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The next black swan: Will illegal exotic meat cause the next pandemic?

Bushmeat, from wild animals captured for food, is a staple in parts of Africa and a delicacy in Europe and beyond.

At first glance, there seems to be nothing unusual about Ridley Road Market. Like any other London market, there are stalls selling fresh fruit and vegetables, cheap electronics, artificial jewellery and other bits and bobs.

Then, the smell hits you. Behind the makeshift stalls are butchers’ shops. There’s a dozen of them within 100 metres, each displaying a panoply of meats and hung carcasses. There are beef ribs, pork shoulders, lamb shanks, chicken thighs – all the standard offerings found at most butchers. But there are also more unusual cuts like lamb heads, ox kidneys, cow hooves and others I don’t recognise.

Some of the butchers show questionable hygiene: they handle meat with bare hands, blood oozes out onto shop floors and flies settle on some of the meat. Most things are unlabelled. None of this deters shoppers, but it’s not what I expected from a market that has already been under the spotlight for selling smuggled bushmeat.

Bushmeat is a catchall phrase for the meat of wild animals found in the tropics, principally West and Central Africa. It is illegal in the UK and many other countries, which were forced to adopt strict rules following disease outbreaks that were linked to the import of wild meat.

Humans have, of course, hunted and eaten wild animals for hundreds of thousands of years. Before we invented agriculture and domesticated animals, wildlife was a key source of nutrition (and still is in some parts of the world). Without such hunting, we would never have become the planet’s dominant species.

But the equation has changed. There are now too many of us and too few of them. Worse still, the imbalance we’ve created has opened us up to diseases that would have otherwise remained in wild animal ‘reservoirs’. If a specific set of circumstances align, an infectious disease that jumps from an animal to a human can spread rapidly and kill indiscriminately in our hyperconnected world.

In a related story, Yepoka Yeebo reported from Ghana’s largest bushmeat market to understand why people eat wild meat. The desire for such forbidden fruits has fuelled an illegal trade in wildlife meat across the world, estimated to be worth billions of dollars every year. What risk does this trade carry for spreading disease?

A US government report believes that the next pandemic will be a black swan event, which means, like the 9/11 attacks, it will be hard to predict and will have a huge impact on society. We may not be able to stop such an event from occurring. But bringing the bushmeat trade under control will help conserve endangered species and give us more time to prepare for whatever that black swan might be.

The many lurking viruses

Infectious diseases are caused by pathogens of all shapes and sizes – from single molecules called prions to multicellular parasites like tapeworms. The diseases they cause range from the mild, like the common cold, to the devastating and fatal, like rabies. Together, infections cause one in five deaths every year, and make billions of us ill.

Fortunately, not all pathogens are capable of creating the next pandemic. Black death, which killed a third of Europe’s population in the 14th century, was caused by the bacterium Yersinia pestis. With modern antibiotics, we generally don’t need to worry about bacteria ­­­– at least not until a superbug resistant to all antibiotics finds a way of spreading.

But some infections have the potential to cause what scientists simply call the next big one. ‘Next’ because this sort of thing has happened before – think about the 1918 Spanish flu pandemic – and ‘big one’ because the scale and cost to society can be tremendous. The next big one could be a known threat, such as Ebola or bird flu, or it could be something you’ve never heard of.

The experts I spoke to agree that the agent most likely to cause the next pandemic will be a virus – more specifically, an RNA virus. These viruses are the bêtes noires of infectious-disease specialists, and are responsible for influenza, MERS, Ebola, SARS, polio, HIV and many more infections you’ve probably heard of.

They also cause lesser-known diseases with the potential to become the next big one: Marburg, Lassa, Nipah, Rift Valley fever and Crimean–Congo haemorrhagic fever to name a few. (In early September a man died from Crimean–Congo haemorrhagic fever in Spain, reportedly the first case in Western Europe in someone who hadn’t travelled to areas affected by the disease.)

Unlike the cells that make up living things, viruses are lean. They carry only as much genetic code as needed to enter a cell and take over its machinery. RNA viruses lack the genetic code to make an error-correcting enzyme called DNA polymerase. This means that they suffer many times the mutation rate of any other kind of organism.

