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Avian flu and the New World

Nature volume 441, pages 137139 (11 May 2006) | Download Citation


The H5N1 avian influenza virus has not yet reached North and South America. What will happen when it does? Declan Butler and Jacqueline Ruttimann investigate.


The H5N1 virus once seemed a problem that was lurking in someone else's backyard farm. But since last summer, the lethal avian influenza virus has surged out of southeast Asia into Europe, the Middle East and Africa. Fifty-one countries — 36 this year alone — have now experienced outbreaks.

The New World is as yet untouched, but many experts consider it inevitable that the virus will reach North and South America. This area is home to the world's largest poultry exporters, Brazil and the United States. And although government and industry officials say they are well prepared for the arrival of H5N1, others argue that they have yet to take on board the full extent of the challenge.

“When H5N1 arrives,” says Mark Cackler, the World Bank's agriculture manager for Latin America and the Caribbean, “it will concentrate minds wonderfully.”

Trade, smuggling and migratory birds are all potential routes for H5N1 to reach the Americas (see page 138). How it arrives is ultimately less important than stopping a subsequent spread of the disease, says Juan Lubroth of the UN Food and Agriculture Organization. And here there is no debate as to what causes spread, he adds: it's not migratory birds, but “human actions, trade and husbandry practices”.

Box 1: H5N1: Into the Americas


Every day, millions of live poultry are moved around the world by ground, air and sea transport, which potentially could carry H5N1 to fresh areas.

Replenishing flocks at huge industrial farms is now a global business: commercial hatcheries export billions of hatching eggs and one-day-old chicks. Egypt, for instance, exported some 180 million chicks annually before the H5N1 virus was detected there and exports were halted. Many experts see trade as the major cause of the spread of avian flu, through infected bird droppings on shells, crates and other surfaces.

In the United States, imported live birds must undergo a 30-day quarantine and tests for avian flu, says Madelaine Fletcher, a spokeswoman for the US Department of Agriculture. Most day-old chicks reaching the country are from Canada or the United Kingdom, and their crates are either disinfected or destroyed, she says.

Hon Ip, a virologist at the US National Wildlife Health Center in Madison, Wisconsin, says it is hard to assess how well quarantine works, as the United States has so far avoided an outbreak of H5N1. But an outbreak of contagious Newcastle disease in California in 2002 shows that quarantine is not always watertight, he says.

A country is generally banned from exporting poultry when it officially reports an outbreak of H5N1 in commercial flocks. But H5N1 can be present before a report is made. Moreover, although H5N1 has occurred in 13 countries in the European Union (EU), the United States bans imports only from regions involved, not from entire countries.

Most US imports from Europe are pet birds from Belgium and poultry products from France, but the country also imports bird skins and feathers from 16 EU nations. In 2005, the United States imported more than 16.8 million day-old chicks and other live poultry as well as 16.8 million hatching eggs.


On 5 September 2005, customs inspectors at the US Department of Agriculture (USDA) found an illegal shipment of 98,400 chicken eggs at a port in California. During October and November, they intercepted nearly 75 tonnes of poultry smuggled in from Asia.

Last month, a man from Nigeria — a country with H5N1 — was stopped at Miami airport after dogs detected dead birds, ostensibly brought in for a religious rite, in his luggage.

How much smuggling goes undetected is anyone's guess, but the illegal trade in birds and poultry products is thought to be third only to narcotics and arms in value. With trade bans imposed on countries with H5N1, the risk of smuggling has gone up, says Ip. “It has become more likely that illegally imported birds could come from an affected country,” he says.

Inspections of markets and restaurants in major US cities regularly turn up illegal imports of poultry from Asia and elsewhere, admits one USDA official.

On the front line, 122 inspectors from the US Fish and Wildlife Service work across 35 ports looking for another target: exotic birds. The risk is real. In October 2004, a Thai man was caught at a Belgian airport as he tried to smuggle in two eagles that were later found to have H5N1.

Most smuggled birds are parrots, macaws and their relatives, or songbirds, says Ip. They come mainly from H5N1-free Australia, South America and Mexico. But traffic is brought in from many other countries. The black-capped lory (Lorius lory) from Indonesia, an H5N1-infected country, is a highly prized bird that is frequently targeted by smugglers, he notes.

