A fowl plague: small farmers are the main victims of avian flu--even when they don't get sick.

Since the latest avian flu outbreak began in late 2003, the virus has struck at least 250 people, killed more than 100 worldwide, terrified millions, and prompted governments to take rapid and decisive action. Agriculture and health officials--men and women in suits and white lab coats, not farmers--embarked upon drastic but seemingly necessary steps to stop the flu's spread, including culling tens of thousands of chickens and other birds in areas where outbreaks occurred, vaccinating chickens and other poultry (with often expensive medications), and recommending that people have less physical contact with their chickens.

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The media, national governments, and development agencies have often blamed the spread of the disease on small rural and urban poultry farmers. Rural farmers especially depend on livestock to meet their daily needs for transportation, food, and fuel. And the cities of the developing world house an estimated 800 million farmers, many of them women, raising crops and animals for food, transportation, and income. It is those backyard and rooftop producers, some claim, with their unsanitary production and processing methods, that have encouraged the spread of avian flu--for example, by allowing chickens and other animals to roam freely in back yards and houses, and selling and killing live animals at wet markets, practices that are centuries old. A senior official of the UN Food and Agriculture Organization (FAO) said in 2005 regarding avian flu, "The backyard chicken is the big problem and the fight against bird flu must be waged in the back yard of the world's poor."

As a result, at least 15 nations have restricted or even banned freerange and backyard production of birds, endangering the livelihoods of countless small farmers and jeopardizing the availability of affordable food for consumers. In June 2006, for instance, the government of Ho Chi Minh City, Vietnam, asked people to give up raising poultry; the ban may remain in place for months or even years. Vietnam has had one of the highest human death rates from avian flu, second only to Indonesia; more than 40 people have died over the last three years. In Cairo, Egypt, too, where women often raise chickens as a vital source of income, the government has outlawed all backyard poultry production, while in Laos and Indonesia, health and government officials are encouraging farmers to stop raising poultry.

But the blame for avian flu and other emerging animal diseases--bovine spongiform encephalopathy (BSE), Nipah virus, and others--cannot be placed on the backs of small farmers (or migratory birds, as some officials at the World Health Organization and FAO have suggested). Recent studies in Asia and Africa indicate that the real culprits may be factory farming and the globalized poultry trade and transport of livestock.

Disease Hatcheries?

People in developing countries now consume half of the world's meat, thanks to rising incomes and exploding urbanization. And cities in the developing world are not just consuming more animal products, they're also becoming centers of production. One of the main risk factors for the emergence and spread of new diseases is increasing demand for animal protein and the adoption of industrial production practices. A visitor to any factory farm will see chickens, pigs, and cattle crammed tightly together in cages, stalls, or feedlots and covered in manure. These animals also look very similar and for good reason: as demand for meat and other animal products grows, producers have abandoned local or native breeds in favor of livestock with very specific genetic traits, including the ability to gain weight quickly or produce more milk. This homogeneity, however, makes animals more vulnerable to disease and compels producers to use antimicrobial drugs, which in turn can lead to antibiotic resistance in animals and humans alike.

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Rising demand has helped drive livestock production from rural mixed farming systems, where farmers raise a few different species of animals on grass, to intensive periurban and urban production of pigs and chickens that eat processed feed made from corn and soybeans. These confined animal feeding operations (CAFOs), or factory farms, create the perfect environment for the rapid spread of disease between animals and, often, people. Thanks to unregulated zoning and subsidies that encourage livestock production, huge chicken and pig CAFOs are moving closer to major urban areas in China, Bangladesh, India, and many countries in Africa. This, says Michael Greger, a veterinarian with the Humane Society of the United States and author of Bird Flu: A Virus of Our Own Hatching, is "bringing together the worst of both worlds--the congested inner cities of the developing world combined with the congested environment on industrial farms." A 2005 report by the World Bank asserts that this "extraordinary proximate concentration of people and livestock poses probably one of the most serious environmental and public health challenges for the coming decades."

