The Worst Thing That Could Happen Nearly Did and Probably Will Soon

It’s early afternoon in mid-September and pouring rain when Andrew Bowman elbows his rented Toyota Avalon into a line of cars funneling into Ohio’s Wayne County Fair. A woman on horseback wearing a plastic poncho directs us to park next to a Ford F-350 pickup with a “My Cat Ate Your Deere” decal on the rear window, and we ride a tractor to the fair’s entrance. Next to me is a high school kid who tells us he’s skipping school to be here. “This is way more important than class,” he says. He could pocket 10 grand if the pig he has raised wins the swine competition.

“Everybody who’s anybody comes to the fair. It’s the center of life in rural Ohio,” Bowman says. An assistant veterinary professor at Ohio State University, he runs a lab that gets $600,0000 annually from the National Institutes of Health and the Centers of Excellence for Influenza Research and Surveillance to track flu in the Midwest. It’s a key tentacle in the world’s elaborate flu surveillance network. He’s here to help figure out how a strain of the virus that passed from pigs to humans in August at the Clark County Fair, 125 miles southwest of here in Springfield, almost became the next global pandemic.

The pig barns are past a pork loin vendor and the poultry exhibit, which was shut down last year for the first time in the fair’s 167-year history to save Ohio’s egg and broiler industries from an avian flu outbreak. Inside a long pig barn, 340 hogs and at least half that many people have pushed in to escape the rain now drumming on the corrugated roof. Bowman sets his sampling kit atop a sow’s pen while we don coveralls, plastic boots, and nitrile gloves. A concerned-looking woman feeding a baby strapped to her chest watches us from the corner of her eye. Next to her, a college-age kid with a weed leaf on his hat works his way through a bowl of ice cream. Next to him is a sign that reads, “Please don’t eat or drink near the animals!”

“And you wonder how people get sick,” Bowman says dryly. A former marching band trumpet player, he’s a big man who wears an OSU polo and jeans and likes his animal puns—“Let’s make like a mallard and get the flock out of here.” Bowman pries open the gate of a pen holding a Hereford named Bubba and sticks a gauze swab the size of a tea bag into its wet snout—“right up where the mucus is,” he explains. The animal responds by trying to eat his hand. The barn is hot and sticky with rain and the invisible droplets of mucus that pigs and humans exhale. Around us, visitors and Future Farmers of America are touching the pigs, touching their faces, touching each other. It’s a flu petri dish in here, but anybody who has visited a fair knows that this is the last thing on anybody’s mind, except Bowman’s. As he works, a small crowd gathers around him and starts asking questions. “Is that pig sick?” “Will I get flu if I eat an infected pig?” (No.) “Have you tested that pig? Because you should—it’s been coughing all summer.”

Highly virulent, easily transmissible, and constantly evolving, flu is among the world’s most infectious diseases. The four flu pandemics of the past century—they occurred in 1918, 1957, 1968, and 2009—collectively shrank the world’s population by somewhere between 60 million and 110 million. Flu occupies the sweet spot of deadly viruses, which makes it—and not scarier-seeming diseases like Ebola—the most likely candidate to be the cause of a global pandemic: It’s transmissible by casual contact and can be strong enough to kill the host but not so strong that it kills before the host passes the virus to someone new, in whom the cycle repeats. “Everybody is worried about the next influenza pandemic emerging from Asia’s live bird markets,” Bowman says. But the Clark County Fair, with its virus-carrying animals and their bodily fluids coming into contact with humans and their ice-cream-loving ways, Bowman says, “is no different.” Each year, 150 million people visit America’s county and state fairs.

