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THE SARS EPIDEMIC: THE PATH

THE SARS EPIDEMIC: THE PATH; From China's Provinces, a Crafty Germ Breaks Out

An hour south of Guangzhou, the Dongyuan animal market presents endless opportunities for an emerging germ. In hundreds of cramped stalls that stink of blood and guts, wholesale food vendors tend to veritable zoos that will grace Guangdong Province's tables: snakes, chickens, cats, turtles, badgers, frogs. And, in summer, sometimes rats, too.

They are all stacked in cages one on top of another -- which in turn serve as seats, card tables and dining quarters for the poor migrants who work there. On a recent morning, near stall 17, there were beheaded snakes, disemboweled frogs and feathers flying as a half-alive headless bird was plunked into a basket.

If you were a corona virus, like the one that causes severe acute respiratory syndrome, known as SARS, it would be easy to move from animals to humans in the kitchens and food stalls of Guangdong, a province notorious for exotic cuisine prepared with freshly killed beasts.

Indeed, preliminary studies of early SARS victims here in Guangdong have found that an unusually high percentage were in the catering profession -- a tantalizing clue, perhaps, to how a germ that genetically most resembles chicken and rodent viruses has gained the ability to infect thousands of humans.

One of the earliest cases, last December, was a seller of snakes and birds here who died at Shunde's First People's Hospital of severe pneumonia. His wife and a several members of the hospital staff contracted it as well, setting off an outbreak that now sounds eerily familiar.

''Oh yes, I heard that a guy here died of that pneumonia,'' said Li Songyu, a 40-year-old wearing a neat tan blouse, as she filleted live frogs and dumped them into a basket. ''But it is very safe and sanitary now.''

Around the same time in December, Huang Xinchu, a chef, was admitted to the Heyuan People's Hospital, 100 miles to the north, ultimately infecting eight doctors there. On Jan. 2, another desperately ill chef was hospitalized in the city of Zhongshan, south of Shunde, setting off an outbreak.

But if such early outbreaks present scientific hints about the origin of SARS, they also provide painful political lessons in how a disease that has spread worldwide could have been prevented.

In early January, alarmed health departments in Shunde, Heyuan and Zhongshan all reported the strange pneumonia clusters to Guangdong provincial authorities, who concluded that they were facing a highly infectious pneumonia caused by a previously unknown agent.

It is unclear whether that conclusion was passed on by provincial officials to the Ministry of Health in Beijing, or ever reported to international health agencies that might have conducted an early investigation into the problem. Instead, it would be another two and a half months before the strange pneumonia had a name, coined only after an Italian doctor working in Hanoi, Vietnam, alerted the World Health Organization about a similar new pneumonia he was seeing there.

And it would be three and a half months before China's leaders would admit that their country had an epidemic of SARS. From January through the middle of March, doctors in Asia and Canada were encountering patients carrying a virulent and highly contagious germ, unaware that they were facing potentially lethal infection.

During that period, hundreds of health workers fell ill. During that period, well-meaning doctors were placing SARS patients in ordinary wards -- as they would patients with normal pneumonia -- and those patients were passing the infection on to hundreds of others.

Origins in Food Trade

Scientists have always considered the teeming farms of southern China, where animals and people crowd together as ideal breeding grounds for new human viruses, which can jump between species under such conditions. So it was no surprise in March when the World Health Organization said it believed that SARS originated in Guangdong.

But when a World Health Organization delegation went to look at data on the earliest SARS cases, they found few farmers among the victims. Instead what jumped out was an odd preponderance of food handlers and chefs -- about 5 percent of the first 900 patients, as opposed to less than 1 percent among patients with normal pneumonia.

So far, studies are in their early stages and have yielded few specific conclusions. Even if food handlers turn out to be the conduits through which SARS passed from animals to humans, all evidence points to human-to-human transmission now.

Still, for much of December and January, several small cities around Guangzhou were fighting -- and often winning -- localized battles with the strange pneumonia that would later be named SARS.

In December, the 32-year-old chef from Heyuan was admitted to the Heyuan People's Hospital, having fallen sick with pneumonia on his job near the boom town of Shenzhen. His family had him transferred to Guangzhou when his condition deteriorated despite medication. But when eight doctors and nurses fell ill with a similar untreatable pneumonia in Heyuan just a few days later, hospital officials became alarmed.

