised the best-looking Duroc, Hampshire, Landrace, Berkshire, or crossbred hog. “The show pig population is the one that’s got all this interaction with people.” But it’s a risk, he says, that “everybody kind of ignored.”

In 2009, Bowman was 2 years into his career as a practicing swine vet in Ohio, like his father before him. A professor from OSU, where Bowman went to vet school, contacted him, asking whether he’d consider coming back to do a Ph.D. focusing on testing show pigs at fairs for influenza. Bowman hesitated to return to academia, but the challenge enticed him. “We had no idea what was happening with flu and these pigs,” he says.

Initially, his requests to take nasal swabs at pig shows were met with much suspicion. “The fear was that we would use the information and shut them down,” Bowman says. Other people worried swabbing would somehow harm the pigs and lead judges to “show them the gate”—show lingo for being eliminated from the competition. “We’ve certainly had, ‘My pig was going to win right up until you swabbed its nose,’” Bowman says. Early on, he did the sampling in the middle of the night to avoid confrontations.

Close up of a pig snout, pink with black splotches, between two metal bars.
Pig snouts harbor influenza virus, making their snot ripe for the picking.Lorrie Cecil/ThisWeek

But the scientific value of the work couldn’t be disputed. In 2012, CDC documented 307 cases of humans infected with variant influenza strains, the highest number ever in a single year, with most connected to agricultural fairs. “Suddenly, I’m holding all of these samples from county fair pigs, and we’ve got all these kids breaking with swine lineage influenza at the same fairs we were at,” Bowman says. “It was a case of me being at the right place at the right time.”

Many human cases in 2012 were in Indiana, and the next year, organizers of that state’s fair asked Bowman to swab noses of incoming pigs to get a better understanding of how many were infected at the outset. The organizers also measured pigs’ rectal temperatures, slowing entry to the fairgrounds and infuriating exhibitors, who wrongly blamed Bowman. Complaints reached the Indiana governor and the National Pork Board. Still, Bowman slowly convinced more and more fair organizers and exhibitors that there wasn’t a great distance between their love of showing pigs and his studies, which aim to educate people and reduce disease in animals, handlers, and fairgoers. “They’ve been a blessing,” says Kelly Morgan, a teacher in Columbus who organizes jackpot shows and, with her family, raises about three dozen show pigs.

Bowman is “a solid veterinarian, a solid scientist, and a pig guy, and so he’s been able to bridge that gap,” Lowe says. “What he’s accomplished, building the relationships with that crowd that lets him get access to sites and do these data collections, is nothing short of a miracle.”

Bowman and Nelson first spoke with each other at a 2015 meeting of an influenza research network organized by NIH’s National Institute of Allergy and Infectious Diseases (NIAID). “In the first few minutes, we realized our interests fit like a glove,” Nelson recalls. She had been studying the evolutionary origin of the variant viruses that caused the major human outbreak in fairs in 2012, but she only had samples from commercial swine. “I was salivating when I found someone actually sampling the show pigs themselves,” she says.

Since then, Bowman’s hands-on expertise with sampling pigs has combined with Nelson’s hard-core focus on the evolutionary biology of the viruses they find. As Lowe puts it, “Martha can’t do what Andy does, and Andy can’t do what Martha does.” The resulting studies of transmission between humans and pigs are “a whole other level,” says Elodie Ghedin, who does genomic studies of parasites at NIAID. “These are really important studies to understand the dynamics and to see what is going on from year to year.”

Bowman’s and Nelson’s first study, published in January 2016 in The Journal of Infectious Diseases, used ornate family trees that Nelson created from Bowman’s virus samples to trace a four-season cycle of viral movement between pigs and people (see graphic, below). It starts in the winter, when seasonal flu viruses spread through the human population and occasionally infect pigs. On small farms, human-to-pig infections quickly burn out. But when humans infect commercial herds, which happens despite biocontainment efforts, the viruses move between the animals throughout the spring and reassort. They can then spread to show pigs that live in separate barns on the same property or even, through the wind, to neighboring farms. By summertime, when show pigs congregate at exhibitions, flu season for humans is over. But the pigs readily infect one another, leading to new reassortment viruses and occasional infections of humans with variant influenza viruses.

