The Fatal Strain

after the scientists, journalists, and other whistle-blowers who tried to reveal the threat.

The virus exploited this opportunity to put down roots. It became entrenched in Asia’s poultry, thus posing a long-term menace to humanity. While some Asian governments eventually intensified their efforts to contain the disease, total eradication was now a distant prospect at best. Not a single one of these frontline countries—China, Indonesia, Thailand, and Vietnam—had adopted the most powerful disease-fighting weapons: truth and transparency.

Later, when I arrived on my first trip to Geneva, a senior WHO official gave me a piece of advice. He counseled me that influenza is all about politics. And those antiquated politics have proven every bit as intractable as the virus itself.

This tale of death and deception begins in the coastal Chinese province of Guangdong, close to where the first human cases were confirmed in Hong Kong back in 1997. The H5N1 flu strain, which went on to ravage farms on at least three continents, infect hundreds of people, and pose the most serious threat of pandemic in a generation, was first isolated in a sample taken from a sick goose during a Guangdong outbreak in the summer and early fall of 1996. That was more than seven years before China first acknowledged any infection in its flocks. By the time Chinese officials went public in early 2004 and stepped up efforts to contain it, the virus had already seeded outbreaks in the country’s neighbors.

Molecular biologists were later able to identify the Guangdong pathogen as the common ancestor of all subsequent H5N1 viruses by analyzing the eight segments of RNA that all flu viruses contain. Each of the segments in a single virus has its own signature, a specific sequence of basic building blocks called nucleotides that make up the RNA. As viruses evolve, these segments mutate. They can even be completely replaced as the promiscuous flu strains swap genetic material. In the lab, genetic genealogists determine the pedigree of viruses by looking for similarities in their RNA. Isolates that share the same pattern are often related and descended from the same specific virus.

A combined team of researchers from the U.S. CDC and China’s official National Influenza Center reported in 1999 that the virus that had killed people in Hong Kong two years earlier was related to the Guangdong goose isolate. The specific H5N1 subtype was identified at the Chinese influenza center. At least three other academic papers written in Chinese by Chinese researchers also reported in 1998 and 1999 that H5N1 had been isolated in Guangdong in 1996, disclosing in one instance that up to 40 percent of the geese on a farm stricken by the outbreak had died. These findings had been reported by Chinese government researchers in government publications. Yet for years, senior Chinese officials continued to deny publicly that Guangdong had been struck by bird flu in 1996 or that it had spawned the wider epidemic.

Over the coming years, Chinese and foreign scientists continued to report periodic outbreaks in southern China, including a large poultry die-off in Guangdong just months before the Hong Kong cases in 1997. A series of research articles published between 2000 and 2002 further documented that H5N1 viruses were continuing to circulate in southern China, for instance in geese and ducks exported from Guangdong to Hong Kong. The virus was also isolated in a specimen taken from frozen duck meat exported from Shanghai to South Korea in 2001. A team composed primarily of mainland Chinese researchers later reported that tests on ducks from southern China between 1999 and 2002 had repeatedly come back positive.

The most damning evidence came in a study published in 2006 by scientists from China, Indonesia, Malaysia, Vietnam, and the United States, which identified China as the wellspring of the international epidemic. “We have shown that H5N1 virus has persisted in its birthplace, southern China, for almost 10 years and has been repeatedly introduced into neighboring (e.g., Vietnam) and distant (e.g., Indonesia) regions, establishing ‘colonies’ of H5N1 virus throughout Asia that directly exacerbate the pandemic threat,” the researchers wrote. They concluded that addressing the “pandemic threat requires that the source of the virus in southern China be contained.”

Chinese initiatives to tackle the disease may have only fueled its spread and honed its lethality. Just days after the government first disclosed in January 2004 that it had detected the disease, New Scientist reported that Chinese poultry producers had been vaccinating their flocks against it for years. But the vaccination campaign may have been mishandled, obscuring the usual symptoms without eradicating the virus itself. “The intensive vaccination schemes in south China may have allowed the virus to spread widely without being spotted,” the magazine alleged.

