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New York City live bird market

Bird flu viruses have been detected every year in the United States since the mid-1960s.2084 In just the last five years, more than a dozen outbreaks of viruses with the potential to mutate into highly pathogenic forms have been discovered.2085 But the largest to date still remains the 1983 Pennsylvania outbreak that spread down through Maryland and Virginia2086 and led to the deaths of 17 million domestic birds2087 at a cost to the nation of more than $400 million.2088

Investigators speculate that the H5N2 virus responsible for this outbreak may have started out in a flock of wild ducks that landed in a pond on a chicken farm in eastern Pennsylvania.2089 Duck feces on the boots of a farmer may have first brought the virus inside the broiler sheds.2090 The virus, like essentially all wild waterfowl viruses, started out benign, causing a drop in egg production or mild upper respiratory symptoms, but soon started “racing though giant commercial chicken warehouses.”2091 The now resident director of the University of Pennsylvania’s poultry laboratory explained that “with that many opportunities to mutate under those intensive conditions” the virus changed from one that gave chickens the sniffles to the “bloody Jell-O” virus Webster called “chicken Ebola,” causing birds to hemorrhage throughout their bodies.2092

Webster’s team performed genetic analyses of the H5N2 virus before and after it turned lethal. To their surprise, the two differed by only a single amino acid. Amino acids are building blocks strung together in chains that make proteins. The H5 hemagglutinin protein is more than 500 amino acids long.2093 All it took was a tiny point mutation in the viral genetic material to change the 13th amino acid in the H5 chain from an amino acid named threonine to one called lysine—a mutation that, in Webster’s words, “change[d] that benign virus into one that was completely lethal.”2094 “That such a tiny change in the virus could enable it to wreak so much havoc,” Webster and colleagues later wrote, “was an awesome discovery.”2095

The U.S. Department of the Interior‘s 127-year-old U.S. Geological Survey (USGS) represents the nation’s leading governmental authority on the biological sciences.2096 Reflecting on the evolution of low-grade to high-grade strains of bird flu, the USGS echoes other world authorities in implicating industrial poultry practices not only as providing an “excellent opportunity” for rapid spread (particularly when “poultry are housed at high densities in confined quarters”) but in part playing an “ideal” role in possibly sparking the next human pandemic.2097

H5N2 resurfaced two years later in low-grade form in Massachusetts, New Jersey, Ohio, and again in Pennsylvania,2098 all traced back to live poultry markets in New York City. A survey of live markets in 1986 found 48 harboring the virus,2099 suggesting to investigators that live poultry markets may have been the critical mixing point between ducks or geese and chickens that triggered the original Pennsylvania epidemic.2100

Efforts to purge bird flu viruses from live poultry markets over the years have been unsuccessful,2101 despite periodic quarantine, depopulation, cleaning, and disinfection. In 2004 an outbreak of highly pathogenic H5N2 was discovered in a 7,000-chicken broiler flock in Texas after the owner introduced a chicken from a live poultry market in Houston into his flock.2102 Considering the Hong Kong outbreak and other U.S.2103 and Italian outbreaks traced to live poultry markets,2104 USDA poultry researchers describe live bird markets as the “missing link in the epidemiology of avian influenza.”2105

The first human case of bird flu infection in the United States was in 2002. An H7N2 virus caused more than 200 outbreaks in chicken and turkey operations across a mass poultry production area first in Virginia, and then into West Virginia and North Carolina, leading to the destruction of almost 5 million birds.2106 It was a low-pathogenicity virus and only suspected in one human infection,2107 but genetic analyses show that it is mutating toward greater virulence.2108

In 2003, a person was admitted to a hospital in New York with respiratory symptoms and was confirmed to have been infected with the H7N2 bird flu virus. Despite a serious underlying medical condition, the patient recovered and went home after a few weeks.2109 By that year the virus had swept through millions of egg-laying hens in huge battery-cage facilities in Connecticut and Rhode Island,2110 outbreaks that the industry admits “confirm the vulnerability of egg production units.”2111 OIE expert Ilaria Capua describes it as “very difficult” to keep an industrial battery-cage egg facility clean and prevent spread from farm to farm via eggs, egg trays, and equipment. “In our opinion,” she told the Fifth International Symposium on Avian Influenza in 2003, “when the infection gets into a circuit, it will spread within that circuit. It finds its way to spread.”2112

The way H7N2 was found to spread in the United States was via live poultry markets. The markets were suspected in the outbreaks in Pennsylvania (1996,2113 1997, 1998, 2001, and 20022114 ), Virginia (2002),2115 Connecticut and Rhode Island (2003), and Delaware (2004).2116 The Delaware outbreak in a broiler operation confining more than 85,000 chickens spread to Maryland before being stamped out by killing more than 400,000 birds.2117 In two cases, direct epidemiological evidence links the presence of trucks hauling birds to live poultry markets at affected farms within a week before the appearance of clinical disease.2118 The trucks deliver birds from the farms to the markets, pick up the empty dirty crates, and then return to the farms. The “most likely scenario,” according to USDA scientists, is that the crates or trucks were not completely disinfected of the potential billions of infectious particles present with any gross fecal contamination.2119

The University of Georgia Southeastern Cooperative Wildlife Disease Study describes the U.S. live poultry market system as an “intricate web of retail markets, poultry auctions, wholesale dealers, and farm flocks.” The study notes that in this system, “birds may change hands up to five times before reaching the consumer,” increasing exposure and decreasing trackability.2120

