Spillover: Animal Infections and the Next Human Pandemic

by David Quammen

The significance of the concept, Lloyd-Smith and his coauthors noted, is that 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.

Zhou himself would eventually become known among medical staff in Guangzhou as the Poison King. He survived the illness, though many people who caught it from him—directly, or indirectly down a long chain of contacts—did not.

“Remember,” she told me, “all this time there are no diagnostic tests.” No tests, she meant, that detected presence or absence of the culpable infectious agent—because no one had yet identified that agent. “We are going purely based on epidemiology—whether there is contact with some of the source patients.” It was blind man’s bluff.

Back in Singapore, health officials and government authorities cooperated to stanch further transmission. They enacted firm measures that reached far beyond the hospitals—such as enforced quarantine of possible cases, jail time and fines for quarantine breakers, closure of a large public market, school closures, daily temperature checks for cab drivers—and the outbreak was brought to an end. Singapore is an atypical city, firmly governed and orderly (that’s putting it politely), therefore especially capable of dealing with an atypical pneumonia, even one so menacing as this.

The very name coined during that early period, SARS, reflects the fact that this thing was known only by its effects, its impacts, like the footprints of a large, invisible beast. Ebola is a virus. Hendra is a virus. Nipah is a virus. SARS is a syndrome.

the symptoms looked a little bit too much like influenza—or, more precisely, like influenza at its worst.

Part of what made the task difficult was that, in pursuing the SARS agent, they didn’t know whether they were looking for something familiar, something newish but closely resembling something familiar, or something entirely new. And there was one other possible category: something familiar to veterinarians but entirely new as an infection of humans. In other words, an emerging zoonosis.

You can’t detect a microbe by its molecular signature until you know roughly what that signature is. So the lab scientist must resort to a slightly older, less automated approach: growing the microbe in a cell culture and then looking at it through a microscope.

Within a few more days, the team had electron microscope images of round viral particles, each particle encircled by a corona of knobs. This was so unexpected that one microscopist on the team had recourse to what amounted to a field guide; he browsed through a book of viral micrographs, looking for a match, as you or I might do for a new bird or a wildflower. He found his match among a group known as the coronaviruses, characterized by a corona of knobby proteins rimming each viral particle.

They were right, and the virus became known as SARS coronavirus, inelegantly abbreviated as SARS-CoV. It was the first coronavirus ever found to inflict serious illness upon humans.

“Were you part of the fieldwork?” “No, I’m a molecular scientist,” he said. It had been like asking Jackson Pollock if he painted houses, I suppose, but Leo Poon didn’t take my question amiss.

These eateries drew their supplies from the “wet markets” of Guangdong province, vast bazaars filled with row after row of stalls purveying live animals for food, such as the Chatou Wildlife Market in Guangzhou and the Dongmen Market in Shenzhen.

In fact, much of the trade in three popular wild mammals—the Chinese ferret badger and the hog badger in addition to the masked palm civet—seemed to come from farm breeding and rearing. Evidence for this supposition, made by the survey team, was that the animals appeared relatively well fed, uninjured, and tame. Caught from the wild, they would more likely show trap wounds and other signs of desperation and abuse.

But even if they arrived healthy and robust from the farm, conditions in the markets weren’t salubrious. “The animals are packed in tiny spaces and often in close contact with other wild and/or domesticated animals such as dogs and cats,” the survey team wrote. “Many are either sick or with open wounds and without basic care. Animals are often slaughtered inside the markets in several stalls specialising in this.”

“The markets also provide a conducive environment,” the team noted, almost passingly, “for animal diseases to jump hosts and spread to humans.”

The hog badgers were clean. The Chinese hares were clean. The Eurasian beavers were clean. The domestic cats were clean. Guan had also sampled six masked palm civets, which weren’t clean; all six carried signs of a coronavirus resembling SARS-CoV. In addition, the fecal sample from one raccoon dog (a kind of wild canid, which looks like an overfed fox with raccoon markings), tested positive for the virus. But the data overall pointed most damningly at the civet.

Using a press conference to break the news about civets, rather than publishing first in a scientific journal, was unorthodox but not unprecedented. Journal publication would have taken longer, because of editorial work, peer review, backlogs of articles, and lead times. Circumventing that process reflected haste, driven by civic concern and the urgency of the outbreak but also possibly by scientific competition.

That act of claiming priority by the CDC, unnoticeable to the world at large, probably put the Hong Kong University scientists on edge against their competitors in Atlanta and elsewhere, and contributed to the decision to trumpet Guan Yi’s discovery at the earliest reasonable chance.

One immediate consequence of Guan’s findings was that the Chinese government banned the sale of civets.

Under the revised policy, farm-raised civets could be legally traded again but the sale of wild-caught animals was prohibited.

The civets might have become infected “from another, as yet unknown, animal source, which is in fact the true reservoir in nature.” They might have functioned as amplifier hosts (like those Hendra-infected horses in Australia).

bats?