A boy plays with the pig he raised to show at the Wayne County Fair in Ohio in August. (Photo: David Bernstein)

A joke among influenza researchers goes like this: “What came first, the chicken or the flu?” Sometime many millions of years ago, flu developed among the world’s 9,721 known bird species, flu’s natural reservoir. Now, on any given day, nearly infinite combinations of its viral descendants take wing. Avian flu can infect humans directly, but flu’s pathway to people often goes through pigs first. To be infected a pig has to huff enough aerosolized avian flu or the virus has to mutate. Like all viruses, flu attaches to cells and effectively hijacks the machinery. Once it has commandeered a cell, it makes a copy of itself. The process is repeated hundreds of thousands of times until either the host’s immune system kills the virus or the virus kills the host.

Most viruses take over cells by printing exact copies of their genome. Every time flu moves between cells, it prints an error. Most of the time the genetic tweaks actually make it less fit or have no significant effect on its viral performance. But typing monkeys eventually produce Shakespeare, and in a single poultry farm a virus can infect 50,000 birds. Each new cell infected can make a virus transmissible to a different species or deadlier or both. “It’s astronomical—a universe of possibilities open up every time the flu jumps between hosts,” says Richard Slemons, professor emeritus of veterinary medicine at Ohio State.

The most unpredictable mutations occur through genetic reassortment. Birds, pigs, people, sea lions, dogs, ferrets, horses, and bats are a few of the animals that carry flu. When two different flu viruses infect a host at the same time the life forms swap RNA, producing an offspring with a novel genetic structure. These changes happen often in swine, which are capable of hosting both avian and human viruses and spend their lives among birds and people. Every year, pigs almost certainly pass the flu to fairgoers and farmers across the country. It’s just not a strain that makes people sick enough to generate a report. But viruses mutate in people, too. It’s by crossing these species barriers that a virus picks up the mash-ups of avian, swine, and human genes that experts say will one day kill hundreds of millions of people worldwide.

I kept thinking, H1N1, H1N1, H1N1—Clark County is about to be the center of a pandemic.

Charles Patterson, health commissioner, Clark County, Ohio

The places where people, pigs, and birds meet have always been the world’s flu mills, but today people raise four times as many chickens as we did just 40 years ago, and each year the world’s 7.7 billion people slaughter 1 billion pigs. Those figures help explain why the number of recorded flu outbreaks jumped by half between 2014 and 2015 (increased surveillance played a role too). Meanwhile, climate change is oiling the machinery: Steeply climbing temperatures in the Arctic, where many wild bird species congregate each summer, are forcing the birds to migrate earlier and fly farther, bringing different species and their pathogens in contact with one another and closing the gap between novel viruses in China’s poultry farms and America’s. A recent USDA study found that 85 percent of viruses found in birds on Alaska’s St. Lawrence Island contained genes from both North American and Asian flus.

Last year, we saw what can happen when wild birds carry a virulent flu strain over the top of the world. Though nobody knows for sure how the flu arrived in the U.S., the going theory is that sometime before the Arctic froze for winter, a virus born in Asia’s poultry mills was carried to North America by wild birds that then passed it to chickens in British Columbia through their waste (in birds, flu is a gastrointestinal disease). Over the next six months, infections on U.S. poultry farms in Washington, Oregon, California, Indiana, and Wisconsin lit up the flu surveillance network. Whether the bug was spread from farm to farm by workers or migrating birds still isn’t entirely understood, but the strategy for containing poultry viruses is the same: tactical slaughter. At the cost of almost $1 billion, USDA officials created viral firebreaks by killing 48 million turkeys and chickens across 21 states. At one Iowa farm, they killed so many birds that tractors piled the carcasses into a 12-foot high ridge stretching six miles.

That virus hasn’t yet infected people. It might never. But if it does, it’ll be in a place where people, poultry, and pigs meet. “It’s not the viruses that are already adapted to people that we need to worry about,” says Slemons. “It’s the viruses that haven’t made the leap yet. Those are the ones we have no immunity against.”