“If there were no commercial swine, there’d be no flu viruses in show pigs,” Nelson says. Bowman’s vast sequence library also allowed them to see that jumps from commercial to show swine likely occur many times each year. “There was a surprising amount of genetic diversity of flu viruses in show pigs, given that they’re such a small population and only convene in large numbers for a short summer show season,” Nelson says.

When pigs flu

The U.S. tradition of livestock shows allows influenza viruses to move between humans, commercial hogs, and show pigs in an annual cycle. Outside the normal human flu season, people may contract novel viral variants from show pigs. Those infections usually burn out. But each year a pandemic variant could emerge.

Flow chart showing the cycle of flu infections, accompanied by an illustration of a young person walking beside a show pig. Winter. Flu moves from infected humans to commercial swine. Show pigs are born. Spring. Viruses move between commercial pigs, which can mix viral genes from different subtypes. Infections jump to show pigs late in the season. Summer. National and regional “jackpots” draw show pigs from many states; infected swine fan out to state and county fairs, where some people become infected. Fall. Seasonal human infections begin, spreading virus to commercial pigs.

Showtime for viruses

In 2018, testing of pigs at 113 exhibitions in nine states found flu at all national “jackpot” shows that mixed pigs from several states. Relatively few pigs were infected, but they carried influenza virus to regional jackpot shows, as well as state and county fairs around the country. In any fairs it reached, the virus had a chance to spread widely because fairs typically last longer than other shows, and it sometimes jumped from pigs to people, causing at least 10 human cases in 2018.


Comparison of commercial pig versus show pig, followed by data on show pig infections.
Commercial pig. Farmers breed hogs for size and fat content; these are slaughtered at about 6 months. Larger farms have herds with thousands of hogs. Show pig.
Bred to be lean and muscular, show pigs are mainly raised on small farms. They ideally show at about 6 months of age. Flu viruses are transmitted from commerical pigs to show pigs. The following data concern populations of show pigs. National/regional jackpot shows. All six shows tested had infected animals, with 12.9% of 594 pigs sampled being positive. County fairs (with infected pigs). At the 42 fairs that had infections, 42.9% of the 1194 pigs tested carried flu viruses; another 56 fairs had no infections.
(Graphic) A. Mastin/Science; (Data) M. I. Nelson et al., Journal of Virology 90 23 (2014) 10.1128/jvi.01457-16; M. I. Nelson et al., Journal of Virology 94 24 (2020) 10.1128/jvi.01453-20

At the same time, as Nelson and Bowman reported in December 2016 in the Journal of Virology, animals at shows in counties and states distant from one another sometimes had identical viruses. “This was the head-scratching moment when we realized there must be something else helping to spread these viruses so quickly over long distances between fairs,” Nelson says.

Jackpot shows like the Exposition are key to dispersing those viruses, Nelson and Bowman realized. Hogs at a county fair must come from that county, and the same geographic restriction applies at state fairs. But jackpot shows draw contestants from far and wide. To understand how they affect viral traffic, the researchers went to an early-season show in Iowa that hosted exhibitors from 17 states. (They won’t name the show to avoid shaming it.) Four distinct influenza viruses spread at that show, one of which accounted for 80% of pig infections. When pigs from the show dispersed to their home states, they carried the virus with them. Through later sampling, researchers found influenza in hogs at 38 county and state fairs, and 94% had the variant dominant at the jackpot show. That variant was also responsible for 90% of that year’s show-linked flu cases in people.

The fairs, not the jackpot shows, are where the pig variants are most likely to jump to humans. Although the Bowman team’s sampling over the years has detected influenza in only about 30% of the fairs, compared with 80% of the jackpot shows, fairs often last longer. So fairs that start with infected pigs wind up with as many as 80% of hogs infected by the end, a far higher prevalence than at jackpot shows. And fairs have far more humans interacting with pigs, increasing the risk of zoonotic jumps. “You see the human cases show up usually in association with the end of the fair because if you’ve got 250 pigs shedding the virus, it’s going be just a cloud of flu virus in there,” Bowman says.

To reduce the risk to people, say Bowman, Nelson, and others, regular testing of exhibition hogs, which make up a mere 1.5% of the U.S. swine herd, should be standard practice. But no such “active surveillance” program exists. Instead, the United States has a passive system that relies on farms to sample sick pigs and then voluntarily report what they find to the Department of Agriculture.

Bowman has already persuaded several pig show organizers to stop children from sleeping near their animals. At one show, kids hung hammocks over their prized pigs. “I’m like, guys,” Bowman says. The hammocks are gone now, as are pen cots—at least at shows his crew attends. “This is moving the needle,” Nelson says.

