4.
The seafood market
‘Next time something strange and new comes anywhere in the world, let us come in as quickly as possible.’
GRO HARLEM BRUNDTLAND
(after the first SARS epidemic)
‘The origin of the new coronavirus is the wildlife sold illegally in a Wuhan seafood market.’ So said China’s Dr George Gao, the director of the Chinese Center for Disease Control and Prevention in Beijing, on 22 January 2020. Four months later, Dr Gao was just as certain that the market was not the source of the outbreak: ‘At first, we assumed the seafood market might have the virus, but now the market is more like a victim. The novel coronavirus had existed long before.’ By implication therefore it was people, not animals, that brought the virus to the market. The story of how the Chinese authorities came to change their minds about the role of the Huanan seafood market may provide rich clues to what they had uncovered between January and May 2020.
The Huanan seafood market was hurriedly closed and sanitised at the end of 2019, just one day after the Wuhan Health Commission issued its emergency notice to local hospitals about the atypical pneumonia cases. According to one employee of a local disinfection company, he received a call at 1 a.m. on 31 December to head to the Huanan market. There his team disinfected stalls selling exotic animal meat products or traditional medicine. In parallel, officials from the Wuhan CDC took hundreds of samples from dead animals in the stalls and from surfaces and sewage in the market. On 1 January, another team from the Beijing CDC arrived and continued to collect samples and remove the rest of the animals.
The swiftness with which local officials shuttered and sampled the market was a sign that, at least at the time, the authorities were convinced that the market was a probable source of the outbreak. Curiously, in mid-January 2020, a local CDC official told health experts from Taiwan and Hong Kong that they had not found wild animals at the market and these were not commonly eaten in Wuhan. The consumption of exotic wildlife for food is generally a southern Chinese speciality, though traditional Chinese medicine is more widespread. At the end of January, the Paris-based World Organisation for Animal Health (OIE) was briefed by the Chinese government, one of its members, that none of the animal samples from the market had tested positive for the virus. Over the next few months, Chinese scientists would test more domestic and farmed animals, reporting to the OIE that all samples tested negative.
The main reason for the immediate suspicion that the market was the origin of the novel SARS-CoV-2 virus was the precedent that wildlife markets and restaurants selling exotic meat had played a vital part in the first SARS virus jumping into the human species in Guangdong province in southern China more than fifteen years before . . .
The first SARS epidemic
On 21 February 2003, Dr Liu Jianlun, a sixty-four-year-old medical professor from Guangzhou, the capital of Guangdong province, checked into Room 911 of the Metropole Hotel in the Kowloon district of Hong Kong to attend the wedding of a nephew. He had already been feeling ill for five days before his visit to Hong Kong, and his condition worsened so much overnight that he was rushed to the intensive care unit of Kwong Wah Hospital, where he would die within two weeks. While in hospital, he revealed that he had been treating a secret outbreak of a new disease in Guangdong and warned his carers to take precautions. Nonetheless, one doctor and five nurses at the hospital caught the infection from Dr Liu. Within days, at least seven other hotel guests staying on the same floor as Dr Liu had carried the SARS virus, unawares, to Toronto, Hanoi, Singapore and elsewhere in Hong Kong. By then the SARS virus had already separately reached Beijing.
A retrospective investigation by the Guangdong Provincial Center for Disease Control and Prevention revealed that the first person known to have fallen ill with SARS was a forty-five-year-old administrator from Foshan City, Guangdong. On 16 November 2002, he suddenly began to feel seriously unwell. He had not travelled outside the local area for two weeks, but had prepared chicken, domestic cat and snake for consumption at home. In Guangdong, domestic cat meat is a delicacy, and a 2002 Guangzhou news report claimed that ten thousand domestic cats were consumed in Guangdong each day – the demand was so large that cats were imported from nearby provinces. Before the end of 2003, domestic cats had been determined to be susceptible to infection by SARS-CoV and also capable of infecting other animals in close contact. The index case’s wife also caught the virus, but his four children did not. After his aunt visited him in hospital, she, her husband and her daughter all also caught the disease.