On Jan. 1, they told the local health department of the cluster of cases. ''On Jan. 2, we reported a new infectious disease to the provincial health bureau,'' said Dr. Ouyang Songhua, deputy chief of the Heyuan Public Health Department. ''They immediately sent out an expert team to investigate it, deciding it was a pneumonia of previously unknown cause.''

Word of the disease spread among local doctors so that when another chef with pneumonia arrived at Zhongshan Hospital on Jan. 2, short of breath and feverish, doctors isolated him in intensive care.

But not soon enough: 13 medical staff members were infected, who in turn infected 15 others in Zhongshan as well. Outbreaks in Shunde, Heyuan and Zhongshan peaked in January, and by February the virus was poised to move on.

By early February, sick and frightened patients from small cities like these were traveling to more advanced hospitals in the provincial capital of Guangzhou -- and that is when the surge of cases really began.

From Feb. 2 through Feb. 4, a very sick man from Zhongshan made the rounds of emergency rooms in Guangzhou as treatment failed to improve his condition, leaving dozens of health workers infected. At the time, emergency room staff members understood little about the new pneumonia that had been cropping up around the province. At first, they did not isolate the man and were wearing no protective gear.

Unfortunately, the man was what is now known as a ''super-spreader'' -- one of a small group of SARS patients who is highly infectious. Dozens of doctors and nurses fell sick at the Zhongshan No. 2 Hospital, where he was finally admitted.

''He was very sick, but who knew there was something so terrible going around?'' said a nurse named Mo at the Zhongshan No. 2 Hospital, recalling the long, frightening quarantine that followed in February, when nurses and doctors spent long weeks living in their units waiting to see if they will start to cough. In China and in much of Asia, more than 30 percent of SARS victims have been hospital workers.

Hong Kong as a Gateway

On Feb. 21, Dr. Liu Jianlun, a 64-year-old lung specialist from the Zhongshan hospital, attended his nephew's wedding in Hong Kong, even though he was running a fever. With what is now known about the disease, health care providers like Dr. Liu with such extensive exposure to SARS would be quarantined and forbidden to travel. But no such guidelines existed then.

At the Metropole Hotel, where he stayed, he passed SARS on to a number of other guests, including two Canadians, an American businessman en route to Hanoi, a Hong Kong man, and three young women from Singapore. SARS, until then confined to the Chinese mainland, was unleashed on the world.

At the Kwang Wah Hospital in Hong Kong, where Dr. Liu went when his breathing became labored, he advised shocked doctors and nurses of the mystery pneumonia that was ravaging his hometown, insisting that they isolate him behind double panes of glass and don protective gear before his exam. The doctor died several days later; no one at the hospital was infected.

But the grisly story was not shared with other doctors in Hong Kong or the rest of the world. And, with the new corona virus silently breeding in their bodies, the nine guests at the three-star Metropole Hotel dispersed on airplanes like bees carrying a deadly pollen, seeding SARS locally and to far corners of the world.

The woman from Toronto, Kwan Sui-chu, died in a Toronto hospital on March 5, but not before infecting her son and at least five health workers. Canada now has identified at least 140 SARS cases, 15 fatal.

Johnny Chen, the American businessman, fell ill at a hospital in Hanoi in late February, where he ultimately infected 20 health workers, including Dr. Carlo Urbani, an Italian medical researcher who alerted the W.H.O. about a new type of pneumonia and who also eventually died of the disease. The Hong Kong man was admitted to a general ward at the Prince of Wales Hospital, setting off a huge outbreak.

The three Singapore women fell ill after going home in late February and were admitted to three hospitals from March 1 to March 3. While two of the women infected no one else, the third, Esther Mok, another super-spreader, set off a chain of infection based at the Tan Tock Seng Hospital, from which over 90 people fell ill, accounting for more than half Singapore's cases. Ms. Mok has recovered, but many members of her family became ill, including her mother and father, who both died.

On March 14, the World Health Organization formally issued its worldwide alert about the new disease, which it called SARS.

A Focus on Prevention

Since then, countries visited by this new plague have taken increasingly severe steps in order to control further spread of a disease that has eluded many conventional infection barriers. Because the disease remains difficult to treat and has a death rate of 5 to 10 percent, by far the most effective way to deal with it is to stop its spread.