Scientists have watched H7N2 since its emergence in live poultry markets in the United States in 1994. As mentioned earlier, the virus’s fail-safe mechanism that shackles it from becoming too dangerous in its natural waterfowl host is the hemagglutinin activation step that limits viral replication to “safe” organs in the body like the intestine. Once placed in a land-based host like a chicken, though, viral mutants that can infect all the victim’s organ systems may have a selective advantage since easy waterborne spread is no longer possible. H5 and H7 viruses can transform by accruing basic (as opposed to acidic or neutral) amino acids in the hemagglutinin protein cleavage site, where the enzymes of the host activate the virus. Once the virus accumulates approximately five basic amino acids, it may transform from a low-pathogenicity virus (LPAI) to a highly pathogenic virus (HPAI).

The earliest H7N2 isolates in U.S. live poultry markets in 1994 already had two basic amino acids in the critical cleavage site. By 1998, the virus was up to three. Then, in 2002, H7N2 viruses were found with four. Only one more tiny mutation and the virus could have become deadly.2121 Even though the virus was technically still an LPAI virus, the federal government could see the writing on the wall and stepped in to stamp out H7N2 wherever it escaped—and indemnify the industry.2122

Efforts to eradicate the virus at the source—in live poultry markets—have failed. According to the USDA Animal and Plant Health Inspection Service, “Despite educational efforts, surveillance, and increased state regulatory efforts, the number of [virus] positive markets has persisted and increased.” In 1998, 30% of the markets were infected with H7N2, particularly in the New York metropolitan area. New York has more live markets than all other states in the Northeast combined.2123 By 2001, inspectors could find the virus at 60% of markets at any one time.2124

The states were failing to control the problem. With the virus dangerously close to potentially locking in that final mutation, the USDA had to intercede, coordinating a system-wide closure of all retail live poultry markets throughout the northeastern United States in 2002. Following the mass closure, all birds were sold off or killed, and all markets were cleaned and disinfected, left empty for days, and then repopulated with birds only from closely monitored source flocks confirmed to be negative for all avian influenza viruses. Then they watched and waited. Within five weeks, H7N2 was back.

It is unknown whether the virus somehow persisted in the markets or was reintroduced. Regardless, despite their best efforts at eradication and control, it seems clear that live poultry markets represent a public health risk. Writing in the Journal of Virology, USDA researchers concluded that “the rampant reassortment of AIVs [avian influenza viruses] in the LBMs [live bird markets] could increase the risk of species crossover because it would increase the chances of the occurrence of the correct constellation of genes to create a virus that replicates efficiently in mammals.”2125

The mass market closure and disinfection did seem to knock the virus back a step, though, back to three basic amino acids.2126 Still, unless all live poultry markets are closed, H7N2 will presumably continue its march towards virulence. As the director of the virology lab at Cornell University’s Animal Health Diagnostic Center put it, “It is two major mutations away from becoming a virus that could kill a lot of chickens and become much more pathogenic to people.”2127 In 2006, USDA researchers published the results of a study which genetically engineered mutants of an H7N2 virus discovered in New Jersey. They found that the insertion of just a single basic amino acid in the right place could transform the virus into a highly pathogenic form.3184 Currently, many suspect that H5N1 is going to beat H7N2 to the pandemic punch, but were it not for H5N1, the betting might be on live poultry markets in New York City—not Hong Kong—to deliver the next killer superflu virus.

According to the USDA’s Agricultural Research Service:
The U.S. currently has the largest, most genetically homogeneous and, thus potentially, the most disease-susceptible population of food animals in the history of mankind…The emergence of a new disease or a slight shift in the epidemiology of an existing disease could lead to immediate and disastrous results for American livestock producers and consumers.2128
In light of the emergence of SARS and H5N1 from live animal markets, a 2006 scientific review concluded that “the most optimal strategy is to forbid all kinds of live animals at wet-markets, with enforcement of central slaughtering.”3183 If traditional live bird markets can be successfully shut down in Asia, they should be able to be shut down in North America as well. Starting in 2008, those found publicly slaughtering birds in Taiwan, for example, may face a NT$500,000 fine (≈US$15,000).3181 Though there has never been a recorded outbreak in Taiwan, the Chairman of their National Science Council explained their reasoning behind the ban: “We can't foresee whether an outbreak of bird flu will happen in Taiwan, but every nation in the world is obligated to take part in the prevention of the epidemic.” 3182

The Virginia outbreak in 2002 that led to the deaths of millions of birds and found its way onto hundreds of farms highlights just how wishful the thinking is that industrial poultry populations are protected by biosecurity. Based on the rapid spread of bird flu in United States in 2002, leading USDA poultry researchers have concluded the obvious: “[B]iosecurity on many farms is inadequate.”2129 The situation has not necessarily improved since then, according to the executive editor of Poultry magazine and professor of poultry science at Mississippi State. In 2005, she editorialized “I believe it is time to reexamine biosecurity in our industry. We’ve become lax in many ways, and this is exactly what it took to get the 1983 AI outbreak moving.” She continued, “If WHO is right and a pandemic brings human AI to the United States, will you be able to look your family and neighbors in the eye and say you’ve done all you can to stop the spread? Having to answer that question alarms me!”2130
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