In the vendor hall at this year’s Exposition, Bowman’s team set up a station to educate kids directly about reducing the spread of influenza. The project, started 7 years ago by his collaborator Jacqueline Nolting—who has a Ph.D. in agricultural education—encourages the kids to join the OSU “swientist” program, offering free popsicles and stickers featuring a pig in a lab coat. A “pathogen shootout” has the kids kill influenza with squirt guns, knocking plastic viruses off pedestals. And they can pick up biosecurity buckets that hold soap, a scrub brush, disinfectant, gloves, and other essentials. “I’m not going to convince the parents to do things differently, but I think I can get the kid,” Bowman says. “So it’s really the long game. In a decade, I think I can change some behaviors.”

A child getting their blood drawn. They sit in a camp chair, near a card table holding various supplies including medical gloves and vials. An adult wearing blue nitrile gloves holds a tourniquet on the child's upper arm in one hand and takes a blood sample with the other hand.
Ohio State University’s “swientist” program recruits children into their studies, educating them about measures to reduce flu virus transmission.J. Cohen/Science

Bowman’s team also enrolls people between 5 and 21 years old in a long-term study to track any flu infections they pick up, which requires an immediate blood sample. (Bandages that look like bacon strips are on offer.) “I’m interested in seeing what they find in my blood,” says new recruit Sam Fox, 18, who lives in Indiana and has shown hogs most of his childhood. “I’d bet there are only a handful of weeks I haven’t been around hogs in the last 8 years.”

Morgan says the education program has helped calm initial concerns about their pig sampling. “Andy and Jacqueline are not there to do anything but better the health of the swine and kids,” says Morgan, whose son showed pigs and took part in the swientist program.

More ambitious ideas from Bowman and Nelson include requiring that all animals receive a flu vaccine, which, if matched to variants in circulation, could reduce transmissions. The researchers have even proposed that hogs attending national or regional jackpot shows not show again for 2 weeks: Hitting the pause button would allow enough time for any virus in infected pigs to burn out before they have a chance to spread it. But Bowman says the idea has had zero traction, in part because people who have winning pigs at jackpots understandably want to exhibit over the next few weeks at state and county fairs. “It’s hard,” he says. “We are making changes and it is pandemic prevention. But how do you even quantify the impact of those changes?”

Bowman says for now, the most urgent need is to gather enough data to properly assess the risks of this cherished U.S. tradition. “Is it going to be this show that kicks off something?” he asks about the Exposition held in June. “I don’t know, because we’ve had our thumb on the pulse of this one for quite a while. But what else is out there?”

This story was supported by a grant from the NIHCM Foundation.


issue cover image
A version of this story appeared in Science, Vol 378, Issue 6618.Download PDF

Des Moines, Iowa—At 4:30 a.m. on 16 June, the last morning of the National Swine Registry’s Exposition, a weeklong hog show at the Iowa State Fairgrounds, Andrew Bowman and his team began winding through massive, open-air barns housing some 2000 pigs. Large fans blew across the pens to cool the pigs and ease the pungent ammonia stench of urine and feces. But Bowman, a swine veterinarian at Ohio State University (OSU), Columbus, and his group of nine vet students and research assistants were more interested in pig sounds than their smells.

“You hear the cougher?” asked Bowman, carrying a blue pail filled with supplies. “There’s somebody over in there that has the barking cough.”

When Bowman found the noisy culprit, he reached into his pail, opened a packet holding a fresh eight-ply gauze cloth, leaned over the rail of the pen, and wiped each nostril on the pig’s snout. As he likes to say, “I’m a professional pig nose picker.” He put the snot-filled rag into a test tube and sealed the cap.

Pigs inflected with influenza virus often have a distinctive barking cough.Andrew Bowman

Bowman and his team were hunting for a most unwelcome guest at the Exposition: influenza virus. Not all coughing pigs are infected, but Bowman’s work over the past decade has shown a “flu break” in even a few animals at a show like this can quickly spread the virus far and wide. As the best pigs fan out from the Exposition and other “jackpot shows” to competitions at the 2000 county and state fairs that take place across the United States through the early fall, they can carry flu with them. With about 150 million people visiting those events, the virus has plenty of opportunities to jump to humans, sickening people with flu outside its typical winter season.