Such a high mutation rate would be considered a curse for a large organism, but for RNA viruses, it is a boon. Most mutations will render a virus less powerful, but every so often one will give it a nasty new power, say the ability to be more harmful to a new host. If such an evolved virus were to find a new host, it could unleash a new epidemic.

The other thing that experts are quite sure about is that the next big one will be a zoonotic disease – one capable of jumping from animals to humans. The fear of such an event, often called a ‘spillover’, is why bushmeat gets a bad rap.

Unlike smallpox and polio, which have been eradicated and nearly eradicated respectively, zoonotic diseases cannot be eradicated – unless we can also eradicate all the species that serve as reservoirs for these pathogens. Black death, Spanish flu and HIV – causes of the three biggest known pandemics – are all zoonotic diseases, and so, almost certainly, will be the next big one.

In 2015, the World Health Organization (WHO) published a list of the top emerging diseases that are “likely to cause severe outbreaks in the near future”. It’s no coincidence that all the diseases on the list are zoonotic diseases caused by RNA viruses, which turn animals – mostly wild ones – into reservoirs to hide in.

To understand why WHO worries about them, consider the example of the influenza virus H5N1. Between 2003 and 2014, this RNA virus, which causes bird flu, infected some 600 people, killing more than half of them. Though the current known strains of virus can kill, they do not have the capacity to pass from one human to another. This is what, according to WHO, keeps most cases of H5N1 restricted to directly spilling over from a host reservoir, mainly wild ducks, into humans.

But a 2012 study in ferrets showed how easily this flu virus could acquire mutations that would enable it to pass from one mammal to another. Scientists at the Erasmus Medical Center in the Netherlands transferred H5N1 virus from the nose of one ferret to another and then to another. They repeated this ten times, and, at the end of the experiment, through mere random mutation and replication, the virus had acquired the ability to transfer from ferret to ferret without any more help from the scientists.

The implication of their study, which was mired in controversy, is that such a crucial mutation could indeed come about as a matter of chance. In the case of ferrets, scientists rolled the dice ten times to hit upon a deadly and easily transmissible strain. We don’t know how many rolls will be needed to achieve a similar effect in a human strain. What we do know is that every human–animal interaction, such as every bushmeat kill, represents a chance roll of the dice for the virus to jump into a new species.

Meat causing mayhem

Pheasants are a delicacy in the UK. In the USA, elk is a popular game meat. Ostriches provide the leanest red meat you can buy in South Africa. Marmot, an oversized squirrel, is a delicacy in Mongolia. The list goes on. Risky or otherwise, there’s a huge market for hunted animals across the world.

All wild meat is dangerous to some extent. Consider the 2012 outbreak of trichinellosis in Europe, the first in more than 20 years. Researchers in Italy found thatuncooked sausages made from wild boar meat were responsible for infecting more than 30 people with the pathogen Trichinella britovi.

An outbreak of anthrax in the Yamal Peninsula region of Russia this year has so far claimed the lives of 2,349 reindeer, four dogs and a 12-year-old boy (having infected 25 humans). The origin may have been an infected reindeer carcass that died 75 years ago during a previous anthrax outbreak. A warming globe may have caused the carcass to thaw, and the pathogen Bacillus anthracis probably contaminated the surrounding soil.

But some wild meats are a lot more dangerous than others. Tropical forests are home to a much higher number of species than other kinds of forest, which means their inhabitants can carry more kinds of disease-causing microbes than wild animals in other parts of the world. Bushmeat in Africa has been shown to be the source of scourges such as HIV. More recently, bushmeat may be to blame for the 2014 Ebola outbreak, which sent a chill down the spines of epidemic experts.

The writer David Quammen warned in his 2012 book Spillover that scientists had predicted a big Ebola outbreak. For decades, careful work had spotted Ebola spillovers across West and Central Africa. None had, however, killed more than a few hundred people. The 2014 outbreak looked different, and that’s what was worrying. It was spreading faster, while maintaining its notoriously high kill rate (nearly 70 per cent). By the time it ended two years later, it had infected 28,000 people and killed more than 11,000. It didn’t spread beyond West Africa, but it raised alarm far beyond.