The last case was detected and isolated in Taiwan on June 15. Hong Kong had been declared “SARS-free.” Singapore and Canada had been declared “SARS-free.” The whole world was supposedly “SARS-free.” What those declarations meant, more precisely, was that no SARS infections were currently raging in humans.

This was a zoonosis, and no disease scientist could doubt that its causal agent still lurked within one or more reservoir hosts—the palm civet, the raccoon dog, or whatever—in Guangdong and maybe elsewhere too. People celebrated the end of the outbreak, but those best informed celebrated most guardedly. SARS-CoV wasn’t gone, it was only hiding. It could return.

On January 5, 2004, the day the first case was confirmed, Guangdong authorities reversed policy again, ordering the death and disposal of every masked palm civet held at a farm or a market in the province. Wild civets were another question, left unanswered.

Woops, civets aren’t the reservoir of SARS. Never mind.

Just after the epidemic ended, his HKU team started trapping animals out there to look for evidence of coronavirus.

So how much coronavirus did Poon find? I asked. “None at all,” he said. That absence suggested that the civet is not the reservoir for SARS coronavirus. “We were quite disappointed.”

Only three kinds of animal out of forty-four showed any sign of infection with a coronavirus. All three were microchiropterans. To you and me: little bats.

“This bat coronavirus is quite different from SARS,” Poon said. That is, he didn’t claim to have found the reservoir of SARS-CoV. “But this is the first coronavirus in a bat.” That is, he had turned up a strong clue.

What they found was a coronavirus that, unlike Leo Poon’s, closely resembled SARS-CoV as seen in human patients. They called it SARS-like coronavirus.

this SARS-like virus was especially prevalent in several bats belonging to the genus Rhinolophus, known commonly as horseshoe bats.

They roost mainly in caves, of which southern China has an abundance; they emerge at night to feed on moths and other insects. The genus is diverse, encompassing about seventy species.

High prevalence of antibodies to the virus among horseshoe bats, compared with zero prevalence among wild civets, was an important discovery.

Comparative analysis of those fragments showed that the SARS-like virus contained, from sample to sample, considerable genetic diversity—more diversity than among all the isolates of SARS-CoV as known from humans.

In fact, the totality of diversity known in the human SARS virus nested within the diversity of the bat virus.

What did this mean? It meant that horseshoe bats are a reservoir, if not the reservoir, of SARS-CoV. It meant that civets must have been an amplifier host, not a reservoir host, during the 2003 outbreak.

It meant that you could kill every civet in China and SARS would still be among you.

This was the “after” condition in a “before/after” contrast revealing how SARS had put a damper on yewei. What had changed here in recent years, Aleksei told me, was the disappearance of the trade in wildlife. Things had been far different in 2003—and even in 2006, when he first started visiting wet markets in southern China.

“People in south China will eat everything that flies in the sky, except an airplane.” He was a northerner himself.

He didn’t disapprove of eating an animal, virtually any animal, so long as it hadn’t been illegally harvested, it didn’t belong to a threatened species, and it wasn’t contaminated with the sort of pernicious microbes he’d come to study.

What about ape? If you were in Africa, would you eat gorilla or chimpanzee? “I can’t draw the line there,” he answered. “It’s either eat meat, or don’t eat meat. You’d have to test me by putting human flesh in front of me.” This could have sounded ghoulish, provocative, or just silly, but it didn’t, because he was earnestly trying to answer my hypothetical with candor and logic. Taxonomy simply wasn’t among his guiding standards of diet. Back in New York, he had told me, he lives mainly on fruit.

Though we were searching for SARS-like coronavirus in these animals, and sharing their air in a closely confined space, none of us was wearing a mask. Not even a surgical mask, let alone an N95. Um, why is that? I asked Aleksei. “I guess it’s like not wearing a seat belt,” he said.

I was literally wondering this lol I'm pretty sure i read this in Viral but whatever moving on

If you were absolutely concerned to shield yourself against the virus, you’d need not just a mask but a full Tyvek coverall, and gloves, and goggles—or maybe even a bubble hood and visor, your whole suit positive-pressurized with filtered air drawn in by a battery-powered fan. “That’s not very practical,” Aleksei said.

what I thought was, Catching SARS—that’s practical?

The least horseshoe bat is one of the suspected reservoir hosts of the virus.

“But if they were food,” he added, “they’d go there,” indicating an ordinary trash basket against the wall. It was a shrug back toward our dinner discussions and the tangled matter of categorical lines: edible animals versus sacrosanct animals, safe animals versus infected animals, dangerous offal versus garbage. His point again was that such lines of division, especially in southern China, are arbitrarily and imperfectly drawn.

The sign was in traditional Chinese characters but I could tell from the illustrations what was disallowed on board Lipu–Guilin busses: no bombs, no fireworks, no gasoline, no alcohol, no knives, and no snakes. We weren’t carrying any.

Wild Flavor doesn’t need to be seasoned with virus.

When will the virus emerge again?

SARS in 2003 was an outbreak, not a global pandemic.