Spillover: Animal Infections and the Next Human Pandemic

Quammen opens his discussion of SARS with a brief interlude of “personification”: He describes how the virus “got on a plane” from Hong Kong to Toronto in February 2003, and then another from Toronto to the Philippines (167). It was particularly hazardous to medical professionals—during its spread to Hanoi it killed a WHO communicable disease specialist who treated a patient there. Once the disease spread to 70 hospitals in Beijing, the WHO issued a global alert about the new disease, originally characterized as “severe, acute respiratory syndrome of unknown origin” (168). The new disease was the subject of so much alarm because of its “infectiousness” and its “lethality”—it was much more dangerous than typical pneumonia (169).

Hong Kong was not the origin of SARS: instead, the virus originated in a neighboring province, Guangdong, the southernmost part of mainland China. In November 2002, a man in Guangdong province became ill with mysterious respiratory symptoms. No samples were taken, but the nature of his illness and the fact that he infected his family led to the assumption that this “local government official” had SARS (170). His more important trait may have been that he prepared a chicken for a family meal, as a restaurant chef in the city of Shenzhen later became ill. An outbreak in Zhongshan in January also involved a restaurant chef, and close to half of those infected were healthcare workers.

By this time, the provincial government recognized an emerging problem and sent a team of “experts”—which Quammen puts in quotes since at this time the disease was not truly understood by anyone. Their recommendations for stopping the spread of this “atypical pneumonia” were too late, as a “seafood wholesaler who had recently visited Zhongshan checked into a Guangzhou hospital and triggered the chain of infections that would circle the world” (172).

This man, Zhuo Zuofeng, was the first “‘superspreader’ of the SARS epidemic. A superspreader is a patient who, for one reason or another, directly infects far more people than does the typical infected patient” (172). The existence of these individuals has profound implications for public health, as Quammen points out:

If superspreaders exist and can be identified during a disease outbreak, then control measures should be targeted at isolating those individuals, rather than applied more broadly and diffusely across an entire population. Conversely, if you quarantine forty-nine infectious patients but miss one, and that one is a superspreader, your control efforts have failed and you face an epidemic (172).

This containment was not possible during the SARS epidemic, and Zhuo Zuofeng infected at least 30 health care workers during the first of his two hospitalizations. At another hospital he infected 51 people, becoming known as “the Poison King” (174). One of the doctors from Zhou’s first hospital carried SARS to Hong Kong, where he attended a wedding and infected many hotel guests at the Metropole Hotel. He became “the second known superspreader” (174). He died on March 4, after infecting a grandmother who flew home to Canada before her symptoms developed.

Another person infected at the Metropole, Esther Mok, returned home to Singapore and visited Tan Tock Seng hospital. Quammen later met with one of the doctors who treated her, an infectious disease specialist named Brenda Ang. Esther Mok became another superspreader. As more cases connected to Mok came in, the WHO notified the Singapore Ministry of Health. The outbreak spread enough that the hospital soon developed a shortage of the N95 masks they wore when treating patients.

Another superspreader event occurred when a cardiology patient was “infected there by a health-care worker, who had in turn been infected by Esther Mok” (180). Before she showed symptoms, that woman was intubated and infected more hospital staff. A resident and his mother died, and more than 20 others were infected. One of the doctors who had treated Esther Mok became ill while traveling home from New York and was quarantined in Frankfurt, Germany. All patients there survived.

Singapore was fairly successful at containing the outbreak, in part because its political culture allowed for measures like fining anyone who violated quarantine rules. Schools and public markets closed, and even cab drivers were closely monitored for signs of illness. Ultimately, Tan Tock Seng hospital saw more than 200 cases. Esther Mok survived, though many of her friends and family did not.

Beyond treating the sick and containing the outbreak, infectious disease specialists also worked in laboratories to identify what exactly SARS was and how it was transmitted. Researchers were not certain whether they were looking for an entirely new pathogen or something related to known diseases. This meant that they had to resort to a less sophisticated technique: namely, “growing the microbe in a cell culture and then looking at it through a microscope” (184). This task fell to a Hong Kong-based influenza specialist named Malik Peiris.

Subsequent cultures showed that SARS “belonged to a group known as the coronaviruses” (185). Peiris and his team conclusively proved that the virus was the same one causing the outbreaks by testing it against the blood of patients. When their antibodies “reacted strongly,” they published their results. The research also strongly suggested that animals were the source of the infection. Unearthing its source fell to a Hong Kong microbiologist named Guan Yi, who investigated the large outdoor markets of southern China. His sampling adventures eventually led scientists and health officials “to cast their suspicious attentions upon a mammal called the civet cat” (186).