Using a wad of gauze, a researcher collects mucus from a pig at the Wayne County Fair in Ohio in August to see if the animal carries flu. (Photo: David Bernstein)

The influenza outbreak that freaked out Bowman and many others started at 2:33 p.m. on Aug. 2 in Clark County, with the buzz and whirr of the health department’s fax machine. Two hours earlier, Dayton Children’s Hospital had sent over a report of a 13-year-old boy with flu-like symptoms—dizziness, fatigue, a 103-degree fever. Now, Nationwide Children’s Hospital in Columbus was reporting a two-year-old girl with a temperature of 100.4 degrees, shortness of breath, and the sort of dry hacking cough that makes parents wince. The Dayton case wasn’t a fluke.

Flu symptoms months removed from regular flu season are cause for concern. More disturbing was that the cases’ only shared history was a visit to the animal exhibits at the Clark County Fair, which was happening that week. Then the fax machine tripped again. Clark County’s health commissioner, Charles Patterson, realized he had a problem. “Three cases already?” he recalls thinking. “If you find a rat or two, you’re going to find more the moment you start looking.”

Seasonal flu goes viral when cold weather drives us inside and, depending on the strain, can kill nearly 50,000 Americans in a season, far more than car accidents or guns do. That steady death rate is why flu is the only one of 500 infectious diseases known to occur in humans that the Centers for Disease Control and Prevention recommends we vaccinate against each year. But vaccines offer little protection against novel flu. All the flu pandemics going back to 1918 had the same origin story as the Ohio cases: an animal virus passed to people.

Patterson immediately had three questions: What is this thing? Is it spreading person-to-person? How are we going to contain it? Each year 15,000 people visit the Clark County Fair, which is half a mile from Interstate 70 and 45 minutes from an international airport. The virus’ escape routes were nearly limitless. All it would take was one infected child passing the flu to a parent, a friend, or a pork loin vendor with travel plans. So many planes now circle the globe that a map of 48 hours’ worth of flight paths looks like fireworks have blotted out the earth. Each day, 90,000 freighters are crossing the oceans. One bad bug can hopscotch across continents in a matter of hours. “I’m not going to lie to you—I was really scared,” Patterson says.

Ohio State University veterinary assistant professor Andrew Bowman retrieves samples of flu virus out of liquid nitrogen storage containers. (Photo: Ken Blaze)

He sent faxes, which remain the health service’s fastest mode of communication because the Health Insurance Portability and Accountability Act doesn’t require their encryption, to all nearby hospital emergency departments, urgent care facilities, county and state health departments, and private medical practices alerting them to watch for flu-like symptoms. New cases poured in almost immediately. One was a friend of the first infected boy, another a whole family unwilling to cooperate with health officials. (“That makes our job very difficult,” Patterson says.) Then he got a call from the health department in neighboring Madison County about its fair. The week before, during another sweltering day in the hottest summer in Ohio history, a prize hog had died suddenly in its stall.

At that moment, thousands of people were milling about the Clark County fair, hundreds probably in the pig barns. Patterson called the fair manager to ask where the 432 pigs at this year’s swine exhibit had come from. “Hate to tell you this,” Patterson says the fair manager told him, “but we’ve got hogs here that were right next to that pig that died in Madison.” He added that when the fair ended the next day, many pigs were bound for the Ohio State Fair, which attracts 1 million visitors each year. Patterson hung up and alerted the Ohio Department of Health and the CDC: They had something on their hands.

Two days later, genetic samples confirming the world’s first human infections with the novel flu strain, H3N2v, came back from the state health department. Then it got worse. The sister of one of the confirmed H3N2v cases fell ill. She had not been in contact with pigs. That indicated the virus that had passed pig-to-person—the 13-year-old over in Dayton—had mutated so that it could pass person-to-person. The nightmare scenario had landed in rural Ohio: a new virus that humans lacked immunity against, of which scientists had no samples for vaccine development. It echoed the swine-origin flu that killed more than 200,000 people worldwide, and infected 1.5 billion more, seven years ago. “I kept thinking H1N1, H1N1, H1N1—this is 2009 all over again,” Patterson says. “Clark County is about to be the center of a pandemic.”