This was not the only index case, however. Between November 2002 and mid-January 2003, SARS seems to have erupted several times across seven municipalities without human contact between the cases. On 10 December, in Heyuan, another city in Guangdong, a restaurant chef fell ill; on 21 December, a factory worker in Jiangmen City; on 26 December, another restaurant chef in Zhongshan City, all near the city of Guangzhou. This pattern left investigators wondering whether there was a missing link between these sporadic index cases or if they had each been exposed to multiple sources of the virus along the massive delta of the Pearl river.
On 3 February, Guangdong province instituted the mandatory reporting of atypical pneumonia cases to local CDCs and the provincial CDC, so that cases could be contact-traced and detailed patient data could be collected. But it was too late. By 24 February, news that more than fifty hospital staff in Guangzhou had been infected with a mysterious pneumonia reached the Global Public Health Intelligence Network. Yet it was not until three months into the epidemic that the Chinese government authorities admitted that there was a serious problem.
Back in 2003, the WHO was severely critical of the Chinese government for its lack of openness. On 14 March that year, without waiting for the Chinese government’s agreement, the WHO announced a global alert, issuing a series of travel advisories. In April, the WHO’s director general at the time, Gro Harlem Brundtland, gave an unprecedented dressing down to a member state, saying: ‘It would have been definitely helpful if international expertise and WHO had been able to help at an earlier stage.’ Despite this criticism, when the WHO sent a team of experts later in April to investigate the extent of the outbreak in Beijing, the Chinese authorities instructed doctors to hide several dozens of SARS patients in a hotel and in ambulances so that the WHO team would not find them. The patients in ambulances were driven around the city while the WHO team visited the hospital.
By this time in April, the virus had infected more than 3,500 people across 25 countries. Scientists in Vietnam had obtained preliminary evidence suggesting that individuals with mild symptoms could spread the virus, and that the incubation period could be longer than a week. An explosive cluster of 250 cases at a housing complex in Hong Kong also hinted that the virus was spreading through infection routes other than droplets from coughing or sneezing by infected individuals. After detecting that the virus was beginning to bring down younger and healthier people, the WHO commented that the SARS virus ‘may have mutated into a more virulent form’.
Fortunately, the strict containment measures worked and by early July the epidemic had petered out after more than 8,000 cases worldwide and a death toll of nearly 800 people. The worst affected country outside of Asia proved to be Canada with 438 cases and 44 deaths. It had been taken by surprise by the Metropole Hotel superspreading event. Countries that were significantly affected by SARS, especially China (particularly Hong Kong), Taiwan, Singapore and Canada, learned valuable lessons from the outbreak that would stand them in good stead in 2020. One of us (Alina) was a teenager living in Singapore when the 2003 SARS outbreak hit. Scenes of quarantined individuals and patients in the intensive care unit were constantly on the news, interlaced with advice for members of the public on best practices to avoid catching the virus. So, in January 2020, when video footage of corpses piling up on the floors of hospitals in Wuhan surfaced on the internet, Alina was immediately fearful that the uncontrolled spread of the virus would soon lead to a similar calamity elsewhere in the world.