Since 2010, the Centers for Disease Control and Prevention (CDC) has recorded nearly 500 human infections with those “variant viruses”—a term the pork industry prefers to the older, better known “swine flu.” (Researchers say this surely undercounts the actual number because standard flu tests cannot detect an infection with a variant virus.) Most infections fizzle out without further person-to-person spread, possibly because humans have substantial immunity to similar flu viruses. But if a pig virus emerged that did spread readily in people, it could spark a pandemic. “It’s about as real as any zoonotic threat,” says Martha Nelson, an evolutionary biologist at the National Institutes of Health (NIH) who has collaborated with Bowman for 7 years.

A researcher leans over the gate of a pig pen to reach a pig's snout with one hand. He's wearing navy blue short-sleeved coveralls and blue nitrile gloves. A second researcher crouches in front of the pen to watch, and a pig in the neighboring pen sniffs at the divider. Many more pens are visible in the background.
Andrew Bowman (top) shows colleague Martha Nelson his pig snout swabbing prowess as they gather samples to test for flu at the Exposition, a show in Des Moines, Iowa.J. Cohen/Science

It has happened before. Nelson, who works at NIH’s National Center for Biotechnology Information and also studies highly lethal avian influenzas, was part of a team that found persuasive evidence that the 2009 flu pandemic, which infected hundreds of millions of people worldwide, began when a new flu virus jumped from commercial pigs on farms in central Mexico. Although many epidemiologists think viruses from birds touched off the 20th century’s three influenza pandemics—including the infamous one that began in 1918 and killed about 50 million people—some argue pigs could have been a key intermediary between birds and humans in each one. “While people want to downplay it, I think the risk is much greater for swine-to-human influenza pandemics than it is for avian,” says Gregory Gray, an epidemiologist at the University of Texas Medical Branch.

Fears about the next flu pandemic usually focus on Asia, where markets sell live poultry and exotic animals such as palm civets, raccoon dogs, and bamboo rats. “If we sit here and talk about the live-animal markets in China or East Asia, you say, ‘Oh we’d never do that in the U.S.,’” Bowman notes. But U.S. hog shows, where handlers—often children—tend, groom, and even sleep with their charges pose a similar risk, he says. “I mean, is it really that different?”

To assess that risk, Bowman and his co-workers have become regulars at shows and fairs across the country. Winning the trust of sometimes-wary organizers and contestants, the researchers have visited about 1000 events and collected samples from some 40,000 pigs, analyzing them for clues to how novel flu viruses spread through the show circuit and shuttle between pigs and people. From their two dozen studies, “We’ve learned a lot about how swine influenza circulates in that particular niche,” says virologist Richard Webby of St. Jude Children’s Research Hospital.

Bowman and Nelson are also devising simple steps that could protect both pigs and people, including testing show entrants and limiting contact between swine and people. “Our goal is to try and figure out how we can make small tweaks in the whole system that will have outsized, downstream effects,” Nelson says.

Pigs have a special place in the ecology of influenza. Two types of influenza virus, A and B, sicken humans, killing up to 650,000 people worldwide in a bad year. Influenza B viruses only circulate in people, but type A can infect many species. Waterfowl harbor the most diversity, with 16 varieties of one surface protein, hemagglutinin, and nine of another, neuraminidase, leading researchers to conclude waterfowl are the main influenza A reservoir. The seasonal influenza A viruses that routinely infect humans today are restricted to variations of the H1N1 and H3N2 subtypes. But other type A viruses regularly spread to poultry, horses, dogs—and pigs.

As the virus circulates, it changes, constantly presenting new challenges to the immune system. One source of change is its highly mutable RNA genome, allowing “drifts” during each round of viral replication. But flu has another maneuver that speeds its own evolution. The viral RNA is broken into eight segments that can be swapped between related subtypes. So if one type A virus finds its way into a human cell already infected with another, their two genomes can mix when they replicate. This reassortment, or “shift,” creates viral progeny with RNA segments from both strains.

Drift forces vaccine developers to roll out a new vaccine each year to combat the spread of seasonal flu. When shifted viruses emerge from an animal reservoir, the changes sometimes greatly enhance transmission and increase immune evasion—and can even spark a pandemic. “Flu is an acrobat,” Nelson says. “You have to think in eight dimensions.”