Though we have been studying Ebola for decades, we didn’t know then, and still don’t know now, some of the most basic things about the virus. For example, what is the animal reservoir from which Ebola spills over? (Read our related piece on searching for Ebola’s hiding place.) Our lack of preparation was astounding – there was no vaccine against Ebola and to develop one would have taken years. Even with the vaccine candidates we now have, it will take at least a year to get a vaccine tested, approved and manufactured – and this testing can only happen during an Ebola outbreak to ensure the results of trials are reliable. The 2014 outbreak showed that we are not even close to being prepared to deal with the next big one.

The only upside was that the world began to take spillovers more seriously. Many African countries stepped up their fight against illegal bushmeat, with some adding bats, the suspected Ebola reservoir, to the list of species banned from being hunted. The Guardian highlighted the practice of eating ‘smokies’ – a West African delicacy that is illegal in the UK. Newsweek ran a story about how New Yorkers are able toeasily buy illegal bushmeat (in which, though they didn’t detect Ebola, researchers found other possible human pathogens, such as simian foamy virus and herpes virus).

The most pertinent report, however, came from the European Food Safety Authority (EFSA). It noted the steps that would be required for a European to be infected with Ebola through bushmeat: “1) the bushmeat has to be contaminated with [Ebola]; 2) the bushmeat has to be (illegally) introduced into the EU; 3) the imported bushmeat needs to contain viable virus when it reaches the person; 4) the person has to be exposed to the virus; and 5) the person needs to get infected following exposure.”

EFSA then concluded that, although it doesn’t have the probabilities for each of those steps to assess the absolute risk of an Ebola spillover in Europe, based on past experience of such events not occurring, it can be “assumed” that the risk is low.

And, yet, it’s this kind of event that has the potential to cause havoc. The National Intelligence Council, which is essentially the US government’s futurism department, describes a spillover pandemic as a black swan event. The writer and former stockbroker Nassim Nicholas Taleb, who developed the theory of black swan events, says that it’s futile to attempt to predict them. Instead, we must prepare for negative ones (and, of course, learn to exploit positive ones).

Infectious spillovers

So what can we do to prevent or prepare for a bushmeat-borne outbreak? First, we can find ways to reduce the occurrence of spillovers, by reducing bushmeat consumption in Africa and the rest of the world. Second, we can develop a strategy to deal with a spillover when it occurs, to stop it from becoming an outbreak.

But before we can start reducing the number of wild animals killed for bushmeat, we need to understand the various answers to one question – why do people eat it?

In rural parts of Africa, people rely on bushmeat for sustenance. Cane rat, duiker and other hunted meat is usually cheaper than farmed meats such as chicken and mutton. That is why the transition from eating wild meat to domestic meat hasn’t happened in many places in West and Central Africa. “To grow domestic animals is quite difficult,” says Michelle Wieland of the Wildlife Conservation Society. “There is no pasture. There are a lot of tsetse flies.”

“In a small town in Central Africa, a mother must make a choice whether to spend the little she has to buy a quarter kilogram of chicken or one kilogram of bushmeat,” she adds. “People prefer to eat fish and wild animals, because they are almost free.”

However, in the right situation and with help from governments, some places have made that transition. “In Cameroon, ten years ago, they were emptying the forests. Every corner you turned, there were hunting camps. When I went back this year, there weren’t any,” says Liz Greengrass of the Born Free Foundation. “There are many reasons. These areas were probably over-harvested. There is better law enforcement today. Many have turned to cocoa farming.”

Beyond accessibility and affordability, there’s a more nuanced, human side to what we choose to eat. “Most people prefer eating what they’ve grown up eating,” says Greengrass. She believes that a lot of demand comes from those who were born in rural areas and then migrated to African cities or even to the West. Hence, in urban Africa and in the rest of the world, bushmeat is generally treated as an exotic food and commands a higher price than farmed meat.

Though in absolute terms the amount of bushmeat consumed beyond rural Africa is small, its price is fuelling the proliferation of professional hunters. A cane rat in Londoncan cost more than £30. A monkey in France can cost more than €100. The prices in the home country can be less than a tenth of those commanded in the West.

“Commercial hunters can make huge amounts of money,” says Greengrass – some well over $1,000 a month, many times the average monthly income of a citizen of a West or Central African country.