Tracking down the zoonotic culprit
Many new viral diseases stem from zoonoses, meaning they jump from another species of animal into human beings. HIV originated in chimpanzees; measles in cattle; Lassa fever in rodents; influenza in ducks and other birds; rabies, Ebola and Marburg virus in bats. Twice in the 1990s, viruses jumped from fruit bats into people: in Australia in 1994 when fruit bats infected horses which infected people with a lethal virus called Hendra; and in Malaysia where fruit bats infected pigs which infected people with a nasty virus called Nipah. In the distant past, the original zoonotic event at the start of an epidemic was almost impossible to identify. Nobody knows exactly where or how the plague that caused the Black Death made the leap from a central Asian wild rodent to a black rat and thence, via a flea, to a person. Even HIV, which is estimated to have spilled from chimpanzees to human beings sometime in the 1920s, remains challenging to trace back to its precise zoonotic source – the one from which humans first received the virus. Despite being named a novel disease in 1981, it was not until 1989 that scientists discovered a very closely related virus in wild chimps, and it was not until 1998 that a separate group of scientists leveraged new technology to sequence the virus from a 1959 human blood sample taken in Kinshasa, in what is now the Democratic Republic of Congo. Determining where and when a novel pathogen first emerged in the human population is exceedingly difficult and requires scientists to gather a large amount of data in a timely manner.
However, genomic technologies and growing scientific knowledge, particularly when applied to emerging pathogens close to world-class research hubs, have changed that and today it should be much easier. The immediate zoonotic source of the first human SARS virus was tracked down rapidly. International interest was high because of the way the outbreak had erupted in Hong Kong and spread to numerous countries and thousands of individuals within a couple of months. Tracing each transmission chain of the virus and hunting down its source in Guangdong was urgent to prevent widespread loss of life. It helped that numerous Chinese experts (several based in Hong Kong where the Metropole Hotel superspreader event had occurred) immediately began to investigate the outbreak.
In the spring of 2003, it dawned on investigators that many of the early cases of SARS had been food handlers, particularly chefs and others who prepared animals for food. In May, in the search for the zoonotic source, a team of scientists from Hong Kong visited a live animal market in Shenzhen, Guangdong, to collect animal samples from different stalls, spanning wild and domestic species, originating from different parts of southern China. All the animals appeared healthy. The scientists took samples from the noses and anuses of twenty-five animals from eight, mostly wild, species: beaver, ferret-badger, hare, muntjac deer, domestic cat, hog-badger, raccoon dog and Himalayan palm civet. Of most relevance to the story of SARS is the palm civet, a tree-climbing, fruit-eating relative of cats. An expensive dish popular with wealthy people in Guangdong is known as ‘dragon-tiger-phoenix soup’. It is flavoured with chrysanthemum petals but contains the meat of both civets and snakes. From the twenty-five market animals, the single raccoon dog and a hog-badger tested positive, as did four of the six civets. SARS virus was isolated from five of the animals, and two virus isolates from the civets were completely sequenced to obtain their genomes.
In parallel, the same team of Hong Kong scientists tested dozens of stall holders for antibodies to SARS, although none had been diagnosed as SARS cases previously. Eight of twenty (40 per cent) wild animal traders and three of fifteen (20 per cent) people who slaughtered animals had evidence of antibodies, while only one of twenty (5 per cent) vegetable traders had them. As a comparison, sixty anonymised samples from Guangdong patients hospitalised for non-respiratory diseases were analysed. None of them tested positive for SARS antibodies. Similar studies were conducted in the same month of May by Guangdong scientists, who detected SARS antibodies in sixty-six of 508 (13 per cent) animal traders from three animal markets; again, none had been diagnosed with SARS or an atypical pneumonia previously. The highest antibody prevalence (72.7 per cent) was found in those who primarily traded civets, with the lowest prevalence (9.2 per cent) in those who primarily traded snakes.
Masked palm civet (Paguma larvata) on sale in a market in Southeast Asia.
travelib prime/Alamy Stock Photo
When SARS broke out again in the winter of 2003–4, civets were implicated once more. This time, of the four new cases, one was a waitress and another a diner at the same restaurant in Guangzhou. The patients each had mild symptoms and did not appear to transmit the virus to others around them – even to healthcare workers. This stood in contrast to the contagiousness and virulence of the first SARS virus. The virus genome sequences from these new cases were distinct from those of the SARS virus that had proliferated earlier in 2003. In addition, unlike the first SARS virus, which had been isolated in March 2003, it was not possible to isolate the new SARS virus from any of the patient samples – signalling that the virus was not yet well adapted to infecting primate cells, the typical means by which viruses are isolated.