The civet cat is one of many wild animals eaten in Chinese cuisine. In Southern China, eating what is known as “wild flavor” is a sign of social status. Restaurants specializing in it had opened in Guangzhou in the thousands. Their supplies came from large outdoor markets known as “wet markets” (188). In response to the trend, more wild animals were being imported or raised in captivity. The markets were often crowded, and it was relatively easy for animals to become sick. Of course, any ill animals were also in close proximity to humans.

Guan Yi visited one of these markets to collect his samples and found six civets carrying SARS. These results were immediately published in newspapers, although people were also aware that person-to-person transmission and its prevention via masks was critical. This discovery was likely reported to newspapers rather than scientific journals to ensure that it would make news before any other scientific teams could publish.

Guan Yi noted that civets might function as an “amplifier,” as horses do with Hendra virus, and focused more intensely on the role of the wet markets as sites of infection. Though laypeople celebrated the end of the initial outbreak, scientists were more cautious, knowing that the reservoir was likely still present and could spread the virus again. In December 2003, more cases were discovered, and the government responded by killing more than a thousand captive civets. Science would later prove that this effort had been unnecessary, because the story of the SARS reservoir was “more complicated.”

The team from Hong Kong university turned to an underdeveloped region of Hong Kong called the New Territories to continue their search, trapping many wild civets. They found no evidence of SARS but decided that trapping in this area would still yield results, as the animal was likely widespread. They found evidence of coronavirus in “little bats.” Another multinational team that included Hendra specialist Hume Field found a virus very similar to SARS in a species known as the horseshoe bat. They further proved that these bats carried many types of coronavirus, of which SARS was only a “small branch,” and this finding established those animals as the reservoir. This meant that civets had acted as an “amplifier” with market conditions providing an opportunity for infection.

Turning to his own adventures, Quammen describes meeting Aleksei Chmura, an ecology graduate student who was studying South Asian zoonotic disease in general and SARS in particular. Quammen characterizes Chmura as a “voracious eater,” readily sampling durian fruit despite its noxious smell and ordering a dish of “congealed pig’s blood” (196). They traveled to a city called Giulin, north of Guangzhou, famous for its caves and therefore home to many bats.

The local market looked tamer and more like Western markets than Quammen expected, which Chmura told him was an aftereffect of SARS. This did not end the trade in wild animals but did drive it underground. Chmura himself was virtually omnivorous, insisting that eating animals was an all or nothing proposition, suggesting he could be tested with human flesh. With Chmura, Quammen visited a cave where they trapped bats with a “mist net” (199). Quammen eventually noticed that, like some of his subjects who caught zoonotic diseases, they wore no masks, in part because it would have made the work more difficult.

In the lab, Chmura and his assistants catalogued the bats by species and took blood samples. Most were released, but two died and were dissected. Chmura disposed of those bats in a bin for hazardous waste, noting that bats eaten for food would go in an ordinary trash can. This reminded Quammen of their earlier discussions about how eating meat is all or nothing, not a matter of drawing distinctions. Instead, “his point again was that such lines of division, especially in southern China, are arbitrarily and imperfectly drawn” (202).

Quammen next describes a journey to a rat farm in the city of Lipu, where rats were raised for sale to restaurants and markets. They met the farm’s owner, Wei Shengzheng, a cheerful and proud man who showed off his bamboo rats. He vaccinated the animals—largely against bacteria—but this would not provide protection against disease once they were at markets for sale. They ate hotpot with the family, including roasted rat, which Quammen decided was likely safest at its source.

To conclude his SARS adventure, Quammen notes that many questions remain. Whether the virus has other reservoirs, how the spillover occurred, and what made the superspreaders so lethal, are some. Others involve the virus itself—the possibility that it evolved during the outbreak, and what role China’s culinary culture played in its spread. Experts agree that the 2003 outbreak was in many ways a “lucky escape” for the world, as the outbreak could have been worse.

Quick and effective laboratory work was a key part of the success story, as were quarantine efforts in public spaces and containment efforts in hospitals. Another was far outside human control: SARS-infected people show symptoms before they are “highly infectious,” which means people can be treated and quarantined before they infect many others. The “Next Big One” will likely involve a disease that is infectious before individuals are obviously ill (208).