Viral Swap Meets

Live Poultry Market

To take advantage of this feathered bounty, the H5N1 virus first had to find a way out from the guts of waterfowl. How did the Guangdong goose H5 ever find the duck N1 in quail? How did the goose-duck H5N1 hybrid find its way from quail to Hong Kong chickens? And how did the virus spread from farm to farm? Although some have proposed live poultry delivery trucks improperly cleaned between separate hauls of different bird species as the culprit, the more likely explanation may be cross-contamination at live bird markets.¹³⁴⁰

Professor Kennedy Shortridge, the virologist who first characterized H5N1 in Asia, may have predicted its site of emergence years before its appearance. In 1992, he urged surveillance in “Hong Kong, as the place with the most extensive contact with China and a possible place of exit of an emerging pandemic virus.”¹³⁴¹ What is it about China that makes it such a hotbed of influenza virus activity? Shortridge blames the “great diversity of influenza viruses in the duck population in this region”—a function, in large part, of “the mass production of ducks for human consumption….”¹³⁴²

For centuries, Guangdong province has had the largest concentration of poultry, pigs, and people in the world.¹³⁴³ The “Asian flu” of 1957 and the “Hong Kong flu” of 1968 are just the latest two examples of pandemics arising in the region. Historical records dating back centuries link emerging influenza epidemics and pandemics to this area of the world, although the first pandemic for which we have cogent data was the one that preceded 1918 in 1889.¹³⁴⁴

Guangdong surrounds and feeds Hong Kong, one of the most heavily populated areas in the world: The city’s seven million people¹³⁴⁵ are packed into densities exceeding 50,000 people per square mile in some areas.¹³⁴⁶ A survey of nearly a thousand Hong Kong households¹³⁴⁷ found that 78% prefer “warm” meat.¹³⁴⁸ One hundred thousand chickens stream into Hong Kong everyday from Guangdong¹³⁴⁹ to be sold alive in more than a thousand retail markets, stalls, and shops.¹³⁵⁰ As one influenza expert quipped, “Hong Kong is one big bird market.”¹³⁵¹

This preference for just-killed poultry provides what Shortridge calls an “avian influenza virus melting pot.”¹³⁵² Chickens and ducks, geese and quail are crammed into small plastic cages stacked as much as five high in these live animal “wet” markets. Distressed birds defecate on those below them.¹³⁵³ Feathers and feces are everywhere.¹³⁵⁴ So are blood and intestines.¹³⁵⁵ According to the World Health Organization, the birds are often slaughtered on the spot, “normally with very little regard for hygiene.”¹³⁵⁶ “The activities of humans have affected the evolution of influenza,” reads a 2004 Cambridge University Press textbook on pathogen evolution, “but not to our advantage. Close confinement of various strains of fowl in live poultry markets provide conditions ripe for the formation of new reassortment viruses and their transmission to humans.”¹³⁵⁷ If live animal markets turned a cold virus into a killer in the case of SARS, it may help turn a flu virus into a mass killer.

According to the Hong Kong survey, householders buy an estimated 38 million live chickens every year, generating millions of human-chicken contacts.¹³⁵⁸ “They touch the neck and blow on the other end to see how good it is,” one Hong Kong microbiologist explained, holding up and turning his hands as if looking at the bird’s posterior.¹³⁵⁹ According to the University of Hong Kong School of Public Health, vendors and consumers are inevitably contaminated with fecal dust at these markets.¹³⁶⁰ Scientists were not surprised, then, that H5N1 surfaced first in Hong Kong.¹³⁶¹

Birds who remain unsold at the end of the day may go back to the farms of Guangdong, taking whatever new viruses they picked up with them.¹³⁶² Webster and colleague D. J. Hulse wrote, “Highly concentrated poultry and pig farming, in conjunction with traditional live animal or ‘wet’ markets, provide optimal conditions for increased mutation, reassortment and recombination of influenza viruses.”¹³⁶³ Once the cycle has been sufficiently repeated, a virus can then use Hong Kong to escape. As the travel and commercial hub of Pacific Asia, Hong Kong represents a viral portal between the intensive farms of rural China and the human populations of the world.¹³⁶⁴

