There is no evidence that wild migrating birds mixing with backyard flocks spreads bird flu. Transnational factory farms and the globalised trade in poultry products are to blame. Dr. Mae-Wan Ho
The European Union is set to approve special funding for poultry farmers suffering from falling prices and demand as the spread of the deadly H5N1 bird flu scares consumers away from chicken, turkey and other fowl . Some 320 000 tonnes of unmarketable poultry meat are in cold storage across the 25 nation EU. Prices have fallen by 13 percent on average, but some countries are harder hit than others. Consumption of poultry products is down 5 percent in Denmark and Finland, but as much as 40 percent in Cyprus, 50 percent in Italy and 70 percent in Greece.
Germany has 70 000 tonnes of poultry products in storage, and estimates its sector has suffered damage of around 150 million euros from falling demand and the cost of culling birds. France with 40 000 tonnes in surplus stocks estimates it loses 31.9 million euros a month.
Bird flu is said to have spread from Asia to Europe in migrating wild birds. The United Nations Food and Agricultural Organisation (FAO) stated in November 2005 : “The movement of migratory birds has caused outbreaks to emerge in several countries and regions simultaneously.”
The first infection of commercial stocks was found on a French turkey farm in March 2006. The EU has ordered commercial stocks to stay inside or be inoculated, and some 45 countries have issued full or partial bans on poultry imports from France .
Meanwhile a fourth Afghan province, Kapisa, has been hit . The virus had been found already in samples from birds in Kabul, Logar and Nangarhar provinces. There are strong suspicions that two other provinces, Laghman and Parwan, are also affected. Afghanistan is on the migration route for several species of wild birds. Poultry have been culled and quarantine measures introduced in affected areas.
Nineteen African nations held a five-day conference towards the end of April 2006 to discuss how they should prepare for a possible deadly outbreak of bird flu . Nigeria, Niger, Cameroon, Egypt and Burkina Faso are the five African countries with confirmed H5N1 bird flu.
H5N1 has forced the slaughter of 200 million birds so far, as the disease spread from Asia to Europe, Africa and the Middle East. Late last year, thousands of migratory birds mysteriously dropped dead in central Malawi, though tests proved negative for H5N1. But the alarm has already hurt the poultry industry in Malawi, with most importers cancelling orders.
While scientists also say that wild birds are spreading the deadly bird flu, there are strong dissenting voices. The Royal Society for the Protection of Birds (RSPB), for example, told the BBC that the trade in birds and the movement of poultry products is a more likely cause . Significantly, there are no migration routes that would take birds from China to Turkey at this time of the year.
There is also little direct evidence that migratory birds carry and transmit H5N1. FAO in collaboration with World Health Organisation (WHO) had admitted in May 2005 , “To date, extensive testing of clinically normal migratory birds in the infected countries has not produced any positive results for H5N1 so far.”
After testing hundreds of thousands of wild birds for the disease, scientists have only rarely identified live birds carrying the highly pathogenic H5N1. In a test of 13 000 wild birds in marshes within the bird flu infested provinces of China, the H5N1 virus was found in only 6 ducks . But the scientists could not bring themselves to conclude that wild migrating birds are probably not to blame: “Our data show that H5N1 influenza virus, has continued to spread from its established source in southern China to other regions through transport of poultry and bird migration.”
The reality is that nearly all the wild birds that have tested positive for the disease were dead, and in most cases, found near to outbreaks in domestic poultry .
The WHO recently said that viruses from Turkey's first two human cases were virtually identical to those that killed 6 000 migratory birds in a nature reserve, Qinghai, in central China last year. But RSPB's conservation director Dr. Mark Avery insists that the trade in wild birds and the movement of poultry and poultry products, such as chicken manure used to fertilize fish farms, has led directly to the transfer of H5N1 across national boundaries .
“No species migrates from Qinghai, China, west to Eastern Europe,” BirdLife's Dr. Richard Thomas said. “When plotted, the pattern of outbreaks follows major road and rail routes, not flyways .
Wild fowl and shore birds are believed to form the reservoir of influenza viruses of type A, (see Box) which cause diseases in many other species, including humans, pigs, horses, mink, cats, marine animals and a range of domestic birds .