The waitress was diagnosed with possible SARS on 2 January 2004. She denied consuming or having been in proximity to civets. Nonetheless, when scientists immediately went to her restaurant to investigate, they found civets. In the restaurant, cages in which the animals were kept had been placed near the dining area. The scientists collected samples from all of the civets and employees at the restaurant. They also traced the restaurant civets to a live animal market in Guangzhou and sampled the animals there for SARS. All six civets sampled at the restaurant tested positive for SARS and the sequences of the civet virus matched those of the two patients. Strikingly, these 2004 SARS sequences more closely resembled the virus that had been isolated from market civets in 2003 than the viruses found in humans in the earlier outbreak. Two of thirty-nine other restaurant employees tested positive for antibodies against SARS but had not reported illness or fever in recent months. These observations strongly indicated that the new SARS cases had resulted from a more recent zoonosis from an animal source rather than an undetected continuation of the 2003 human SARS epidemic.
Based on this second emergence of SARS within months of the first epidemic, Guangdong officials implemented strong measures on 5 January 2004 to eradicate any animal in farms and markets that might transmit SARS virus. Approximately ten thousand civets were exterminated, largely by drowning the animals in vats of disinfectant, while objects that had been in contact with these animals were incinerated. Continued investigation of hundreds of the animals revealed that although there was widespread infection of SARS among civets in markets, there was none in the farms where they were reared. Oddly enough, four civets at one farm in Guangdong tested weakly positive for SARS antibodies, but this farm specialised in obtaining them from various markets to sell as pets – it was possible that the civets had been infected with SARS at these markets prior to being brought to the pet farm.
So the civets could not be the original source of the virus. The market civets sampled by the Hong Kong team in May 2003 had originated from different regions of southern China yet had caught almost identical viruses. It was more likely that they had picked up the virus during transit closer to point of sale or at the markets from any of the numerous other animal species there. The presence of SARS antibodies in animals and animal traders from several different markets in Guangdong province suggested that there was frequent and widespread circulation of SARS-like viruses, with the 2003 SARS virus being the first to demonstrate a capacity to afflict humans with severe respiratory disease and spread rapidly from human to human. Where were these SARS viruses coming from?
Between the summer of 2004 and the spring of 2005, a team of Hong Kong scientists captured 127 bats, 60 rodents and 20 monkeys from 11 locations in the wild in Hong Kong, and analysed their noses, anuses and blood for signs of coronaviruses. The anal swabs from 29 bats tested positive for coronavirus, largely those from the species known as the Chinese rufous horseshoe bat, Rhinolophus sinicus. The viruses that some of these bats were carrying proved to be similar to the SARS virus but were not close enough to be the immediate ancestors. Their genomes also shared a short sequence with the civet SARS viruses that was missing from the human version (excepting one of the earliest human cases from the 2003 outbreak), implying that the bats could not have caught the virus from people. More likely both the civet version and the human version were descended from a bat virus. From this moment bats took centre stage.
The MERS eruption
Between the epidemics of SARS in 2002–4 and SARS-CoV-2 in 2019, another deadly coronavirus spilled from animals into humans. In 2012, Dr Ali Mohamed Zaki, a skilled Egyptian virologist based at a private hospital in Jeddah, in Saudi Arabia, isolated a novel coronavirus, which we now know by the name of MERS (Middle Eastern Respiratory Syndrome virus). In the previous two decades, Dr Zaki had been the first to diagnose dengue in Saudi Arabia (1994) and to identify a new tick-borne flavivirus that causes severe haemorrhagic fever (1997). The patient who was admitted to his hospital in June 2012 declined rapidly, presenting acute pneumonia and renal failure, dying eleven days later. Before the patient’s death, Dr Zaki took a sample from the throat and inoculated it into two types of monkey cells that are commonly used in laboratories to study viruses. Under the microscope, he observed cell death alongside ‘syncytia’, or large, fused cells with multiple nuclei. That told him that he was probably dealing with a virus not a bacterium. However, by then the patient had died, and others were no longer interested in investigating the mysterious new infectious agent. Undeterred, Dr Zaki conducted genetic tests for influenza, Nipah, Hendra and hantavirus (a rodent-borne pathogen), which returned negative results; but a general test for a coronavirus produced a strong positive signal. When repeated tests for SARS virus also came back negative, Dr Zaki began to realise that he was dealing with a new kind of coronavirus. Sure enough, he had discovered MERS, a nasty disease that kills more than a third of the people it infects. Dr Zaki’s decision to alert the world to this novel pathogen on 15 September 2012 infuriated the Saudi authorities. He fled to his native Egypt, leaving his belongings behind in Jeddah.