Researcher Martha Nelson kneels next to a pig pen, resting her crossed arms on one knee. A black and pink pig has pushed its snout through the bars of the gate beside her. Nelson's face is turned toward the pig and she is smiling widely.
Despite studying the evolution of influenza viruses from pigs and other animals for many years, Martha Nelson hadn’t attended a pig show until this year.J. Cohen/Science

Pigs are a major venue for those acrobatics. When infecting pigs, avian viruses can reassort with viruses already in the swine that more readily infect people. The result can be a novel strain, foreign to the human immune system, that is more apt to spread in people than the original bird virus.

Just such a cascade of trouble began in 1979, when an avian H1N1 virus journeyed from wild ducks to pigs in Europe. Decades later, some of its genes were found in the H1N1 that triggered the 2009 pandemic after jumping from Mexican pigs to humans around March 2009.

Just 5 months after what was dubbed pH1N1 surfaced, nasal swabs of show pigs at the Minnesota State Fair underscored the threat of cross-species transmission by showing 12% of the animals had the virus: This time, humans had infected the pigs. When then–Secretary of Agriculture Tom Vilsack reported the infection of pigs at the show, pork prices plummeted. “The industry was very angry at us,” says Gray, who then was with the University of Florida and led the study. “We were just doing science, but it got political real fast.”

The risk that a flu virus with pandemic potential finds its way to humans via pigs infected by birds remains as real as ever. But massive commercial farms raising hogs by the thousands may not be the biggest threat. On large farms in the United States and many other countries, biocontainment measures limit contact between people and pigs, says James Lowe, a swine vet at the University of Illinois, Urbana-Champaign, who studies influenza in commercial pig herds. Instead he worries about shows like the Exposition, where young handlers compete for belt buckles, banners, and ribbons for having raised the best-looking Duroc, Hampshire, Landrace, Berkshire, or crossbred hog. “The show pig population is the one that’s got all this interaction with people.” But it’s a risk, he says, that “everybody kind of ignored.”

In 2009, Bowman was 2 years into his career as a practicing swine vet in Ohio, like his father before him. A professor from OSU, where Bowman went to vet school, contacted him, asking whether he’d consider coming back to do a Ph.D. focusing on testing show pigs at fairs for influenza. Bowman hesitated to return to academia, but the challenge enticed him. “We had no idea what was happening with flu and these pigs,” he says.

Initially, his requests to take nasal swabs at pig shows were met with much suspicion. “The fear was that we would use the information and shut them down,” Bowman says. Other people worried swabbing would somehow harm the pigs and lead judges to “show them the gate”—show lingo for being eliminated from the competition. “We’ve certainly had, ‘My pig was going to win right up until you swabbed its nose,’” Bowman says. Early on, he did the sampling in the middle of the night to avoid confrontations.

Close up of a pig snout, pink with black splotches, between two metal bars.
Pig snouts harbor influenza virus, making their snot ripe for the picking.Lorrie Cecil/ThisWeek

But the scientific value of the work couldn’t be disputed. In 2012, CDC documented 307 cases of humans infected with variant influenza strains, the highest number ever in a single year, with most connected to agricultural fairs. “Suddenly, I’m holding all of these samples from county fair pigs, and we’ve got all these kids breaking with swine lineage influenza at the same fairs we were at,” Bowman says. “It was a case of me being at the right place at the right time.”

Many human cases in 2012 were in Indiana, and the next year, organizers of that state’s fair asked Bowman to swab noses of incoming pigs to get a better understanding of how many were infected at the outset. The organizers also measured pigs’ rectal temperatures, slowing entry to the fairgrounds and infuriating exhibitors, who wrongly blamed Bowman. Complaints reached the Indiana governor and the National Pork Board. Still, Bowman slowly convinced more and more fair organizers and exhibitors that there wasn’t a great distance between their love of showing pigs and his studies, which aim to educate people and reduce disease in animals, handlers, and fairgoers. “They’ve been a blessing,” says Kelly Morgan, a teacher in Columbus who organizes jackpot shows and, with her family, raises about three dozen show pigs.

Bowman is “a solid veterinarian, a solid scientist, and a pig guy, and so he’s been able to bridge that gap,” Lowe says. “What he’s accomplished, building the relationships with that crowd that lets him get access to sites and do these data collections, is nothing short of a miracle.”