Animal-health experts later told me about an even riskier strategy that China had adopted to suppress the spreading virus years before officials publicly disclosed its presence. Acting with the approval and encouragement of the government, Chinese farmers had tried to douse major outbreaks among chickens with amantadine, an antiviral drug meant for humans. As a result, international researchers concluded that this drug might no longer protect people in case of a flu pandemic. The H5N1 subtype circulating in Vietnam and Thailand had become resistant to the drug, which is one of two types of medication for treating human influenza, though another viral subtype found elsewhere was still sensitive to it.

China’s use of amantadine violated international livestock regulations. It had long been barred in the United States and many other countries. But veterinarians and executives at Chinese pharmaceutical companies said farmers had been using the drug to contain the virus since the late 1990s. “Amantadine is widely used in the entire country,” confirmed Zhang Libin, head of the veterinary medicine division of Northeast General Pharmaceutical Factory in Shenyang. He added, “Many pharmaceutical factories around China produce amantadine, and farmers can buy it easily in veterinary medicine stores.” Zhang and other animal health experts said the drug was used by small private farms and larger commercial ones. China’s agriculture ministry had approved the production and sale of the drug, and local government veterinary stations instructed Chinese farmers on how to use it by adding it to the chickens’ drinking water—and at times even supplied it.

One veterinarian steered me toward a popular Chinese handbook, titled Medicine Pamphlet for Animals and Poultry, which provided farmers and livestock officials with specific prescriptions for amantadine use to treat chickens and ferrets with respiratory viruses. The manual, written by a professor at the People’s Liberation Army Agriculture and Husbandry University and issued by a military-owned publishing company, prescribed 0.025 grams of amantadine for each kilogram of chicken body weight. Farmers also used the drug to prevent healthy chickens from catching bird flu, giving it to their poultry at least once a month and often mixing it with Chinese herbs, vitamins, and other medicine.

After China’s misuse of amantadine was first reported in the Washington Post in June 2005, the Chinese government angrily denied the account. “This is groundless and isn’t in accordance with the truth,” the agriculture ministry said in a statement. “The Chinese government has never permitted farmers to use amantadine to treat bird flu or other virus-related disease.” But the government-owned China Daily acknowledged in a front-page article that some farmers had in fact used the drug in poultry. The newspaper said the agriculture ministry planned to send inspection teams across the country to halt the practice. I was never able to determine whether it was indeed brought to an end nor the extent to which it had been part of a concerted Chinese effort to conceal the outbreaks. In private, officials at WHO had also been asking the Chinese government about the improper use of antiviral drugs in livestock. They, too, were never given a satisfactory answer.

From China, the virus had ventured south. It stole across the border to Vietnam and began infecting poultry there no later than 2001, more than two years before the children in Hanoi’s National Pediatric Hospital started succumbing to the mysterious outbreak of respiratory disease in late 2003.

Vietnamese scientists knew the truth about the early poultry infections. These researchers had participated in a study that the CDC’s intrepid investigator Tim Uyeki had helped put together sampling various species of poultry in the live bird markets of Hanoi. Uyeki had suspected that the novel flu strain was still circulating in China even after Hong Kong’s mass cull of 1997 had expunged the virus from that city. But mainland China was, for all practical purposes, off-limits for the kind of scientific study he envisioned. So he tried the next-best thing: peering in from the distance by sampling birds south of the Vietnamese border. In the fall of 2001, the researchers discovered two geese with H5N1 in a pair of Hanoi markets. This strain was closely related to the isolate from the Guangdong goose. Lab tests revealed that this pathogen was devastating for chickens, killing every single bird inoculated with the agent within forty-eight hours.

Sometime in 2002 or the first half of 2003, a new variant of the H5N1 virus again slipped across the border from China. This one was later traced to China’s Yunnan province, just north of Vietnam. It was even more virulent.