Just a few months ago, for example, avian flu reemerged in Thailand. This latest outbreak was called a "national threat" and the government declared one-third of the country a disaster zone. Even Bangkok was not immune because, as in so many cities around the world, people there raise chickens in their back yards and even in their apartments. The Thais thought they had gained control of the disease by massive culling and vaccination efforts in 2004 and 2005. But the unreported story behind this outbreak is that there are huge factory farms across Thailand. They are owned by CP Group, one of the biggest poultry producing companies in the world, with facilities in Thailand, China, and other Asian countries. According to a 2006 report by the Barcelona-based agriculture NGO GRAIN, CP is present in nearly every country where bird flu has broken out. In Thailand, where it is headquartered, it contracts with approximately 10,000 growers; in China it is the biggest supplier of poultry chicks and runs a hatchery in bird flu-infested Lanzhou province. CP also owns half of the industrial poultry operations in Vietnam; in 2004, 117,000 birds infected with the flu were killed at a CP farm in Ha Tay province. GRAIN points out that while CP is not solely responsible for the current bird flu crisis, it's hard to ignore the growing role industrial agriculture plays in spreading disease. Like other factory farms, the CP farms concentrate thousands and thousands of birds in sheds, making it easy for diseases to erupt and then spread quickly. The movement and trade of poultry across Thailand also likely helped the disease spread from big farms to small backyard producers.

In India, the production of poultry and eggs in urban areas has expanded tremendously over the last 30 years thanks to the "Tysonization" of the chicken industry. Tyson Foods touts itself as the biggest producer of protein on the planet, and its success is due to John Tyson's idea in the 1930s to control every aspect of the chicken business from start to finish. By buying up feed plants, starting hatcheries, contracting with producers, and building processing plants, Tyson created a system of vertical integration in which the company owns each of its millions of chickens from before they hatch to the day they're slaughtered. Now the same thing is happening in India and other developing countries.

The rapid commercialization of the poultry industry over the last 40 years has allowed India to become the world's fifth largest producer of eggs as well as a leading producer of broilers, or meat chickens. And 70 percent of the nation's eggs and poultry meat are consumed in urban areas. As production has shifted from back yards to factory farms, there has been a growing tendency to place these facilities near cities, because in countries (like India) with poor infrastructure, such as roads and refrigeration, it seems to make perfect economic sense to large agribusiness companies to have food production as close to cities--and consumers--as possible. And while locating hatcheries, factory farms, and slaughterhouses near cities makes it easier to transport animals and for eggs and meat to reach consumers, the close concentration of birds next to densely populated cities can help create and spread disease. The first case of avian flu in India was discovered in a factory farm near the small town of Navapur, a fairly isolated community near the Gujarat border. Indian officials initially tried to blamed the outbreak on wild birds and small poultry farms, but it's likely, according to the GRAIN report, that the infected chickens came from Venkateshwara Hatcheries. Venkateshwara is India's biggest supplier of poultry and poultry products and ships all over India, including to Navapur. The company denies its involvement.

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Despite the continued insistence that freerange birds and chickens are responsible for avian flu, there have been no recorded deaths from avian flu from backyard farms in India. Nevertheless, according to Dr. Sagari Ramdas of the India-based veterinary group ANTHRA, as part of the international and national avian flu control strategies in India, huge numbers of unaffected backyard poultry were slaughtered in areas that fell into quarantine zones. Avian flu has existed among backyard flocks for centuries, but it doesn't evolve to the highly pathogenic form, such as the H5N1 virus that is spreading now, on backyard farms. Backyard poultry are more genetically diverse and there are far fewer birds than found in factory farms, making them more resistant to disease. However, even genetically diverse native chickens can't remain immune to the virus for long; it circulates from factory farms to backyard flocks and then back to factory farms, becoming more virulent. Although having birds concentrated together in large factory farms may make it easier to monitor chickens and eradicate infected flocks, freerange birds are less likely to encourage an outbreak in the first place.

In Laos, according to GRAIN, 42 of the 45 outbreaks of avian flu during the spring of 2004 occurred in factory farms. Thirty-eight of those outbreaks were in the capital, Vientiane. The few small farms where outbreaks occurred were located close to commercial operations. In Nigeria, the first cases of avian flu were found in one of the nation's industrial broiler operations. The virus spread from that 40,000-bird farm to 30 other factory farms in the country--and then quickly to neighboring backyard flocks, forcing already poor farmers to kill their chickens.