Fortunately, MERS cases have been sporadic, but at the time of writing 2,574 people have had it and 886 of them have died, mostly in Saudi Arabia. There has been a single large outbreak since its discovery: in 2015, MERS spread to South Korea in an infected traveller from the Middle East, killing thirty-eight people. Once MERS was sequenced, the main clue that it had originated in bats was that a similar lineage of bat coronaviruses had been sampled in China in 2007. Some MERS-like coronaviruses have been identified in bats in Saudi Arabia and South Africa, but none of them is a recent ancestor of the MERS viruses found in humans. In the past decade, prolific research into MERS has concluded, based on strong epidemiological and genetic evidence, that camels have carried MERS viruses for decades before human cases were even identified. Multiple genetic lineages of the virus have been observed from camels in Saudi Arabia alone, with MERS antibodies detected in camel blood samples from as early as 1983 in Sudan and Somalia. Exactly how and in what form the virus got from bats to camels remains unclear.
The wildlife trade and traditional medicine
After the 2003 SARS epidemic, the Chinese government cracked down on the sale of wildlife in markets, banning the sale of wild animals altogether that year, forbidding hunting, and even outlawing the consumption of wild animals. But not all exotic – non-domesticated – animals were caught in the wild. Some were being bred and reared in farms. Within months, the rules had been relaxed for fifty-four species of wild animal reared on farms, including civets. Indeed, the business of farming exotic species was booming. By 2017, the practice of wildlife breeding had burgeoned into a $73 billion industry providing employment for more than fourteen million people, particularly in rural areas of China. In November 2019, according to the Los Angeles Times, the Jiangxi provincial government boasted that it had helped 1,700 people in one town to ‘embark on the road to riches’ by taking up the breeding of civets. ‘Wildlife breeding and utilization is a rapidly developing industry in recent years,’ said a director of wild animal and plant protection at the Forestry Academy in Jiangxi. ‘Our province should seize the opportunity.’
As this quote and job title suggests, many of those charged with wildlife protection are also involved in its commodification. Three of the fourteen vice chairs of the China Wildlife Conservation Association had strong links to traditional Chinese medicine (TCM) companies, according to the Los Angeles Times, including ones that sold tiger bone wine, snake bile, seahorses and pangolin scales. There is little doubt that the exemption for farmed exotic animals also opened a loophole that was widely exploited by trappers and smugglers trafficking animals caught in the wild, including species such as the yellow breasted bunting, a small bird highly valued for its taste, sold on the black market, consumed in the millions and now driven to the brink of extinction. Many animals are sold alive in these markets and sometimes even restaurants, to show customers that they are fresh and healthy before consumption.
One reason for the boom in exotic wildlife markets is that, under Chinese President Xi Jinping, TCM has been championed. Practitioners of TCM believe that meat or medications that come from certain exotic animals, such as pangolins, bears, tigers or snakes, can be used to cure ailments. In 2019, at China’s request, the WHO officially adopted TCM as a recognised form of medicine. Export markets for TCM are being developed by Chinese firms in Africa. In October 2019, weeks before the first case of Covid-19, President Xi opened a conference with these words: ‘Traditional Chinese medicine is a treasure in Chinese civilisation, which carries the great wisdom of Chinese people.’ In May 2020, Beijing health authorities publicly solicited submissions on a draft regulation that could criminalise anyone who slandered TCM.