In response to the emergence of H5N1, the government of Hong Kong has tried separating different species and ordered all duck and geese intestines packed when being sold in live chicken stalls to reduce cross-contamination. Over the long term, the UN Food and Agriculture Organization has asked Hong Kong to move toward centralized slaughter facilities, a touchy subject with political as well as economic implications.¹³⁶⁵ Paul Chan, a professor of microbiology at Chinese University of Hong Kong agrees, “I support doing away with selling live poultry altogether.”¹³⁶⁶

Even if all Hong Kong live markets were closed, argues Webster, this would be unlikely to reduce the overall pandemic risk unless live markets could be closed throughout China and elsewhere.¹³⁶⁷ The China Wildlife Conservation Association estimates that within Guangdong province itself, several thousands of tons of wild birds are consumed in special stores each year, where they may mix with farmed birds before they are slaughtered for food.¹³⁶⁸ Bird markets outside of Hong Kong may be subject to even less regulation and are likely accompanied by less intensive surveillance for disease as well.¹³⁶⁹ China has set the precedent, however, of attempting¹³⁷⁰ to ban all live bird markets in Shanghai, its largest city, as well as the capital city of Beijing.¹³⁷¹ Hong Kong has also finally decided to phase them out,¹³⁷² and the Chinese government has reportedly urged all big cities to “gradually call off the killing and sales of live fowls in the market.”³¹⁷⁷. Similarly bans have reportedly been proposed in Singapore, Bangkok,³¹⁷⁸ Japan³¹⁷⁹ and Vietnam’s Hanoi, Hai Phong, Vinh and Ho Chi Minh City.³¹⁸⁰ “Until the traditional practice of selling poultry in the live market changes,” concludes Webster’s team, “we will have to accept that live markets are breeding grounds for influenza viruses….”¹³⁷³

These breeding grounds are not limited to Asia.¹³⁷⁴ We shouldn’t forget that before H5N1, the biggest outbreak of bird flu in history wasn’t in China; it was in Pennsylvania. In the 1980s, the United States suffered the most costly and extensive disease eradication in its history, the outbreak of H5N2 that led to the deaths of 17 million chickens at a cost to taxpayers and consumers exceeding $400 million.¹³⁷⁵ The outbreak may have been linked to live bird markets in the northeastern United States.¹³⁷⁶ Before then, highly pathogenic bird flu had struck in the 1920s and later occurred in Texas in 2004. Both of these other high-grade bird flu incidents,¹³⁷⁷ ,¹³⁷⁸ as well as most of the latest U.S. discoveries of low-grade viruses, have also been tentatively linked to U.S. live poultry markets.¹³⁷⁹

The USDA estimates more than 20 million birds of different species pass through 150 known storefront live bird markets just in northeast metropolitan areas every year.¹³⁸⁰ Unlike Hong Kong, which learned its lesson and now segregates waterfowl from terrestrial species, U.S. ducks and chickens are still crammed on top of one another.¹³⁸¹ As in Hong Kong markets, cages are generally stacked four to five tiers high, ensuring plenty of fecal splatter from distressed birds.¹³⁸² “If you have seen these markets, you know that the birds are under stressful conditions,” said a veterinarian with New York’s Department of Agriculture. “And birds under stress are much more prone to disease.”¹³⁸³

Though suspected to play a pivotal role in the spread of bird flu in the United States,¹³⁸⁴ the problem seems to be worsening. In New York City, for example, the number of live bird markets almost doubled from 44 in 1994 to more than 80 in 2002.¹³⁸⁵ Given the risk, many in the U.S. commercial poultry industry are “absolutely determined” to have live markets eliminated, according to a Louisiana State University poultry scientist.¹³⁸⁶ Briefly but incisively, the president of the USA Poultry and Egg Export Council commented, “We can’t jeopardize the entire U.S. [poultry] industry.”¹³⁸⁷