And, from the perspective of conservation, Michelle Wieland believes that hunting for trafficking purposes ­– feeding people in cities or sending the meat internationally – is a bigger problem than people consuming bushmeat to get enough protein to survive. A2008 report estimated that more than 1 million tonnes of wildlife is eaten in Africa, which is forcing many species towards extinction.

“Individuals bring [bushmeat] back [to the West] for personal use or for family and friends,” says Jenny Morris of the Chartered Institute of Environmental Health, the professional body of environmental health workers. “What’s less clear is how much of a commercial trade there is. Because it is a high-value product and it isn’t allowed to be sold, there is commercial trade in it, but proving that is much harder.”

Seizing illegal meat in the UK

In 2012, a BBC investigation found that butchers at Ridley Road Market in London were selling bushmeat. It wasn’t on display, but asking nicely could get you a cane rat, a larger cousin of a house rat that is found in West Africa and considered a delicacy there. The investigation also revealed that between 2009 and 2012, despite having been made aware of the sale of illegal meat, environmental health officers had only made two enforcement visits. Worse, none of the shops had had their licences revoked. (The local council says that the number of enforcement visits since 2012 has gone up considerably.)

One of the biggest issues around the international bushmeat trade is that we don’t have a good idea of how big the problem really is. In the UK, the Department for Environment, Food and Rural Affairs (DEFRA) publishes annual reports about seizures of illicit goods entering the UK. In 2014, it caught some 40 tonnes of meat from across the world. However, it doesn’t say how much of that was bushmeat. (I received no response from DEFRA about why they don’t specify what type of meat is seized. The UK Border Force declined to share any information.)

It is estimated that only 10 per cent of the bushmeat that comes to the UK is stopped at the border.

We also don’t know what the bushmeat being seized actually is. “Currently, it’s seized, it’s bagged, and then incinerated before it even formally enters the UK, without anybody inspecting it for species or pathogens,” says Rob Ogden. In 2005, Ogden, now President of the Society for Wildlife Forensic Science but then part of a company he set up called Wildlife DNA Services, convinced the UK government to do something about the bushmeat problem. “Look, we said, we’d like to know what’s coming in,” he remembers.

With help from Her Majesty’s Revenue & Customs and DEFRA, Ogden and his colleague Ross McEwing began their work. “We went to Heathrow. Set up a lab. Got a sniffer dog to look at passenger luggage and pick up any kind of food products. Then from those samples we extracted DNA and sequenced it.”

Their 2007 report analysed 230 meat samples. Seven were recognised as wild meat (four pangolins, one marsh buck, one cane rat and a wild pig species). They even analysed some samples bought by local authorities in London markets with help from the Food Standards Agency (FSA). All three of these samples were cane rat. (A full copy of the report was kindly provided to me by Ogden.)

Following the report, Ogden convinced the FSA to develop a standardised method to detect wild meats. But then the government’s interest declined and, as far as he knows, it’s never been used.

“I don’t think [officers] are routinely going to markets and trying to identify illegally sold wild meat, or testing it even when they are seizing it. When they know it’s illegal, they have grounds to confiscate it and send it for incineration. It rarely goes to prosecution. If they don’t need to know the details at the species level to confiscate it, then they are unlikely to test it,” Ogden says.

A 2013 DEFRA report backed up his claim, stating that “no laboratories have carried out any bushmeat or exotic meat analyses owing to lack of demand from [local authority] clients”.

The 2008 recession also had an effect. “Especially after the financial crisis, every department we’ve talked about has been abolished or contracted,” Ogden says. “There aren’t resources for doing things that aren’t immediately and directly the responsibility of a department.”

Bushmeat also suffers another bureaucratic hurdle – because multiple government departments are involved in wildlife trade, the responsibilities around managing bushmeat are also split. DEFRA deals with international bodies that set wildlife trade regulations, for example; the Home Office deals with border security to confiscate wild meat moving through ports and airports; the FSA works with local authorities to stop the sale of bushmeat, and so on.

For Europe as a whole, the most recent estimate of the size of the illegal bushmeat market comes from a study of seizures made at Charles de Gaulle airport in Paris in 2010. Marcus Rowcliffe of the Zoological Society of London and his colleagues confiscated nearly 200 kg of bushmeat during those seizures. With the help of statistical analysis, Rowcliffe and his colleagues estimated that about five tonnes of bushmeat enters Europe every week.