“An infected bird in one part of the world can be in North America within 24 hours, whether that bird is fit to fly or not,” says Ip.


Migratory birds could bring H5N1 to the Americas as early as this month — to Alaska, a short hop across the Bering Strait from Russia. Some 6.6 million birds will arrive in the state by the end of May, travelling up a flyway from Siberia, China and southeast Asia. The fear is that these birds could infect American migrants, which would then carry the disease back down the length of the Americas in the autumn.

To prepare for this, US agencies are already catching birds for testing — the start of a procedure that will examine 75,000-100,000 swabs from the birds for avian flu. “It's the largest and most complex migratory bird capture and sampling programme in the history of Alaska,” says Dirk Derksen of the Alaska Science Center in Anchorage, one of the project's main coordinators. Birds will also be monitored along the major flyways running down through North America, particularly along the West Coast.

H5N1 could also arrive from the east: birds from West Africa and Europe fly over Greenland into northern Canada. But the smaller number of birds and species, and the longer flight distances, make this a less likely route for H5N1, says Derksen, and so sampling is not taking place there.

Biologists have identified the relative risk of each species of Alaskan migrant. Top of the list is the northern pintail (Anas acuta), which breeds widely across North America and Eurasia. It is among the most highly infected of waterbirds, with one in ten birds carrying some flu virus (B. Olsen et al. Science 312, 384–388; 2006).

But whether migratory birds can carry H5N1 over long distances remains controversial. The first outbreak of H5N1 in Africa — in Nigeria — was widely attributed to migratory birds. But many now see the imports of day-old chicks as a more plausible cause.


Experience in Asia and Europe provides best practices on controlling avian flu, says Jim Butler, director-general of the Inter-American Institute for Cooperation on Agriculture in San Jose, Costa Rica. “We don't need to reinvent everything.” The task for the Americas, he says, is more about “building consciousness” of the risks and existing best practices.

Such practices include setting up surveillance and diagnostic capacities that can quickly detect any initial outbreak. But despite all best efforts, some virus will always go undetected, so countries must also have policies in place to make their farming systems more resilient.

Such policies can be as simple as requiring the poultry industry to disinfect all material and people moving in and out of farms. Another is to reorganize national poultry industries into regional ‘cells’ that operate independently of one another, so that if one goes down with H5N1, the others do not.

France prepared by using both approaches, and so far the H5N1 found there has been stopped in its tracks. Turkey did neither well, and has suffered persistent outbreaks. The well-developed animal health services in the United States and Canada have implemented similar measures to those in France, and are widely expected to quickly contain any outbreak of H5N1.

Unlike regions of southeast Asia and Africa, where poultry live outdoors and mingle freely with each other and with wild birds, US flocks are highly concentrated in industrial farms, where birds are raised indoors, isolated from external contaminants. One potential weakness is the popular live markets in California and the northeastern states. In the northeast, these markets have sustained an avian flu virus of low pathogenicity, H7N2, since 1994. In the past, as many as 60% of birds sampled have carried flu viruses, although control measures have reduced the levels.

Such live markets “continue to be a major source of avian influenza viruses and a risk for introduction to commercial poultry operations”. This is what David Swayne and David Suarez of the US agriculture department's main poultry research laboratory in Athens, Georgia, told an influential 2004 workshop on pandemic planning that was organized by the US National Academies.

South America is also preparing well, experts say, as it has decades of experience of handling other highly contagious diseases, such as foot-and-mouth disease. Lubroth gives the continent good marks for “high awareness favouring quick detection and response”.

Brazil's poultry industry is both larger and more complex than that in the United States. Backyard farms are common in the poor northeastern part of the country, and smallholdings are scattered throughout urban areas and along the Amazon. But its core production remains in large commercial farms, which are well aware of the economic risks of H5N1, says Lubroth. “If H5N1 entered,” he predicts, “they would stamp it out quickly to preserve the main industry.”

That view is overly optimistic, argues Cackler, who sits on the avian-flu taskforce for the World Bank. Many South American countries, he says, have only recently woken up to H5N1 as something they might need to worry about. He recalls speaking to the agriculture minister of “one to-be-unnamed country” last November, who “just didn't get it; H5N1 was nothing to worry about”. Cackler met him again in January, after H5N1 had ripped across Europe. “This time, the guy got it.”

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