Bowman and Nelson first spoke with each other at a 2015 meeting of an influenza research network organized by NIH’s National Institute of Allergy and Infectious Diseases (NIAID). “In the first few minutes, we realized our interests fit like a glove,” Nelson recalls. She had been studying the evolutionary origin of the variant viruses that caused the major human outbreak in fairs in 2012, but she only had samples from commercial swine. “I was salivating when I found someone actually sampling the show pigs themselves,” she says.

Since then, Bowman’s hands-on expertise with sampling pigs has combined with Nelson’s hard-core focus on the evolutionary biology of the viruses they find. As Lowe puts it, “Martha can’t do what Andy does, and Andy can’t do what Martha does.” The resulting studies of transmission between humans and pigs are “a whole other level,” says Elodie Ghedin, who does genomic studies of parasites at NIAID. “These are really important studies to understand the dynamics and to see what is going on from year to year.”

Bowman’s and Nelson’s first study, published in January 2016 in The Journal of Infectious Diseases, used ornate family trees that Nelson created from Bowman’s virus samples to trace a four-season cycle of viral movement between pigs and people (see graphic, below). It starts in the winter, when seasonal flu viruses spread through the human population and occasionally infect pigs. On small farms, human-to-pig infections quickly burn out. But when humans infect commercial herds, which happens despite biocontainment efforts, the viruses move between the animals throughout the spring and reassort. They can then spread to show pigs that live in separate barns on the same property or even, through the wind, to neighboring farms. By summertime, when show pigs congregate at exhibitions, flu season for humans is over. But the pigs readily infect one another, leading to new reassortment viruses and occasional infections of humans with variant influenza viruses.

“If there were no commercial swine, there’d be no flu viruses in show pigs,” Nelson says. Bowman’s vast sequence library also allowed them to see that jumps from commercial to show swine likely occur many times each year. “There was a surprising amount of genetic diversity of flu viruses in show pigs, given that they’re such a small population and only convene in large numbers for a short summer show season,” Nelson says.

When pigs flu

The U.S. tradition of livestock shows allows influenza viruses to move between humans, commercial hogs, and show pigs in an annual cycle. Outside the normal human flu season, people may contract novel viral variants from show pigs. Those infections usually burn out. But each year a pandemic variant could emerge.

Flow chart showing the cycle of flu infections, accompanied by an illustration of a young person walking beside a show pig. Winter. Flu moves from infected humans to commercial swine. Show pigs are born. Spring. Viruses move between commercial pigs, which can mix viral genes from different subtypes. Infections jump to show pigs late in the season. Summer. National and regional “jackpots” draw show pigs from many states; infected swine fan out to state and county fairs, where some people become infected. Fall. Seasonal human infections begin, spreading virus to commercial pigs.

Showtime for viruses

In 2018, testing of pigs at 113 exhibitions in nine states found flu at all national “jackpot” shows that mixed pigs from several states. Relatively few pigs were infected, but they carried influenza virus to regional jackpot shows, as well as state and county fairs around the country. In any fairs it reached, the virus had a chance to spread widely because fairs typically last longer than other shows, and it sometimes jumped from pigs to people, causing at least 10 human cases in 2018.


Comparison of commercial pig versus show pig, followed by data on show pig infections.
Commercial pig. Farmers breed hogs for size and fat content; these are slaughtered at about 6 months. Larger farms have herds with thousands of hogs. Show pig.
Bred to be lean and muscular, show pigs are mainly raised on small farms. They ideally show at about 6 months of age. Flu viruses are transmitted from commerical pigs to show pigs. The following data concern populations of show pigs. National/regional jackpot shows. All six shows tested had infected animals, with 12.9% of 594 pigs sampled being positive. County fairs (with infected pigs). At the 42 fairs that had infections, 42.9% of the 1194 pigs tested carried flu viruses; another 56 fairs had no infections.
(Graphic) A. Mastin/Science; (Data) M. I. Nelson et al., Journal of Virology 90 23 (2014) 10.1128/jvi.01457-16; M. I. Nelson et al., Journal of Virology 94 24 (2020) 10.1128/jvi.01453-20

At the same time, as Nelson and Bowman reported in December 2016 in the Journal of Virology, animals at shows in counties and states distant from one another sometimes had identical viruses. “This was the head-scratching moment when we realized there must be something else helping to spread these viruses so quickly over long distances between fairs,” Nelson says.

