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Cambridge University Science Magazine
HIV, Ebola, and SARS-CoV-2. To most, these will be familiar names, having hit headlines and caused death and suffering worldwide. Aside from that, these viruses also share one common feature — they originated in animals. Diseases transmitted between animals and humans are termed ‘zoonotic diseases’, with The Center for Disease Control and Prevention (CDC) estimating that three quarters of newly emerging infectious diseases originate in animals.

The ongoing COVID-19 pandemic has highlighted the devastating impact zoonotic diseases can have on a society reliant on global trade and travel, forcing us to evaluate how our actions contribute to the prevalence of such diseases.

Potential sources of zoonotic infections are numerous but can be broadly separated into three categories: wildlife, domestic livestock, and pets. All three have a well-documented history of aiding the spread of zoonotic disease and each presents unique challenges to the development of appropriate public health measures.

Paying a Price for a Taste of the Wild?

When a group of children returned to their village with the body of a chimpanzee one day in January 1996, they did not know they were harbingers of death. The remote village, Mayibout 2, in north-eastern Gabon is surrounded by the vast Minkebe forest. Ensuring no valuable protein went to waste, the chimpanzee was cooked and eaten. Within a few hours they developed a fever followed by intense fatigue, rashes, diarrhoea, kidney and liver damage, vomiting, and internal and external bleeding. The World Health Organization (WHO) was called in and the area was isolated for six weeks. Of the 31 people infected, 21 died. Mayibout 2 had just crossed paths with a now infamous zoonotic disease: Ebola, a virulent virus with a fatality rate of up to 90%.

For a disease to jump from animal to human, the two must come into contact. One of the ways these ‘spillover’ events occur is through consumption of wildlife. This was the case with Mayibout 2’s Ebola encounter. With COVID-19, a wet market in Wuhan, China is the pandemic’s suspected ground zero. By definition, wet markets sell fresh produce and animal products, which can include live animals slaughtered on customer purchase. Wet markets can be found around the world and not all sell wildlife. But at those that do, factors including unregulated hygiene standards and the indiscriminate mixing of species both wild and domesticated, sometimes combined with a tropical climate, make for the perfect meeting place for pathogens and humans.

COVID-19’s wide-reaching effects have focused international attention on wildlife consumption and trade as public health issues. In response, many have called for wildlife trade to be banned outright. Others, like researchers at the Oxford Martin Programme, believe this would be a mistake, calling it a ‘knee-jerk and potentially self-defeating measure’ in a recent Conversation article.

While wildlife trade is a key driver of biodiversity loss and species decline, the reality is that wildlife trade, both legal and illegal, is an extremely nuanced issue and debates around its prohibition must take this into account. When Elizabeth Maruma Mrema, the acting United Nations Biodiversity Chief, called for prohibitions on wet markets in April, she cautioned against the unintended consequences of reactionary bans on the millions of people dependent on wild animals for their livelihoods.

Wildlife trade is often perceived solely as the selling of exotic animals harvested from wild places in tropical countries, but in reality it is more complex, encompassing a wide range of species, ecosystems, and localities. These include marine and freshwater fish, fungi and medicinal plants, and game including rabbits, deer, and various bird species. Wildlife trade also encompasses various production types, including wild-caught, captive breeding, and farming of wild species. The scale of the industry is evidenced by its value: an estimated US$188 – 300 billion annually.

International trade is regulated by the Convention on Trade In Endangered Species (CITES), a voluntary multilateral agreement that classifies species into categories that dictate various restrictions on their trade. However, despite these efforts, illegal wildlife trade (IWT) is a profitable industry valued at between US$7 – 23 billion annually, and remains a threat to biodiversity. IWT is recognised as organised crime, and is often linked to drugs, arms, and human trafficking via complex transnational networks.

Recreational hunting and expensive tastes for exotic wildlife products as symbols of status and wealth fuel both legal and illegal wildlife trade all over the world. According to environmental science news platform, Mongabay, ‘an estimated 40 tonnes of bushmeat is flown into Geneva and Zurich airports every year’, the former ironically being the city home to the CITES convention. Illegal wildlife products are also seized at the borders of other European countries and the US. These consumers represent a lucrative end point for wildlife poachers and traffickers who answer consumer demands with supply.