There are 3 types of influenza viruses, A, B and C. The influenza A virus genome consists of 8 segments of RNA coding for 11 proteins, and they are further classified by subtype on the basis of the two main surface glycoproteins (proteins with complex carbohydrate side chains): haemagglutinin (HA) and neuraminidase (NA). Only influenza A viruses infect birds. Humans can be inflected with influenza types, A, B and C viruses. Subtypes of influenza A currently circulating among people worldwide include H1N1, H1N2, and H3N2 .
Avian influenza A viruses of the subtypes H5 and H7, including H5N1, H7N7 and H7N3 viruses have been associated with high pathogenicity, and human infection with these viruses has r anged from mild (H7N3, H7N7) to severe and fatal disease (H7N7, H5N1).
Wild birds are the natural host for all known subtypes of influenza A viruses. In wild birds and poultry throughout the world, influenza A viruses representing 16 HA and 9 NA subtypes have been detected in numerous combinations, such as H1N1, H3N3, H16N3 and so on . Typically wild birds do not become sick when infected.
Domestic poultry such as turkeys and chickens can become very sick and die from avian influenza, and some avian influenza A viruses also can cause serious disease and death in wild birds.
Avian influenza viruses are designated as low pathenogenic (LPAI) when they do no cause disease or only mild disease, and highly pathogenic (HPAI) when they do. The switch from low to high pathogenicity is not fully understood.
The HA protein is synthesized as a single polypeptide precursor, which is cleaved into HA 1 and HA 2 subunits by proteases. The switch from low to highly pathogenic avian virus appears to be associated with basic amino acid residues introduced into the HA cleavage site, which makes the protein easier to cleave and facilitates virus replication.
In general, human infection with avian influenza viruses occurs very infrequently, and has been associated with direct contact with infected sick or dead domestic poultry. At least part of the barrier preventing person-to-person transmission is that the HA protein on the virus' coat must bind to cell surface receptors in order to gain entry into cells. This binding is specific for certain carbohydrate side chains attached to the cell surface receptor proteins. The HA of the avian virus recognizes carbohydrate side chains that end in sialic acid linked to galactose in an a -2,3 chemical bond, i.e., SA- a -2,3-gal, whereas the human influenza virus HA recognizes an a -2,6 chemical bond: SA- a -2,6-gal. The HA protein of H5N1 is typical of avian viruses, which is why the virus cannot replicate sufficiently in a human host for person-to-person transmission to take place. However, many scientists believe that once the H5N1 has mutated its HA to recognize SA- a -2,6-gal, then human transmission would occur, and a global pandemic would result
Influenza viruses evolve by small point mutations (antigenic drift) or large changes due to reassortment (antigenic shift), the mixing of genome segments from different viruses.
Certain birds, particularly water birds, are thought to act as hosts by carrying the virus in their intestines and shedding it in saliva, nasal secretions and faeces. However, the viruses circulating in wild birds are generally not the highly pathogenic avian influenza (HPAI) strains that cause deadly bird flu. They do not cause illness in the birds, and are referred to as low pathogenic avian influenza (LPAI) viruses. LPAI have been isolated from at least 105 wild bird species of 26 different families. All subtypes have been detected in the bird reservoir and in poultry, whereas relatively few have been detected in other species. Ducks, geese, swans, gulls, terns and waders are the major LPAI virus reservoir, where the virus preferentially infects cells lining the intestinal tract and is excreted in high concentrations in their faeces. Influenza viruses remain infectious in lake water for up to 4 days at 22C, and for more than 30 days at 0C. Faecal to oral transmission is the most frequent route for transmitting viruses, both of high and low pathogenicity.
The species in which influenza viruses are endemic, such as ducks, gulls and waders share the same habitat at least part of the year with other species in which influenza viruses are frequently detected, including geese, swans, rails, petrels and cormorants.
Wild migrating birds mostly follow routes (flyways) that go North-South, but some birds have breeding ranges that cross the Atlantic, and the birds over-winter in the same geographic area in the south. Migrating birds make frequent stops en route where different species congregate, increasing the chances of exchanging viruses among themselves and distributing LPAI viruses between countries and continents.
Since 1997, more than 16 outbreaks of H5 and H7 influenza have occurred among poultry in the United States. Highly pathogenic strains can cause 90 to 100 percent deaths in poultry. So how do low pathogenic viruses become highly pathogenic?