Jackpot shows like the Exposition are key to dispersing those viruses, Nelson and Bowman realized. Hogs at a county fair must come from that county, and the same geographic restriction applies at state fairs. But jackpot shows draw contestants from far and wide. To understand how they affect viral traffic, the researchers went to an early-season show in Iowa that hosted exhibitors from 17 states. (They won’t name the show to avoid shaming it.) Four distinct influenza viruses spread at that show, one of which accounted for 80% of pig infections. When pigs from the show dispersed to their home states, they carried the virus with them. Through later sampling, researchers found influenza in hogs at 38 county and state fairs, and 94% had the variant dominant at the jackpot show. That variant was also responsible for 90% of that year’s show-linked flu cases in people.

The fairs, not the jackpot shows, are where the pig variants are most likely to jump to humans. Although the Bowman team’s sampling over the years has detected influenza in only about 30% of the fairs, compared with 80% of the jackpot shows, fairs often last longer. So fairs that start with infected pigs wind up with as many as 80% of hogs infected by the end, a far higher prevalence than at jackpot shows. And fairs have far more humans interacting with pigs, increasing the risk of zoonotic jumps. “You see the human cases show up usually in association with the end of the fair because if you’ve got 250 pigs shedding the virus, it’s going be just a cloud of flu virus in there,” Bowman says.

To reduce the risk to people, say Bowman, Nelson, and others, regular testing of exhibition hogs, which make up a mere 1.5% of the U.S. swine herd, should be standard practice. But no such “active surveillance” program exists. Instead, the United States has a passive system that relies on farms to sample sick pigs and then voluntarily report what they find to the Department of Agriculture.

Bowman has already persuaded several pig show organizers to stop children from sleeping near their animals. At one show, kids hung hammocks over their prized pigs. “I’m like, guys,” Bowman says. The hammocks are gone now, as are pen cots—at least at shows his crew attends. “This is moving the needle,” Nelson says.

In the vendor hall at this year’s Exposition, Bowman’s team set up a station to educate kids directly about reducing the spread of influenza. The project, started 7 years ago by his collaborator Jacqueline Nolting—who has a Ph.D. in agricultural education—encourages the kids to join the OSU “swientist” program, offering free popsicles and stickers featuring a pig in a lab coat. A “pathogen shootout” has the kids kill influenza with squirt guns, knocking plastic viruses off pedestals. And they can pick up biosecurity buckets that hold soap, a scrub brush, disinfectant, gloves, and other essentials. “I’m not going to convince the parents to do things differently, but I think I can get the kid,” Bowman says. “So it’s really the long game. In a decade, I think I can change some behaviors.”

A child getting their blood drawn. They sit in a camp chair, near a card table holding various supplies including medical gloves and vials. An adult wearing blue nitrile gloves holds a tourniquet on the child's upper arm in one hand and takes a blood sample with the other hand.
Ohio State University’s “swientist” program recruits children into their studies, educating them about measures to reduce flu virus transmission.J. Cohen/Science

Bowman’s team also enrolls people between 5 and 21 years old in a long-term study to track any flu infections they pick up, which requires an immediate blood sample. (Bandages that look like bacon strips are on offer.) “I’m interested in seeing what they find in my blood,” says new recruit Sam Fox, 18, who lives in Indiana and has shown hogs most of his childhood. “I’d bet there are only a handful of weeks I haven’t been around hogs in the last 8 years.”

Morgan says the education program has helped calm initial concerns about their pig sampling. “Andy and Jacqueline are not there to do anything but better the health of the swine and kids,” says Morgan, whose son showed pigs and took part in the swientist program.

More ambitious ideas from Bowman and Nelson include requiring that all animals receive a flu vaccine, which, if matched to variants in circulation, could reduce transmissions. The researchers have even proposed that hogs attending national or regional jackpot shows not show again for 2 weeks: Hitting the pause button would allow enough time for any virus in infected pigs to burn out before they have a chance to spread it. But Bowman says the idea has had zero traction, in part because people who have winning pigs at jackpots understandably want to exhibit over the next few weeks at state and county fairs. “It’s hard,” he says. “We are making changes and it is pandemic prevention. But how do you even quantify the impact of those changes?”

Bowman says for now, the most urgent need is to gather enough data to properly assess the risks of this cherished U.S. tradition. “Is it going to be this show that kicks off something?” he asks about the Exposition held in June. “I don’t know, because we’ve had our thumb on the pulse of this one for quite a while. But what else is out there?”

This story was supported by a grant from the NIHCM Foundation.

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