Visitors to the poultry barn at the Wayne County Fair in Ohio in August seemed oblivious of signs attempting to discourage the transmission of swine flu. (Photo: David Bernstein)

The textbook response to a virus that delivers all that H3N2v threatened came with that 2009 pandemic. It started on April 15, when a 10-year-old patient in California reported a fever and tested positive for influenza. Two days later and 130 miles to the north, an eight-year-old was diagnosed with the same infection. The bug’s genetic signature pointed to a novel swine-origin flu that had become a mutt of human and avian DNA. As the disease detectives in California quickly found out, neither patient had crossed paths with any swine. Both, though, had been to or near Perote, a mountain town in Veracruz, Mexico, that’s home to a breeding operation for the pork packer and hog producer Smithfield Foods. Some pigs had probably passed their flu to a Smithfield employee, in whom it may have mutated again, making it possible to infect humans. Then somewhere on their way to California, the kids had met that employee, or a person he or she had come in contact with, or someone whom that person had come in contact with.

If anyone doubts how quickly an outbreak can spread, two weeks after the California cases were reported, between 113,000 and 375,000 people in Mexico were sick. Cases cropped up in California’s San Diego and Imperial counties, in Texas, and in Kansas. Then 45 kids and staff members at one New York City high school got sick. Already, the CDC was racing to develop a vaccine against a virus that weeks earlier nobody knew existed, a process that takes at least six months.

It’s not the viruses that are already adapted to people that we need to worry about. It’s the viruses that haven’t made the leap yet. Those are the ones we have no immunity against.

Richard Slemons, emeritus professor of veterinary medicine, Ohio State University

At the end of April the CDC began releasing to state and county health departments a quarter of the medical supplies cached at the Strategic National Stockpile, which comprises high-security warehouses of emergency supplies located around the country, and activated its Emergency Operations Center in Atlanta, where 250 of what would grow to become 3,000 epidemiologists, doctors, and support staff were tasked with stopping the emerging virus in its tracks. A week later, the U.S. discussed closing the border with Mexico. By then, the flu was established in 45 countries and on its way to 35 more.

“It was like trying to fix one of the five screen doors on your submarine,” says Michael Osterholm, the director of the University of Minnesota’s Center for Infectious Disease Research and Policy and a consultant to the World Health Organization on containment of infectious viruses.

The pandemic rattled the world’s public health experts. One in five people worldwide had been infected. The global vaccine response was concluded to be too little, too late. It took 41 facilities in six countries a year to produce 1.322 billion fewer vaccine doses than were needed. To extend a grim scenario to its darkest, the only thing that kept 1 billion people from dying, which would have had a cataclysmic effect on global markets, and could have toppled governments and caused panic and societal breakdown, was that this novel virus, for reasons unknown, had a death rate lower than some seasonal varieties—just 0.02 percent.

The winter after the 2009 pandemic, Osterholm and a team of flu experts issued their Report to the President on Reengineering the Influenza Vaccine Production Enterprise to Meet the Challenges of Pandemic Influenza. They recommended that $1 billion a year be spent on flu research. Meanwhile, another independent review concluded that “[b]ringing novel influenza vaccines to the global market would require a highly coordinated leadership effort similar to the mission critical prioritization of the Manhattan Project.”

Since then, Ebola and Zika have emerged from the tropics, each demanding its own unique response and casting flu to the dark side of the public spotlight. Such coordination hasn’t been realized and probably won’t be until the world falls ill again. The good news is that vaccine research has been ongoing and progressive. Just this past week, researchers at McMaster University in Ontario, Canada, announced they had identified antibodies in the immune system that can recognize a portion of the flu virus that doesn’t mutate or change year to year. The discovery is an enormous leap toward a “one-shot” flu vaccine giving lifetime immunity, which researchers estimate could be possible in five short years. Many experts remain skeptical that a silver bullet exists for a virus that has proved to be so adaptable. As Slemons likes to say, “The only thing that’s predictable about flu is that it’s unpredictable.” But it’s impossible to overstate how badly such a vaccine is needed. WHO estimates that the next flu pandemic could kill 165 million, sicken 1 billion, and cost the globe $3 trillion.