''On an individual level it is relatively low risk, but the proportion of people who have a severe course appears to be quite high,'' said Rob Breiman, a respiratory expert who has worked for the World Health Organization on the outbreak. ''Until we know more about this disease, protecting against exposure is extremely important.''

In Canada, for example, even healthy travelers arriving from affected areas are advised to go into a 10-day voluntary quarantine, where they are advised to stay at home, take their temperature frequently and sleep in a separate room from other family members. Ontario alone now has 7,000 people under various types of quarantine.

But some people have resented the restrictions for what most often proves to be nothing more than a fever from a common cold. On Easter Sunday, one health care worker who had been exposed refused to stay at home, attending church services and a funeral in Toronto. Health officials are now considering a court order to keep him isolated.

Companies and governments in the West are drastically curtailing travel to SARS-affected regions. Some are also are requiring employees to stay at home for 14 days after visiting SARS-infected areas.

''I'm not too worried about the disease,'' said Jane Cowells, a resident of New Zealand, as she arrived this week, unmasked, at Beijing Capital Airport. ''But the whole thing is a headache, since when I go home I can't go back to work for 10 days.''

In Vietnam, where the epidemic is now under control, officials said they were considering sealing off the entire 800-mile border with China to prevent sick tourists from reintroducing the germ.

In many Asian countries, airports have come to resemble bioterrorism labs, as nurses in protective gear assess arriving passengers for signs of disease. No place is more vigilant than Singapore.

Singapore's Drastic Steps

''Welcome to Singapore! Are you feeling well today?'' chimes a chorus of nurses, their faces covered by masks, their eyes by goggles, their bodies by yellow hospital gowns. Passengers coming from other countries with SARS are guided to pass through a high-tech thermal scanner that picks up temperatures over 100. Masked soldiers are there to escort away those with fever.

Those who pass muster are given a card warning that they might have been exposed to a deadly disease. Those who are feverish are whisked, without apology, into a 10-day quarantine, and Singapore means business. Video cameras will be installed in the home by a security firm, to make sure patients do not stray. Those few who do are tagged with an electronic wristband that records their movements.

But even in a small country, placing thousands on quarantine has been a strain. Last Monday, after a case of SARS was discovered in a vendor at Singapore's largest vegetable market, the Ministry of Health ordered all 2,400 food sellers to report for quarantine, up from a total of 467 quarantined before. Since 80 percent of the country's vegetables pass through the Pasir Panjang Market, restaurants were bracing for a shortage of greens.

''We do what we have to,'' said Dr. Balaji Sadasivan, a neurosurgeon who is Singapore's minister of state for health. ''I don't think we've seen anything like this before and it is a global problem. For now this is a battle that is being fought with the thermometer and quarantine.''

Because of elaborate contact tracing, the Singapore outbreak is by far the best defined in the world. All but 4 of the 188 victims were infected in the hospital or by a family member at home. The four exceptions are a child who got the disease from a classmate with an infected parent, a flight attendant who served an infected doctor from Singapore on a flight in Europe, a cab driver and a vegetable salesman.

Dr. Sadasivan is unapologetic as he describes the draconian measures his department has adopted to halt the spread of the germ.

When the three young women from the fateful Hong Kong hotel brought SARS to three different hospitals in Singapore in early March, Singapore doctors were unaware of the odd pneumonia that was hospitalizing dozens of patients each day in Guangdong and so admitted them to ordinary wards. If the Chinese had publicized their severe pneumonia in Guangdong, or if the Hong Kong doctors had more aggressively reported the information about Dr. Liu, their response almost certainly would have been different.

Two of the women did not pass on the germ, but one infected more than 20 people, both patients and hospital workers. One of the nurses she infected also proved to be a super-spreader, passing SARS to 26 others. One of the 26 was a patient in the cardiac intensive care unit whose SARS was not recognized because of many other medical problems.

Within a month, 90 people at the Tan Tock Seng Hospital had the disease. The Health Ministry dug up an old law that allowed them to impose mandatory quarantines, with fines of 5,000 Singapore dollars for those who disobey. They also essentially closed the 1,000-bed hospital to other patients -- hoping to contain the virus within its walls.