So it was not just the sale of fresh meat that posed a risk of zoonosis. Although bats are eaten throughout southern China, it is mostly the much larger fruit bats that are consumed, not the small horseshoe bats, on which there is little meat. However, the smaller bats are used in TCM. For example, the ‘greater’ (but still small) horseshoe bat Rhinolophus ferrumequinum lives in the vicinity of Wuhan and its droppings are used in medications to treat eye conditions. It has been found to carry coronaviruses, although no virus closely related to SARS-CoV-2 has been detected in Wuhan or Hubei province despite thousands of bats having been sampled in the area over several years. The bat’s body parts and its guano are also dried and ground into a powder to be ingested as a detox treatment or applied to the human body. Drying the dung or the body parts probably inactivates any viruses, but the handling of bats clearly carries a risk to the trader.
So it is little wonder the wildlife trade came under suspicion at once. ‘Probably bats are the origin from looking at the virus itself, and it got from bats into people in the wildlife market,’ said Dr Peter Daszak, president of the EcoHealth Alliance and long-time collaborator of Dr Shi at the WIV, in late January 2020. ‘This is absolutely déjà vu all over again from SARS.’ Dr Shi was equally certain: the outbreak was ‘nature punishing the uncivilized habits and customs of humans’.
The snake theory
The Huanan seafood market was one of the largest ‘wet markets’ in China – so called because of their constantly wet floors due to the melting ice used to preserve meat and the regular washing down of stalls to get rid of blood and dirty water. It had nearly seven hundred stalls and an estimated ten thousand people visited every day. At the end of 2019, it was rumoured that these stalls offered a wide range of animals for sale, mostly alive or preserved, including crocodile, turtle, badger, bamboo rat and hedgehog, as well as plenty of seafood. One price list showed prices for foxes, wolf puppies, giant salamanders, snakes, rats, peacocks, porcupines and even koalas. Bats were not on sale, as far as anybody could tell, and nor were pangolins.
At first suspicion fell on snakes, which were sold alive in the market, although slaughtered at the point of sale. A study by five Chinese scientists published in the Journal of Medical Virology on 22 January 2020 claimed that the novel SARS-CoV-2 virus had the ‘most similar codon usage bias with snake’. The argument was that viruses tend to use the amino-acid-encoding three-letter codes (codons) most frequently used by their host so that they can more effectively hijack the host protein production machinery. The new virus sported codons more commonly used in snakes than in marmots, hedgehogs, bats, birds and humans, the researchers found.
Before the pandemic, approximately nine thousand tonnes of snakes were sold in Chinese markets each year. One village in southern China, Zisiqiao, was home to a snake museum and a hundred snake farms, selling three million of the creatures a year, many of them venomous. Snakes and their venom have been a staple in TCM for thousands of years, and a few of the farmers in Zisiqiao made millions of dollars each year. These are conditions of density conducive to disease outbreaks, but cold-blooded reptiles are extremely unlikely to catch viruses from distantly related and hot-blooded mammals such as bats, let alone to pass them on to human beings. Even birds are generally too distant to share their pathogens with people, although influenza did manage to make the transition, probably via another intermediary species such as pigs. By far the greatest risk of zoonosis into humans lies with mammals. Yet when speculations emerged that the novel SARS-CoV-2 virus might have come from snakes, the Chinese authorities temporarily banned the snake industry and the lucrative business in Zisiqiao was shuttered.