Dead ducks at a nature preserve in northern Ohio await testing for avian flu. (Photo: Ken Blaze)

It’s a hot and windy day a little more than a month after the first cases appeared at the Clark County Fair, and Bowman, eyes hidden behind a pair of off-brand wraparound sunglasses, is driving his Avalon west on Interstate 90 just below the speed limit. Corn rows and Lake Erie’s southern shores flicker by. Today he’s sampling influenza at a posh duck-hunting club between Detroit and Cleveland. “When something bad shows up on the radar, we try to hunt it down,” he says.

Bowman didn’t so much find flu as it found him. In 2007, he was working as a private vet when a barn full of pigs got sick at the county fair and passed the virus to people. Transmission of flu from pig to person has probably been happening forever, but until 2007, it was largely undocumented. “At the time, swine flu was a pig thing—a problem for pig owners to worry about—and that was pretty much it,” Bowman says.

That outbreak foreshadowed something far worse: the swine-origin flu that caused the 2009 pandemic. While that bug was still raging, the National Institutes of Health asked Slemons, who founded Bowman’s lab in the 1980s and was still in charge of it, to look for pandemic viruses that could emerge in the U.S. Slemons made a map of the most pig-dense region in Ohio and picked 15 fairs within it. Since then, the project has expanded to 100 fairs in Iowa, Indiana, and Michigan, while Bowman has continued to research flu in its host species. Last year he and his staff drove more than 20,000 miles between 90 county fairs and dozens of wildlife refuges, where they sampled thousands of wild birds and pigs to understand what viruses are moving between species and why. Bowman’s team had sampled pigs at the Clark County Fair just before the outbreak.

“We’ve been here long before the outbreak, and we’ll be here long after,” Bowman says, steering onto a dirt road. Cormorants slick with water and great blue herons rise from the swamp with ungainly flaps. He doesn’t think he’ll find H3N2v in the ducks he samples today, but given that Bowman finds flu in 5 percent of the birds he tests, there’s a good chance he’ll find something else.

The club looks like it should smell of cigars—overstuffed leather chairs are lined against the wall, and next to pictures of presidents who hunted here are wooden decoys priced at $10,000—but it’s the aroma of wet animals that permeates. In a picking room, where hunters clean the ducks, four dead teal are laid out on a wood block. Jacqueline Nolting, Bowman’s laboratory operations manager and a Ph.D. student at Ohio State, snaps on a pair of blue nitrile gloves. Birds shed flu from the south end; Nolting pulls back one duck’s tail feathers to reveal its cloaca. In goes Nolting’s Q-tip; out comes a feces stain. This is a skill nobody dreams of one day perfecting. “I once had a carny tell me my job sucks,” Bowman says. “I didn’t even tell him how many years I went to school for this.” (He has a master’s degree and two doctorates.)

Nolting breaks the Q-tip off in a library-pencil-size vial filled with a beef-brain and beef-heart infusion broth that sustains live virus. Back at the lab in Columbus, she’ll grow these samples in pathogen-free chicken eggs, isolate any existing virus, then pull from the cells a genetic sequence that can be used to track where the virus came from and predict where it might be going.

The next morning Bowman shows me where these samples will end up. From his office at Ohio State, decorated with a photo of him giving a giraffe a wellness exam, we ride an elevator downstairs to a room off a long hallway. Here is the lab’s virus collection. Separating one of the world’s richest repositories of flu virus and a stream of college kids is a door locked with the same kind of key-card system familiar to anyone who has stayed at a Comfort Inn. This doesn’t bother Bowman.