The influenza A virus genome is in eight separate segments. The segmented genome allows the viruses from different species to mix and exchange segments to create new influenza viruses. A pig infected with a human virus and a bird virus at the same time would allow the two viruses to exchange segments to create a new virus that retained most of the genes of the human virus but had the avian haemagglutinin and/or neuraminidase gene(s). The resulting new virus might be able to infect humans and spread from person to person (see Box). If this new virus causes serious illness in humans, then a pandemic would result. This g ene exchange could even take place in a human infected at the same time with human and avian flu viruses.
In 1997, an HPAI outbreak caused by H5N1 occurred in chicken farms and live bird markets in Hong Kong. This resulted in the first reported case of human influenza and death attributable directly to avian influenza virus. The H5N1 HPAI virus reappeared in 2002 in waterfowl at two parks in Hong Kong and was also detected in other captive and wild birds. It resurfaced again in 2003 and devastated the poultry industry in large parts of Southeast Asia since 2004. In 2005, the virus was isolated during an outbreak among migratory birds in Qinghai Lake, China, affecting large numbers of wild birds. This wiped out an estimated 10 percent of the global population of Bar-headed Geese. Subsequently, the virus reappeared across Asia, Europe and the Middle East, and in several African countries. Wild bird deaths have been reported in several of these countries in Europe, particularly affecting Mute Swans and Whooping Swans, but also other waterfowl species, and occasionally in raptors, gulls and herons. So far it has caused mortality in more than 60 wild bird species .
But do wild migratory bird carry and spread HPAI as has been claimed, or are they just the victims of the deadly bird flu viruses that emerge in domestic fowl?
Genetic analysis of avian influenza viruses in the public databases, based on the matrix protein gene M, reveals that the viruses can be divided into two distinct lineages , Eurasian and American, reflecting the long-term ecological and geographical separations of the hosts. Both lineages are also quite separate from human influenza viruses. The H5N1 highly pathogenic influenza viruses form a lineage derived from the Eurasian lineage.
The genetic separation between Eurasian and North American avian flu viruses is a bit surprising, as the bird fauna of North America and Eurasia are not absolutely isolated from each other. Some ducks and shore birds cross the Bering Strait during migration or have breeding ranges that include both the Russian Far East and Northwestern North America.
There are also other aspects of the virus that would appear to encourage genetic exchange between the two groups of avian flu viruses when the host birds meet up, such as the reassortment of viral genome segments (see above). Apart from that, the usual process of recombination (exchange of parts of genome segments) could also occur.
Not only do the avian flu viruses of Eurasia and North America form distinct lineages, the gulls in Eurasia and North America also each have their own distinct lineage of viruses. The evidence suggests that there are strong interspecific barriers to gene exchange, and it is not easy for viruses to jump species, and that complex adaptations are needed to achieve sustained transmission of the virus in a new species  (see “What can you believe about the bird flu pandemic?” this series).
The fact remains that HPAI viruses such as H5N1 are not endemic in wild birds as they are in domestic poultry, and when wild birds do contract the HPAI viruses, they succumb in large numbers, and are in no state to further transmit the disease along their usual migration routes .
As the researchers conclude : “For the H5N1 virus, it is without doubt that domestic waterfowl, specific farming practices, and agroecological environments played a key role in the occurrence, maintenance, and spread of HPAI for many affected countries… Although numerous wild birds have also become infected, it has been much debated whether they play an active role in the geographic spread of the disease…”
Wild birds are not the only victims of bird flu; the other victims are small farmers and ordinary people who keep domestic fowl in their backyard to supplement their income or diet.
In response to the spread of bird flu, governments around the world are destroying backyard flocks and making indoor confinement of poultry mandatory [8, 12]. So far, 16 countries in Europe, Asia and Africa have imposed bans or restrictions on outdoors poultry farming. Forced confinement of poultry threatens the livelihood and food security of small- scale farmers and poor families in countries affected by bird flu. In Southeast Asia, governments, supported by the FAO, are encouraging framers to set up mesh screens or bamboo enclosures for their poultry. The costs, estimated at US$50-70, are simply beyond the means of Asia's small farmers, and are forcing them to abandon poultry altogether . Forced confinement also threatens certified organic poultry operations, grass-fed pastured poultry and free-range egg production .
Quebec in Canada has imposed strict rules that require all farmers to keep poultry indoors and to keep wild birds out; despite the fact that the Canadian Cooperative Wildlife Health Centre survey of wild birds has found no incidence of HPAI in Canada .
