It was a gray, damp January afternoon a few years back when I visited the Jiangfeng wholesale poultry market on the outskirts of Guangzhou, in the southern Chinese province of Guangdong. With its bleak wire enclosures and grid of cement paths, the place had the feel of a neglected 1970s-era urban zoo. And despite the comparatively narrow range of species there — chickens, geese, ducks, quails and partridges, mostly, with a smattering of rabbits and one large slumbering hog — it smelled like one, too. As I walked around, watched suspiciously by the market’s handsome young security guards, a slimy mix of bird droppings and decomposing feathers slowly crept up the heels of my clogs.
Every few months, it seems, an invasive virus from a distant land attacks the Americas: dengue, chikungunya and, most recently, Zika. But the pathogens that frighten me most are novel strains of avian influenza.
I’d come to see their birthplace. Highly virulent and easily transmissible, these viruses emerge from open-air poultry farms and markets of the kind that stretch across Asia. Thanks to rising demand for chicken and other poultry, they’ve been surfacing at an accelerated clip, causing nearly 150 percent more outbreaks in 2015 than in 2014. And in late 2014, one strain managed to cross the ocean that had previously prevented its spread into the Americas, significantly expanding its reach across the globe.
Novel avian influenza viruses are mongrels, born when the influenza viruses that live harmlessly inside the bodies of wild ducks, geese and other waterfowl mix with those of domesticated animals like the ones at Jiangfeng, especially poultry but also pigs. It’s possible to squelch their emergence. One way is to protect domesticated animals from the excreta of waterfowl, which can spread infection. But no such protections are in effect at markets such as Jiangfeng, which, like the rest of southern China’s booming poultry industry, lies within the East Asian flyway, one of the world’s most important waterbird migration routes.
The poultry enclosures are open to the air. Droppings from the birds in cages as well as the birds flying overhead coat the floor. Stony-faced women with shovels push the mess into reeking, shoulder-height heaps of wet mush. Any virus that lurks in those piles can easily spread to the birds and the people who tend them. Up to 10 percent of poultry workers in Hong Kong, a study has found, have been exposed to bird flu. A fine dust of desiccated bird waste permeates the air. It settles on the leaves of the workers’ makeshift vegetable plots behind the cages and on the window panes of their nearby flats.
These markets and the unique viral ecology they enable are not new, as Malik Peiris, a virologist at the University of Hong Kong, points out. But “now the situation is very different,” he said. “This is being done on a much bigger scale than it was years ago.”
As health-conscious consumers in the West cut beef out of their diets and newly affluent Asians add more meat to theirs, demand for bird flesh has skyrocketed. Global poultry production has more than quadrupled since 1970. And nowhere has the taste for poultry risen faster than in Asia, where chicken farming expanded by nearly 4.5 percent a year from 2000 to 2012. China now consumes more chicken than the United States. Tyson Foods aims to double production in China. “We just can’t build the houses fast enough,” Donnie Smith, the company’s chief executive, said to The Wall Street Journal, referring to poultry production buildings, and “we’re going absolutely as fast as we know how to go.”
It’s not just the growing scale of the poultry industry in Asia that increases the probability that new avian influenza viruses will emerge. It’s also the peculiar nature of the trade. About half of China’s poultry trade traffics in live birds. That’s because many Chinese consumers, wary of the safety of frozen meats, prefer to buy their chickens while they’re still clucking. This creates a wealth of opportunities for new viral strains to spread and adapt to human bodies. Rather than visiting the sterile frozen-food aisles of grocery stores, shoppers crowd into poultry markets, exposing themselves to live birds and their viral-laden waste. And to serve the markets, more birds travel from farms into towns and cities, broadcasting viruses along the way.
Most novel strains of avian influenza cannot infect humans. But some can, including three currently circulating strains: H5N1, a mash-up of viruses from geese and quail; H7N9, an amalgam of viruses from ducks, migratory birds and chickens; and H10N8, the product of viruses from wild birds, ducks and chickens. These viruses kill roughly 30 percent to 60 percent of their reported human victims. None can spread efficiently from one person to another, for example through sneezes and coughs, yet. But, given the opportunity, they will continue to evolve. And if they fine-tune their transmissibility among humans, the result will almost certainly be the kind of pandemic that epidemiologists most fear — one that could sicken a billion, kill 165 million and cost the global economy up to $3 trillion.