The codon-usage snake origin hypothesis came to nothing. Even the snake study had acknowledged that the virus’s genome was clearly related to that of bat viruses and not snake viruses. By February, the WIV’s unveiling of a bat virus with 96.2 per cent genetic similarity to the human SARS-CoV-2 virus put the spotlight firmly back on bats. This seemed to bear out some dire warnings that had emanated from experts for many years. In 2007, four scientists from the University of Hong Kong, including those who had first found SARS-like viruses in bats, reflected on the SARS experience in a paper published in Clinical Microbiology Reviews and concluded starkly – and presciently: ‘The presence of a large reservoir of SARS-CoV-like viruses in horseshoe bats, together with the culture of eating exotic mammals in southern China, is a time bomb.’ Two of the authors repeated the warning in February 2019 in a paper with two other colleagues from the University of Hong Kong: ‘Bat–animal and bat–human interactions, such as the presence of live bats in wildlife wet markets and restaurants in Southern China, are important for interspecies transmission of [coronaviruses] and may lead to devastating global outbreaks.’
Nonetheless, in the case of SARS, bats had not been determined to have infected people directly. They had infected palm civets or other susceptible animal hosts, which then passed the virus to people processing the civets for eating. Likewise with MERS, bats had probably infected camels which had infected people. An intermediate host, one that was likely to come into contact with bats as well as people, therefore seemed worth seeking in the case of SARS-CoV-2 as well.
The third time round
If we count the two SARS outbreaks in the winters of 2002–3 and 2003–4 in Guangdong province, the emergence of SARS-CoV-2 in Wuhan was the third time a SARS-like virus had led to a detected, reported outbreak in human beings in China. Contrast the technology available in the early 2000s with that of 2020. In 2003, scientists first had to culture the virus, then clone fragments of its genome for individual sequencing by laborious and slow machines. It took weeks to sequence a coronavirus genome. Today next-generation sequencing machines and software can spit out a full genome sequence in a few days. Yet contrast the timeline of the two epidemics. The SARS virus was isolated in March 2003, its genome sequenced in April, and animal sources in markets identified in May. At the same time in mid-2003, multiple groups of scientists were finding evidence that the animal trading community had previously undetected, widespread exposure to SARS-like viruses. When SARS emerged again in late 2003, the tracking of the spillover source was even faster. A waitress was diagnosed on 2 January 2004. Within two days, samples had been collected from all palm civets and employees at the restaurant, several of which tested positive for the virus. By 5 January 2004 the outbreak had been traced to a market. In other words, it took only a few months in the first round (expedited to a couple of weeks on the second round) to go from identifying a SARS virus to finding the proximal zoonotic source by which people had been infected. Yet today, close to two years into the outbreak, with much more superior technology and similar outbreak circumstances, we still have no idea where the first patients caught SARS-CoV-2.
In 2019, news about the novel coronavirus had leaked to the public on 30 December. The Chinese authorities knew what needed to be done. By the next day, local CDC employees had started to collect hundreds of samples from the Huanan seafood market and the market was closed. However, apart from a private meeting of the World Organisation for Animal Health (OIE) on 31 January 2020, no detailed results about the testing of Huanan seafood market samples were released during 2020. According to the Wall Street Journal, the OIE was told that none of the test results from animals were positive but information about the sample size and sample species was lacking. The 22 January announcement by the Chinese authorities that the virus had spilled over from illegal wildlife at the Huanan seafood market became the established wisdom throughout the world over several months. It remains the default understanding of many lay observers to this day despite the absence of any animal samples testing positive for SARS-CoV-2 from the rigorously sampled market.
Vital information about the samples tested from the market that could have helped the world to understand and, ideally, to inform public health responses to the pandemic was not shared in the timeliest manner. By December 2020, the Chinese authorities still had not confirmed whether any live animals had been tested in January and we were left piecing together scraps of leaked or half-announced information to try to ascertain whether a key hypothesis about the worst pandemic in a century was well substantiated.
During all these months, it turns out that Dr Gao’s colleagues were in possession of a map, finalised around 22 January, showing exactly which stalls in the market had belonged to or been visited by people who fell ill, and which stalls had provided positive tests of environmental samples. This map was not shared with the world, although a slightly different version did reach the United States Centers for Disease Control and Prevention and the WHO, both of which also chose to keep it secret.