Worse Cures

While H5N1 may have been a product of the world's factory farms, it's small producers who have the most to lose from many of the policies implemented to control the virus. For the poor in developing countries, freerange poultry--which typically eat bugs and kitchen scraps in addition to small amounts of grain--are a cheap source of protein as well as income, especially for women and children. Because small producers forced to cull their birds are rarely compensated for the full market value of the dead chickens, they sometimes hide chickens from authorities, leading to the further spread of the disease. This practice has been seen in Cairo, where a law banning outdoor production of chickens has not provided adequate compensation to people for getting rid of their flocks or any incentive for people to report sick chickens to authorities. As a result, people have resorted to hiding their poultry in their homes and even under their beds. According to Dr. Linda Logan, an official with the U.S. Department of Agriculture's Animal and Plant Health Inspection Service, all of the people infected in Egypt have been women who have been hiding birds in their homes.

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But even paying farmers for their chickens may not be an ideal solution. In Indonesia, for example, where the government is having a hard time controlling the flu and where more than 55 people have died since 2005, nearly every household keeps poultry. Giving these people money for their dead chickens won't compensate them for the other things the chickens provide. "It is difficult to put a value on things that people value differently," says Dr. Mohammed Husenni Omar of Cornell University's College of Veterinary Medicine. "Some people think in economic ways and some people think in social. We know the virus is always going to be there, it is not going to run away. But we are depriving people of proteins, giving them money which they might spend otherwise. So it is a very complicated issue."

In rural areas, regulations to control the spread of avian flu may also have the unintended effect of pushing rural farmers off their land and into cities. In just the last 50 years, some 800 million people have moved from the countryside to the cities in search of higher incomes and better lives. But a 2006 FAO study says that investing more in rural agriculture, including training of community veterinarians to help spot diseases, can help ease rural-to-urban migration, decrease poverty, and curb crime, pollution, and other problems in cities. "Properly managed, agriculture can not only produce food but also have a positive impact in such areas as poverty alleviation, food security, population distribution, and the environment," according to the Japanese-funded Roles of Agriculture program, which was launched in 2000 and targeted 11 countries.

Uneasy Neighbors

Siting CAFOs near cities leads to a daunting variety of problems. Besides H5N1, the spread of a whole range of other emerging animal diseases and food-borne pathogens, including Nipah virus, Streptococcus suis (swine fever), BSE, and E. coli, has been linked to factory farming near urban areas. Moreover, large neighboring concentrations of animals and people can also provide perfect opportunities for agroterrorism. In this era of terror alerts, farms that forsake genetic diversity have shed their battle armor. Despite their mammoth technological capabilities, huge factory farms crammed with chickens or pigs are much more vulnerable than smaller, more diverse farms to the unintended or malicious introduction of disease. "The loss of livestock genetic resources makes it harder for livestock to survive a disaster, whether it be natural, man-made, or terror-caused," says Chuck Bassett of the American Livestock Breeds Conservancy. "One properly placed vector can wipe out 90 percent of an indoor flock--no problem. In a flock with more broad genetic spread, that is harder to do." Peter Chalk, an agroterrorism expert at the RAND Corporation, says that terrorists "choose the path of least resistance. Attacking agriculture is far more simple than using bombs because of inherent vulnerabilities within the system." And as more factory farms are built closer to urban areas, terrorists may see them as easier and easier targets.

Another vulnerability of industrial agriculture is the rapid and extensive movement of animals and agriculture products from both rural and urban farms to processing plants and then to consumers. Transporting animals and agricultural products long distances increases the number of entry points for terrorists to introduce toxic agents. "These openings for contaminants," says Chalk, "combined with the lack of security and surveillance at many processing and packing plants, have helped to substantially augment the technical ease of orchestrating a food-borne attack." More than 44 million cattle, pigs, and sheep are traded across the world each year, and millions more are transported over long distances by road and rail within countries. In the United States, more than 50 million animals are transported between states each year. And it's not just animals: millions of tons of meat, eggs, and milk are also shipped long distances. (A kilo of meat typically travels 1,600 kilometers before it is consumed.) A June 2005 report in the Proceedings of the National Academy of Sciences notes that just a few grams of botulism, poured by bioterrorists into a dairy tanker truck, could cause hundreds of thousands of deaths and billions of dollars in economic losses in the United States alone. Because the milk from multiple farms is consolidated in tankers, the toxin could be widely distributed and consumed within days by more than 500,000 people.