“The volume and nature of import and trade suggests the emergence of a luxury market for African bushmeat in Europe. Imports are supplying an organized system of trade and are not solely being brought for personal consumption,” Rowcliffe and his colleagues wrote in their study. “This is indicated by the large size of many individual bushmeat consignments, and the presence of traders within Paris who are able to supply bushmeat to order.”

Reports suggest an operation held in Belgian airports in 2013 caught similar amounts of bushmeat, which indicates that the international trade is still rife. However, there haven’t been any more recent estimates. Rowcliffe told me that he tried to update his own analysis from 2010 but found that governments either didn’t have the data or weren’t willing to share.

Without data, and without governments having the appetite and commitment to get more, it’s hard to know the scale of the problem of illegal bushmeat smuggling. But one way to reduce it – and the risk of a spillover – no matter where it’s happening, is to find a sustainable source for the ‘wild’ species people have a taste for.

At the Experimental Burger Society in London, you can get a taste of exotic meats without the attendant risks, thanks to a supplier called Freedown Food. The company told me that they comply with all UK and European regulations. Their list includes crocodile from Namibia, ostrich from Spain, halal bison from Canada, and zebra and antelope from South Africa.

Even some countries known to be hotspots for bushmeat are looking at this kind of option. For example, the Ghanaian delicacy of cane rat is being farmed in Accra, the capital of the country, for its urban residents. Other common species of bushmeat, such as duikers, porcupines and squirrels, could also potentially be farmed, and perhaps lessen the demand for endangered bushmeat species such as apes, monkeys, elephants, pangolins and big cats. It’s possible too that city dwellers would be happy to pay a little extra to know that the animals on their plates were treated well and are disease-free.

Who takes charge?

The reality is that, even with greater support from governments and more sustainable ways of meeting demand for ‘wild’ species, the bushmeat trade is unlikely to stop completely. Rural consumption in West and Central Africa is impossible to regulate. And, like the illegal drug trade, there will always be people willing to pay for certain products and sellers willing to find ways to smuggle them. So, what can we do to prepare for a spillover and prevent it from becoming a full-blown pandemic?

The poorest countries in the world cannot afford to invest much, if anything, in epidemic preparedness and prevention. And, as infectious diseases do not respect borders, a joined-up approach is vital. So, we should be thinking globally, and the obvious candidate to lead on this is WHO

Sadly, WHO is an imperfect candidate. An independent analysis of its response to the 2014 Ebola outbreak found three big problems: a lack of preparation, an underestimation of risks and a lack of money. WHO learned the lessons the hard way and has since worked greatly to improve. The organisation’s response to the 2015 outbreak of Zika, which is a less deadly disease than Ebola but has spread more widely, has been better. WHO sounded the alarm relatively early and used some money from an emergency fund it had created after the Ebola inquiry. Yet, it couldn’t stop the spread of Zika, which has now affected more than 60 countries and territories across South America, North America, Africa and Asia.

Things could have been different if we’d had a vaccine ready for Ebola or Zika. But vaccine development is not WHO’s job. Fortunately, there are a small but growing number of organisations working to fill this crucial gap.

One is the US Centers for Disease Control and Prevention (CDC), which was set up in the 1940s as a malaria-fighting unit. One of its key goals today is to understand emerging infectious diseases. Supporting CDC’s work is the non-profit Global Viral. Since 2003, it has been collecting blood samples from bushmeat hunters across Africa. Its aim is to detect novel viruses and develop early-warning systems to prevent pandemics.

Most recently, in August 2016, the Coalition for Epidemic Preparedness Innovations(CEPI) began its work. It hopes to create vaccine candidates for all emerging infectious diseases and in the priority order that WHO has set out. The premise is simple: vaccines are the best insurance policy you can buy against the next big one.

After spending millennia with wild animals, we are finally understanding more about the invisible, microbial connections that tie us together. While we coexist without problems for much of the time, it only takes one spillover to change the world. We may not be able to predict when and what the next big one will be. But there is one thing we do know. We need to be ready.

This article was first published on Mosaic.com and was co-commissioned by Mosaic and Quartz. Wellcome, the publisher of Mosaic, is a founding partner of CEPI.

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