The Chinese CDC’s map only emerged in a leak to the South China Morning Post, which published it in mid-December 2020, almost a year after the initial outbreak in Wuhan. It showed that thirty-three stalls in the market were linked to forty-five suspected or confirmed human cases of Covid, mostly in the western block of the market, west of Xinhua Road. In the middle of this block, there was a hotspot of positive environmental samples in one section selling wildlife and poultry and a second section selling seafood. In the news story about the map of the market, Dr Lawrence Gostin, director of the O’Neill Institute for National and Global Health Law at Georgetown University, told the South China Morning Post that China’s ‘failure to allow a full and independent investigation into the origins of the outbreak was a major failure of transparency and international cooperation’.
Eventually, when international experts convened by the WHO were granted permission by China to visit Wuhan and arrived in early 2021, they were given a detailed run-down on what had been found in the market. The China-WHO joint report published on 30 March 2021 revealed that the Chinese CDC inspectors had visited the market about thirty times from 1 January before a final clean up on 2 March 2020. In addition to animal products and frozen goods, samples had been taken from doors, stalls, transport carts, trash cans, toilets, sewage, ventilation systems, stray cats and other animal vectors such as mice. Two other nearby markets had also been sampled.
This China-WHO report revealed a different picture from that given by media reports. The market was called a seafood market for a reason: most of the stalls were selling seafood and freshwater aquatic products. Crocodiles were being sold alive. Snakes and salamanders were being slaughtered on the spot for sale. From sales records in December 2019, just ten stalls were selling meat or products from birds and mammals, including chickens, ducks, geese, pheasants and doves; and deer, badgers, rabbits, bamboo rats, porcupines and hedgehogs. According to the market authorities, all of these animals were from licensed farms and no illegal trade in wildlife was detected.
The authorities tested 457 samples from 188 animals spanning 18 species. They all proved negative for SARS-CoV-2 genetic material. This included 27 stray cats (a species that is susceptible to the virus), which were presumably living free in or around the market, as well as 52 rabbits and hares, 16 hedgehogs, ten mice, seven dogs, six muntjac deer, six badgers, six bamboo rats, a number of pigs, five chickens, three giant salamanders, two wild boar, two crocodiles, two soft-shelled turtles, two fish, one sheep and one weasel. They tested 616 animals of ten species from the suppliers to the market and found no sign of SARS-CoV-2 genetic material.
A total of 923 environmental samples were tested, meaning samples from countertops, door handles, toilets, sewage and the like. By mapping the samples that came back positive for virus genetic material to the stalls in the market, the China-WHO team were able to assess what products the vendors at those affected stalls were selling. Of the twenty-one impacted vendors, sixteen were selling ‘cold-chain products’ – delivered and sold in frozen form – out of eighty-seven vendors selling such products whose stalls were sampled; thirteen out of seventy-three selling aquatic products; six out of fifty-six for seafood; eight of thirty-seven for poultry; five of thirty-six for livestock; and two of eight selling vegetables. Only one out of nine vendors selling wildlife products was linked to a positive market environmental sample, and he or she had also been selling cold-chain products, aquatic products, poultry and livestock products.
Needless to say, this was a vital slug of information to emerge after so many months of speculation worldwide that the wildlife trade was bound to be the culprit. There was, after the back and forth by the Chinese CDC director and a year of waiting, no evidence that the virus had emerged in the Huanan seafood market via the wildlife trade. The epidemiological data, the genetic data and the positive environmental samples from the market were consistent with a scenario in which a sick person brought the virus into the market, where it became amplified in a poorly ventilated and crowded space. On the role of the Huanan seafood market, the China-WHO joint team stated that: ‘No firm conclusion therefore about the role of the Huanan market in the origin of the outbreak, or how the infection was introduced into the market, can currently be drawn.’