There is growing evidence that HPAI originates in factory farms and is spread not by migrating wild birds so much as by the globalised poultry trade. In low-density backyard flocks, a high pathogenic bird flu virus will simply kill all the birds quickly without infecting other birds. In a factory farm with a high density of birds, however, the virus can spread and multiply rapidly throughout the huge confined flock, and beyond that, via the global trade in live birds, eggs, virus-contaminated feed and manure, across country borders and across continents.
There is indeed strong correlation between exposure to factory farms and incidence of HPAI. Thailand, China and Vietnam, all have a highly developed poultry industry that has expanded dramatically. Production of chicken meat in Southeast Asia - Thailand, Indonesia and Vietnam – jumped from around 300 000 tonnes in 1971 to 2 440 000 tonnes in 2001 . China's production of chicken tripled during the 1990s to over 9 million tonnes a year. Practically all the new poultry production has happened on factory farms outside major cities and is integrated into the transnational production system. Live birds and eggs are exported to countries such as Nigeria (where the first HAI outbreak in Africa occurred), as well as ‘feed' which often includes litter (i.e., manure) in the ingredients. Nigeria has a large and poorly regulated factory poultry sector that is supplied with chicks from factory farms in China 
Manure that may contain live virus is spread on surrounding farmland, or exported as fertilizer and through run-off, may end up in surface waters where wild birds feed and rest. Chicken manure is even found in fish farm feed formulations where it is introduced directly into the aquatic environment.
Wild birds and poultry that have fallen victim to HPAI in Asia, Turkey and Nigeria appear to have been directly exposed to HPAI virus originating in the factory farm system.
In Asia, a flock of wild ducks died from HPAI after having come into contact with the disease at a remote lake where a fish farm used feed pellets made from poultry litter from a factory farm . In Turkey, a massive cull of backyard flocks – and the deaths of three children – took place after a nearby factory farm sold sick and dying birds to local peasants at cut-rate prices.
Recent genetic evidence suggests that domestic ducks may act as a reservoir of H5N1 influenza viruses after the virus has emerged . H5N1 viruses were isolated from apparently healthy domestic ducks in Mainland China from 1999 to 2002, and researchers found that the isolates were becoming progressively more pathogenic for mammals . Twenty-one viruses isolated were confirmed to be H5N1 subtype and antigenically similar to the virus that was the source of the 1997 Hong Kong bird flu haemagglutinin gene. All are highly pathogenic in chickens, most causing 100 percent mortality, although the earliest isolates were less lethal. When tested on mice, however, there was a marked increase in pathogenicity with time. The earliest seven isolates were non-pathogenic or of low pathogenicity, the next seven were more pathogenic and the last four, highly pathogenic. The results suggest that while circulating in domestic ducks, H5N1 viruses gradually acquired the characteristics that make them lethal in mice. One possible explanation is the transmission of duck H5N1 viruses to humans, the selective evolution of the viruses in humans, and their subsequent transmission back to ducks.
The presence of H5N1 viruses lethal to chickens from apparently healthy farmed ducks is another important route for the virus to spread through trade.
Numerous papers, statements and documents issued by the United Nations FAO, WHO, and government agencies have been silent on the role of industrial poultry farming in the bird flu crisis, and indeed, have proposed to compensate them generously for loss profits (see above). Instead, the finger is pointed at backyard farms, calling for tighter controls of their operations and greater “restructuring” of the poultry sector.
The big poultry corporations are even trying to use the bird flu outbreaks to shut down small-scale poultry farming altogether. “We cannot control migratory birds but we can surely work hard to close down as many backyard farms as possible,” declared Margaret Say, Southeast Asian director for the USA Poultry and Egg Export Council.
A team of scientists who analysed the H5N1 epidemic in Thailand 2004 found that the risks for HPAI infection were 5.3, 5.1 1.5, 32.4 and 2.3 times higher, respectively in commercial layers, broilers, ducks, quails and geese than in back yard chickens . This is clear evidence corroborating other findings that corporate factory farms are to blame, and not backyard farms. On that basis, we should be calling for closure of factory farms, not family farms.
Genetic engineering scientists too, are taking this opportunity to promote their wares: transgenic ‘flu-resistant' chickens . “Once we have regulatory approval, we believe it will take between four and five years to breed enough [transgenic] chickens to replace the entire world population,” said Laurence Tiley, Professor of Molecular Virology at Cambridge University in the UK. Genetic engineering is the best way to breach species barriers and to allow viruses to jump species to create pandemics (see “What can you believe about bird flu?” this series).
Article first published 05/05/06
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