A majority of experts predicted, in a 2006 survey, that a pandemic would occur within two generations. That prediction is based, in part, on the increasing number of novel strains of avian influenza and the accelerating speed of their emergence. It’s also based on history. The virus that caused the influenza pandemic of 2009 killed an estimated 200,000 people, hitting young people in the Americas hardest. It originated in birds. So did the 1918 flu, which killed 50 million, including an estimated 675,000 Americans.
For years, experts considered the Americas comfortably isolated from the virulent avian influenza viruses hatched on distant Asian poultry farms and markets. “Being in North America,” said Carol Cardona, an avian disease expert at the University of Minnesota, “we weren’t bothered.”
Some of the novel strains of avian influenza emerging from the Asian poultry trade can be picked up and spread far and wide by migratory birds. But the migratory routes of these birds don’t cross the oceans. Even as they spread H5N1 and other pathogens into dozens of countries in Europe, Asia and Africa, the Americas remained untouched.
That changed in late 2014, when a highly virulent avian influenza from Asia infiltrated North America. Its prospects here differed from those in Asia. Relatively few people are regularly exposed to live poultry and their waste. And farmers protect their domesticated flocks from pathogens by screening and controlling ventilation in barns and by regularly disinfecting farm equipment.
Remarkably, none of these safeguards arrested the virus’s inexorable spread. It was as if the virus “knew the weaknesses of each individual farm,” said Dr. Cardona, “and found that and exploited it.” Infected farms euthanized entire flocks by smothering them with carbon dioxide or firefighting foam. From December 2014 to last June, more than 48 million domesticated poultry in 21 states were slaughtered, the majority in waterfowl-rich Minnesota and Iowa, in what the Department of Agriculture called the worst animal disease epidemic in United States history. By the time it ended, a 12-foot-wide ridge of bird carcasses from a single farm in Iowa stretched more than six miles.
Nobody knows just how this virus migrated over the oceans protecting the New World. But it’s possible that another consequence of human appetites — climate change — played a role.
While Asian and European birds don’t migrate into North America, they can pass on viruses to birds that do. That could happen in a place where millions of birds from both the Old World and New World are instinctively drawn every spring: the Arctic lands surrounding the Bering Strait, known as Beringia.
In the past, New and Old World birds in Beringia visited numerous ponds spread out across the tundra. But with temperatures in the Arctic rising twice as fast as anywhere else, conditions are changing rapidly, shifting the distribution of creatures and their pathogens. Historically segregated species are coming into novel kinds of contact. As birds are forced to migrate earlier and farther, feeding at new times and in new places, they overlap with other bird species in unprecedented ways that pathogens can exploit.
Some already have. In 2012, a parasitic roundworm normally found some 1,000 miles southeast turned up in birds in western Alaska. In 2013, birds in Alaska suffered their first epidemic of avian cholera, which typically infects birds in the lower 48 states.
While the precise conditions under which the virulent Asian-origin virus arrived in North America in 2014 remain murky, what’s known is this: Migratory birds picked up the virus from a poultry farm in Asia, carrying it with them into Siberia and Beringia for the breeding season. There, whether it was because of the new intimacy of the changed landscape, or because of something about the virus itself, the pathogen spread into other bird species, including those that would later head into North America, such as gyrfalcons and northern pintail ducks. By December 2014, they had brought the virus into British Columbia, Washington and Oregon, infecting wild and domesticated birds along the way and igniting the epidemic.
If this strain had been one that could infect humans, a deadly and disruptive public health emergency would have ensued. Luckily, it was not.
But there are more where it came from, at the growing interface between live poultry and humans on the other side of the Pacific. The workers at Jiangfeng, with their bare hands and tall boots, toil at its border. I watched them in the crowded enclosures as they lassoed birds around the neck with long, curved poles, stuffing them into plastic bins and loading them onto trucks. When a security guard caught me staring, I quickly walked away, footsteps muted by the membrane of bird waste encasing the soles of my shoes. Perhaps I could scrounge some bleach solution at my hotel with which to sterilize them, I thought to myself, although of course the birds whose lives and peregrinations are shaped by our appetites would not be so circumspect.
As I padded toward the exit, a stream of vehicles crammed with fowl, and whatever viruses replicated inside their feathery bodies, steadily rumbled out of the market, bound for points unknown.
Sonia Shah is the author of the forthcoming book Pandemic: Tracking Contagions, From Cholera to Ebola and Beyond.