Bird ‘flu follows trade, not migration routes
A comprehensive critical review of recent scientific literature on the spread of Highly Pathogenic Avian Influenza H5N, published in the British Ornithologists Union journal Ibis, concludes that poultry trade, rather than bird migration, is the main mechanism of global dispersal of the virus.
The review finds that migratory birds have been widely and repeatedly blamed for outbreaks that have subsequently been found to originate in the movement of live poultry and products such as poultry meat. The authors, French ecologists Michel Gauthier-Clerc, Camille Lebarbenchon and Frederic Thomas of Station Biologique de la Tour du Valat (a research centre for the conservation of Mediterranean wetlands) and GEMI (Génétique et Evolution des Maladies Infectieuses –the Laboratory of Genetics and Evolution of Infectious Diseases), warn that a misdirected emphasis on contacts between wild birds and outdoor poultry may lead to a reversion to intensive indoor poultry rearing, which actually increases the risk of outbreaks.
Wild birds constitute a permanent source of gene fragments of low pathogenic avian influenza, which are sometimes transmitted to domestic birds. But Gauthier-Clerc et al. say that how the virus subtypes subsequently evolve depends on poultry rearing practices.
“When bird densities are low, a very virulent subtype leading to high host mortality may disappear because of the impossibility of transmitting quickly to healthy birds before the death of sick ones. In Asia, densities of domestic birds are especially high. These ecological conditions favour the preservation and the fast transmission of very virulent strains.”
The progenitor HPAI H5N1 was discovered in 1996 in domestic geese in the province of Guangdong, southern China, and would have been dispersed through movements of geese and other poultry, including domestic ducks capable of carrying it asymptomatically. “This would have allowed the virus to extend, thanks to trade, over a vast zone without being discovered. The major epizootic” (an epidemic in non-human species) “started between December 2003 and January 2004 in chickens, which are more susceptible than domestic ducks, with episodes being reported almost simultaneously in eight countries in southeast Asia… The geographical extension and the genetic evolution of the virus since 1996 had probably taken place without any link with wild birds.”
At the beginning of 2005, the virus was still confined to southeast Asia. Cases were reported from Indonesia to China, including Cambodia, Thailand and Vietnam. The only wild birds found infected were victims of the virus circulating in domestic birds, such as sparrows, magpies, herons and birds of prey which scavenge around poultry farms. “Migratory birds do not recognize borders, yet the virus remained restricted to China and southeast Asia for some years,” the authors point out.
Then in spring 2005, wild birds were found dead from the virus at Lake Quinghaihu in the centre of China. The dead birds included Bar-headed Geese Anser indicus, which winter in India, Bangladesh, Nepal and Pakistan from October, and depart northwards at the end of March. “If Bar-headed Geese brought the virus to Lake Quinghaihu during their spring migration, it is necessary to postulate that they contracted the virus during 2004 in China, and would thus have been likely to contaminate India during the autumn or winter of 2004/05. It thus seems far more likely that these migratory birds were the victims of the H5N1 by arriving in spring 2005 on breeding areas which were already infected by the virus.”
A year later, in May 2006, it was revealed that Bar-headed Geese were artificially reared near the lake, raising the possibility that farmed birds were the source of the outbreak.
If migratory wildfowl were a key agent of the dispersal of H5N1, the spring migrations in 2004 and 2005 should have carried it to Siberia, where it would have infected breeding birds that winter in India, Pakistan, Bangladesh, the Middle East, east Africa, Australia and New Zealand. “A new wave of contamination, on a wide front from Europe to Central Asia, would then have begun in spring 2006.”
"...strong veterinary scrutiny and control of trade is more likely to be a successful strategy.” —Gauthier-Clerc et al.
Instead the virus began its westward expansion across east Asia from Novosibirsk in July 2005, a month when waterfowl are moulting and flightless. The spread followed major trading routes such as the trans-Siberian railway, with the largest and most widespread outbreaks in countries with unreliable border controls and poorly developed biosecurity and veterinary services.
By the beginning of January 2006, no case had been reported in the Indian subcontinent, the Middle East, Africa, America or Australia, even though the southward migration had ended and many species were preparing to go north to their breeding grounds.
In early 2006, a series of outbreaks in wild birds made its way westwards and northwards across Europe. The birds were mostly waterfowl, particularly swans, which had been pushed westwards by a spell of extreme cold weather in Eastern Europe, and the spread did not correspond to the usual routes or timing of migration. “It is remarkable that outbreaks remained localized and did not extend like an epizootic around each initial outbreak,” the authors observe.
Migratory birds such as ducks and waders travel several hundred kilometres in a single day, so if migrating birds were the main vectors, the virus should also spread by large jumps of hundreds or thousands of kilometres. “The observed expansion has rather been by a progressive expansion from isolated outbreaks, the geographical pattern of which corresponds well with major routes and patterns of human commerce.”
And if migratory birds were a main agent of dispersal, then after July 2005 we might have expected massive die-offs of wild birds in the breeding areas and along migration routes, since bird populations would have been encountering the virus for the first time. “However, only sporadic cases were observed. The cases in Western Europe after the cold spell on the Black Sea showed that the virus can spread through infected wild birds travelling short distances, but no evidence for long-distance transmission during seasonal migration has yet been found.”
By May 2006, an international conference in Rome had recognized that the virus was mainly spread through the poultry trade, both legal and illegal. But OIE and FAO media releases (and most recently the initial response of UK government agencies to the outbreak at a Bernard Matthews factory farm in Suffolk, England, linked by road transport to a subsidiary operation close to an outbreak in Hungary), have continued to focus on the role of migratory birds.
“Given that a key part of the remit of the FAO is to develop international agricultural trade, reluctance to accept that this trade is the main agent of global dispersal of HPAI H5N1 is perhaps unsurprising,” Gauthier-Clerc et al. comment.
Paradoxically, they conclude, “fear of transmission by wild birds could lead to a reversion to battery farming , which increases risk of outbreaks, rather than maintaining the current trend to better animal welfare resulting from free-range agriculture. All the evidence suggests that maintaining these trends whilst controlling disease through strong veterinary scrutiny and control of trade is more likely to be a successful strategy.”
 Recent expansion of highly pathogenic avian influenza H5N1: a critical review M. GAUTHIER-CLERC, C. LEBARBENCHON & F. THOMAS. Ibis (2007) [citation to appear]
 A recent report from agricultural biodiversity NGO Grain finds that in the last year, a combination of FAO guidance and moves by southeast Asian governments to protect their poultry exports has led to exactly this: the suppression of small-scale outdoor poultry rearing, which has hosted few documented outbreaks, in favour of industrial poultry farming.
To see the report click here