But it escaped all the same. Some patients who had been at Tan Tock Seng in March contracted the disease and later went to other hospitals when they developed coughs -- setting off secondary outbreaks. One went to Singapore General for an endoscopy and was screened for SARS, but did not run the telltale fever because he was on steroids that suppress the body's response. Ninety people at the hospital were infected.

After this resurgence, the Health Department instituted a policy that every patient at every hospital be considered a potential SARS patient. Nurses are always masked when seeing patients, who are allowed only one visitor a day. Confirmed SARS patients are allowed no visitors at all, though they can talk to friends and family on their cellphones. Nurses may not work on more than one unit and patients may not transfer from hospital to hospital.

''We used to have a health care system organized for efficiency,'' said Dr. Sadasivan. ''But now our hospitals are organized for SARS prevention.''

Outside of the hospitals, the ministry closed all schools for two weeks to halt potential transmission of the virus. All cab drivers now take their temperatures twice a day. Temperature checks and health questionnaires are standard for those entering buildings.

At Tan Tock Seng Hospital last Monday, an ambulance arrived carrying a vegetable seller who came under the market quarantine. Although he felt well, the man said he had a fever, and so the driver told him he might have to remain in the hospital. Approaching a cordoned-off screening area, he was resigned, saying, ''I don't think I could have the disease, but I know I have to do it.''

China's Slow Response

But Singapore's aggressive, open confrontation with a viral enemy is a lesson that some other countries have been slow to learn, especially China, the world's most populous country, where SARS emerged almost half a year ago.

Although doctors in Guangzhou were well aware of the problem as early as January, information about an epidemic was suppressed for months, and only started dribbling out at the beginning of April, under intense international pressure.

Only in the last week have numbers begun to emerge elsewhere in China, and the task is still not complete. In Beijing, they already paint an alarming portrait of an epidemic that is likely to dwarf that in either Guangdong or Hong Kong.

At a news conference on April 10, He Xiong, the deputy director of the Beijing Centers for Disease Control, was still delivering a calm message, endorsing numbers that the government released at the time: that in Beijing there were only 27 SARS cases, so people should not worry.

''Of course they can travel, we think it's very safe,'' he said, referring to an approaching national vacation when tens of millions of Chinese would normally be expected to travel.

But that misinformation only fueled the spread of SARS, as people -- with fevers and coughs -- continued to go to school and work, passing the disease on to others. As the number of cases increased well into the hundreds, the illusion proved hard to maintain in a city with a world-class gossip network that spread rumors of overflowing SARS wards.

By last weekend, everyone was skeptical, as a smattering of schools and hospitals mysteriously closed. One People's Armed Police hospital in Beijing was closed after five patients were infected. The Zhongguancun No. 1 Primary School closed when a relative of a student got SARS. The Beijing University Institute of Economics put several dozen people on quarantine after a secretary's mother got pneumonia.

More than a dozen of Beijing's universities had reported suspected cases. At the Economics and Finance University alone, more than a dozen students and faculty members were listed as suspected SARS cases, resulting in the suspension of classes from April 17.

That day, the main gate of the Northern Construction University was a panic scene, as masked students made arrangements to flee to their hometowns in the wake of suspected SARS cases on campus. ''I want to get out of here as soon as possible,'' said one alarmed student, making calls on her cellphone to borrow money for the trip home.

Then, last Sunday, the Chinese government fired both the health minister and the mayor of Beijing, and started releasing alarming data that confirmed these fears. As of Friday, there were close to 900 confirmed cases in Beijing, a number that is certain to strain the resources of city hospitals and will make SARS far difficult to control.

But can the lessons of prevention learned in a tiny, authoritarian country like Singapore be applied elsewhere, particularly in a vast, chaotic place like China, with far more cases and a highly mobile population?

In Singapore, with its aggressive system of identifying and isolating SARS patients, no health care worker has been infected for over three weeks. But in Hong Kong, 2 to 10 doctors and nurses are falling ill each day, in part, health officials there say, because doctors are still not identifying them as SARS victims early enough and are admitting them to ordinary wards.

''There is so much we don't know about this virus -- how long it will be with us? Will it mutate and become more easily transmitted?'' Dr. Breiman said. ''But it is a little frightening that something which started in one location could spread so quickly around the world.''

Rise of a Virus

The first article in this series examined the economic impact of SARS. Later articles will examine the response of health officials and the search for the virus. The articles are online at nytimes.com/sars.