The USDA agrees that live bird markets have been shown to present a “major risk” to the nation’s poultry industry.¹³⁸⁸ USDA scientists write, “The live bird markets of the Northeast remain the biggest concern for the presence of avian influenza in the United States.”¹³⁸⁹ If both the industry and the USDA agree (as they tend to do), why have live bird markets persisted and indeed been allowed to flourish? Some industry officials fear that closing bird markets would drive the entire trade underground, making it even more difficult to regulate.¹³⁹⁰ After SARS, for example, customer demand in Asia drove the cost of civet cats up to $200, making it likely that such animals could be obtained regardless of legality.¹³⁹¹ The USDA has therefore chosen to “manage or mitigate the risk rather than to outlaw it.”¹³⁹²

By its own admission, the USDA is doing a poor job of risk management. Speaking at the Fifth International Symposium on Avian Influenza in 2002, USDA poultry researchers said, “Considerable efforts are continuing on the part of industry and state and federal governments to control influenza in the LBM [live bird market] system, but currently the efforts have been unsuccessful.”¹³⁹³ “Despite educational efforts, surveillance, and increased state regulatory efforts,” the USDA admitted the following year that “the number of [bird flu] positive markets has persisted and increased.”¹³⁹⁴ Live bird markets seem inherently risky. In response to virus isolations from New Jersey’s markets, the State Veterinarian said, “They can be doing everything right and still have a market that tests positive.”¹³⁹⁵ Despite risk mitigation efforts, experts at USDA and the University of Georgia concluded in a 2006 review that U.S. live bird markets remain “an ideal environment for transmission, adaptation and evolution of avian influenza viruses.”³¹⁷⁶

Even if a segment of the live bird trade was forced underground, it might not get much worse. Record-keeping in live poultry markets is already sparse or nonexistent even as to the birds’ countries of origin.¹³⁹⁶ Currently, the purchase and sale of live birds is a cash business in which market owners are “disinclined to keep accurate records that would be costly if subjected to IRS scrutiny.”¹³⁹⁷ A 2003 survey of handling practices at live bird markets found that fewer than 2% of suppliers followed the recommended biosecurity practices to prevent the spread of the disease.¹³⁹⁸ USDA Science Hall of Famer¹³⁹⁹ Charles Beard is concerned that U.S. live bird markets could be the portal by which H5N1 enters commercial poultry flocks in the United States.¹⁴⁰⁰

Live bird markets continue to exist in the United States only because local health authorities continue to license them. They are exempt from federal meat inspection laws because they slaughter fewer than 20,000 birds a year,¹⁴⁰¹ an exemption that doesn’t apply for other animals.¹⁴⁰² Poultry specialists predict that if live bird markets had to be held to the same federal standards of inspection, cleanliness, and pathogen control as the commercial poultry industry, or small producers of other animals, “authorities could virtually eliminate LBMs.”¹⁴⁰³

The University of Hong Kong School of Public Health laid out the pros and cons: “The trade-off between the preference for eating the flesh of freshly slaughtered chicken and the risk to local, regional, and global population health from avian influenza should be addressed directly, and in terms of a precautionary public health approach aimed at providing the greatest benefit to the maximum possible number of people.”¹⁴⁰⁴

Robert Webster, considered the world’s authority on avian influenza, concludes a landmark article on the emergence of pandemic strains of influenza with these words: “An immediate practical approach is to close all live poultry markets….” He goes on to note that with refrigeration systems widely available—even through much of the developing world—it is no longer necessary to sell live or just-slaughtered birds. “The reality is that traditions change very slowly,” he said, but “a new pandemic could accelerate this process.”¹⁴⁰⁵