“My worst nightmare is that the power goes out, and we lose all this,” Bowman says, opening one of seven freezers in the room. Each freezer is connected to a phone that calls him at any hour if there’s an error, but he’d much prefer a backup generator. Bowman pulls from the freezer a four-foot-tall stack of cake-size boxes held together by cam straps—the bounty of his collection work. Each contains dozens of vials of live and isolated virus. The oldest sample dates to 1986. “When the next scary one emerges, we’ll go back and look at the viral history and say, is there anything else like it?” Bowman says. If there is, they can grow that virus from the archive and send samples to other researchers or the CDC for vaccine production.

Bowman’s lab is low security because unlike the CDC facility in Atlanta, where flus that have infected humans or killed thousands of poultry are kept, all the viruses here have so far been well behaved. That isn’t as comforting as it sounds; a flu that’s not deadly to birds can be extremely lethal to humans. “Look at H7N9,” Bowman says, clicking the freezer shut. The bug has killed 75 percent of the 600 people it has infected in China. Remember, the 2009 pandemic had a 0.02 percent death rate. H7N9 doesn’t kill birds, which makes it nearly impossible to track. It hasn’t spread from person to person—all of the infected had spent way too much time in places drenched in avian viruses. But give it, or any other flu virus, enough spins at the genetic roulette wheel, and it might.

A research assistant in a testing lab at the Animal Influenza Ecology & Epidemiology Research Program at Ohio State University prepares plates of cells for virus isolation. (Photo: David Bernstein)

Patterson and public health officials around the Midwest didn’t yet know, in August, how strong a virus they were dealing with. For two weeks after the first novel influenza cases emerged from the Clark County Fair, they kept ramping up their response. Patterson and his staff traded hundreds of emails with the CDC and the Ohio Department of Health on how to contain the outbreak without inciting panic. At county fairs, public health warnings broadcast over the loud speakers were increased, and fairgoers must have grown tired of hearing over and over again, “Please don’t eat or drink in the animal exhibits.… Please don’t sleep in the barns.…” They discussed quarantining sick pigs and people and delayed the transportation of swine to the Ohio County Fair until they could confirm the pigs weren’t sick. “I threw up as many roadblocks as I could to keep it in Clark County,” Patterson says.

Of course he wasn’t able to. Human cases popped up at fairs in northern Michigan and southern Ohio. By the end of August, the Midwest had 18 known cases and almost certainly more that hadn’t been reported. The link was that each patient had attended one of seven infected county fairs. Bowman’s team had taken samples at six of them. After the Clark County Fair, the state vet, in collaboration with the public health department, asked him to run his samples from that fair’s pigs. What he found was an identical match to the virus that was making the humans sick—a smoking gun. Not only were pigs the proved vector, but by comparing the viral swabs taken from swine snouts with human patients, health officials could see the virus wasn’t mutating in people. The sister of the 13-year-old was a false alarm; she hadn’t had flu, meaning H3N2v wasn’t spreading human-to-human after all. “We could finally peel ourselves off the ceiling,” Patterson says.

Up in Wayne County a few weeks later, Nolting suddenly stops her work. “You hear that?” she says. It was a dry hacking sound like a bark somewhere in the barn. “That’s a pig’s cough,” she says, not quite excited. No human cases of H3N2v have been reported in almost two weeks, but both she and Bowman agree it’s probably here, and if it is, chances are that most of the pigs have it. That means more chances to infect someone like the nursing baby or the ice-cream-eating guy in the cannabis cap. Or worse, more spins on the genetic roulette wheel.

I step out of the pen and walk through the barn until I see a 12-year-boy, Tyler, with a mop of blond hair, sitting in a closed pen with a gilt he has raised since birth. The pig turns to drink, and Tyler holds his fingers under the water pouring off her snotty snout.

“Her name’s Scrat,” Tyler says. She’s eight months old and he has spent nearly every day of her life using marshmallows to train her for yesterday’s competition. The ribbon they earned is pinned above Scrat’s cage—fourth overall, despite Tyler placing last in showmanship.

“I just didn’t know what to do with my hands,” he explains, scratching Scrat’s ear. “So I just kept touching her the whole time.”