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Tough S***

Other aspects of urban livestock production also present public health challenges. In many parts of the world, including the east coast of China, in Thailand around Bangkok, and in Brazil in the state of Sao Paulo, there is, according to a report by the World Bank, an "excessive concentration" of factory farms, along with an excessive concentration of animal manure. Some provinces on China's east coast, close to both consumers and good port facilities, have a livestock density of over 500 livestock units per square kilometer, which is five times as many animals as the surrounding land can handle. Globally, only about half of all livestock waste is effectively fed into the crop cycle. Much of the remainder ends up polluting air, water, and the soil itself. Nitrate from manure can seep into groundwater, for example, and high nitrate levels in wells near feedlots in the United States have been linked to a greater risk of miscarriage. Moreover, the grain-heavy diet of animals in factory farms encourages the growth in their digestive systems of pathogenic E. coli, which during slaughter can contaminate meat. If manure from factory farmed animals is used as fertilizer, the pathogen can contaminate vegetables. This mechanism is a leading possible cause of the recent deadly spinach episode in the United States.

Even raising smaller herds of freerange livestock in cities can present waste management problems. In the city of Kisumu in western Kenya, keeping livestock in the city is officially illegal. Despite this very long-standing ban, however, many urban Kenyans, as well as the inhabitants of other cities, rely on livestock for both income and food. But the problem in Kisumu is that there is little land available to absorb animal manure. Cattle can produce very large amounts of dung--from 6 to 11 kilograms each per day. According to a recent study by Lagrotech Consultants, three-fourths of the dung produced in the city is not utilized as fertilizer for growing crops nor as a source of fuel. And because there is no regular waste removal system in the city, the manure piles up, contaminating soil and water and presenting a significant health hazard.

One way to prevent these problems is simply to discourage large producers from keeping animals in or near cities. A recent FAO report suggests that a combination of zoning and land use regulations, taxes, incentives, and infrastructure development can encourage producers to raise animals closer to croplands, where manure can be used as fertilizer and where there is less risk of disease transmission to people. According to FAO, controlling land and livestock nutrient imbalances means raising livestock in areas that have enough land to handle the waste from large operations. Thailand, for example, has levied high taxes on poultry production within a 100-kilometer radius of Bangkok, while exempting farmers outside that zone. As a result, over the last decade poultry production near Bangkok has dropped significantly.

But more fundamental changes have to occur within the meat industry. Factory farms are allowed to get away with a variety of economic and ecological crimes, but they are only "efficient" because they don't have to pay the true cost of their inputs--for example, subsidized cheap corn and soybeans to fatten cattle--or their outputs, including the spread of disease and pollution. So bigger definitely does not mean better. Recent studies by the International Food Policy Research Institute, in fact, suggest that small livestock farms may be more efficient than large production operations at generating profits per unit of output.

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Carefully designed policies to support urban livestock farming can serve cities' need for nutrition and economic opportunity without threatening them with disease. In Dar es Salaam, Tanzania, strict regulations concerning noise, dirt, and manure cleanup have framed an effort to encourage urban agriculture. Between 1985 and 2005, the number of animals kept in the city quadrupled and the amount of land under cultivation doubled, hundreds of jobs were created, and the availability of locally grown food increased dramatically. Housewives who keep cows or raise vegetables in their back yards report making two to three times more per year than their husbands by growing and selling food.

Blaming the poorest victims of the avian flu outbreak--urban and rural farmers in the developing world--will not stop pandemics, nor will outlawing urban livestock production. Despite bans on raising chickens and other livestock in cities, farmers will continue to raise animals because they must to survive. FAO, the World Health Organization, and other international agencies should focus their avian flu prevention efforts on the big poultry producers. Unfortunately, these agencies are using the avian flu crisis--and people's fear--to further industrialize the poultry industry and push small farmers out of business. Ironically, these measures will also decrease diversity and concentrate birds, increasing the vulnerability of both chickens and humans to the disease. "What people really need," says Devlin Kuyek of GRAIN, "is adequate and enforced protection from the transnational poultry industry." The industrial food system, which ignores or punishes small farmers, not only threatens their livelihoods but puts us all at risk for a potential pandemic. Reversing this trend will mean standing up for those farmers and demanding food production that is safe for animals and humans alike.

Danielle Nierenberg is a research associate at Worldwatch, specializing in food and agriculture.

For more information about issues raised in this story, visit www.worldwatch.org/ww/fowl.