For these consumers, wildlife consumption is a choice, but this is not the case for everyone. Many indigenous and rural communities around the world, such as the villagers of Gabon’s Mayibout 2, rely on bushmeat as an affordable source of protein. A blanket ban would mean disaster for the food security of these communities, who may have few alternatives. Charles Emogor, a PhD student at the University of Cambridge studying the pangolin in Nigeria, draws attention to the socioeconomic considerations of a ban: ‘How are you going to supplement the income levels of people who depend on wild meat? I work with hunters and see them buy clothes and food from hunting — it is a way of life’.

Wildlife trade is an economic opportunity for many. A June 2020 New York Times article recounts the story of Mao Zuqin, whose bamboo rat farm in China lifted him out of destitution. The chubby bamboo rat is a wild species, the farming of which has been encouraged by the Chinese government in poverty alleviation efforts. However, in the wake of the government’s ban on wildlife consumption in response to the COVID-19 outbreak as many as 100,000 people have seen their businesses become illegal overnight. At the time of writing, whether the ban (which conveniently left loopholes for the medicinal use of some animals like the pangolin) will stick remains to be seen.

A complicated web of legal and illegal activity at different scales, wildlife trade is driven by a range of people harbouring a myriad of motivations. The difference in socioeconomic status between those at the start versus the end of the supply chain can be staggering. Understanding motives of the people along this chain is a vital consideration in effectively controlling trade. A blanket ban on wildlife trade without dealing with its root causes may simply drive trade underground, where it is harder to regulate. It would also make enforcing welfare and hygiene standards more difficult, the latter a crucial factor for disease prevention. Supposed “quick-fix” bans instituted without behavioural change efforts and increased enforcement will likely be ineffective.

This is not to deny that illegal, unsustainable trade and conditions that are unhygienic and highly stressful for animals should be prevented. However, reactionary a blanket ban may fail to accommodate those who consume wildlife or engage with its trade not out of choice, but out of need, like the people of Mayibout 2 in Gabon and the bamboo rat farmers of China. The voices of these stakeholders must be heard at policy level to avoid backlash at community level and to ensure regulations are relevant to the real-world context.

Wildlife consumption is just one of many ways zoonotic diseases can be introduced to humans. Since the 1940s, more than half of zoonotic outbreaks have been linked to agricultural intensification, expanding land use, and escalating livestock production. Humans’ intensifying encroachment on natural habitats results in increasing contact with wild species and the diseases they may carry. For example, Malaysia’s 1998 Nipah virus outbreak is thought to have been caused by bat migration into orchards in response to slash and burn agriculture. Using domesticated pigs as an intermediate host, Nipah virus jumped from bats to humans, causing over 100 deaths.

Many may view outbreaks of zoonotic disease as the result of foreign practices in ‘exotic’ places. However, they may not realise that these outbreaks can originate from common farmed meats available at the local supermarket.

Could an Appetite For Animals Trigger the Next Pandemic?

With recent media coverage focusing on the risk of zoonotic disease from wet markets, it can be easy to overlook the risk that other diets pose. Humans farm various livestock all over the world for food. Even though these animals are not wild, our interactions with them still put us at risk of disease outbreaks of pandemic proportions.

Global consumption of meat such as poultry and beef has increased rapidly over the past 50 years as diets have changed from those based primarily on cereals to an increasingly protein-rich diet, with farmed livestock as a key component. It is estimated that in Western Europe 80–90 kg of meat is consumed per person annually. This increasing demand for cheap and abundant meat has seen a rise in factory farming practices across the globe, with close to 2,000 industrial-sized pig and chicken farms now operating in the UK.

Conditions in factory farms are a virus’s dream. Cramped conditions housing many thousands of animals provide ample opportunities for infection. Viral spread is aided by the often identical genetic makeup of factory farm animals. Selective breeding for desirable characteristics such as larger chickens has seen the generation of breeds which grow four times faster than a typical chicken from the 1950s. While this leads to an increased meat yield, selective breeding also reduces the genetic variation within the flock. Variation within a population helps to slow the spread of disease. A virus which can infect one individual may encounter stronger immune defences in the next, preventing infection and thus, spread of disease. However, if animals are genetically identical, when a virus mutates such that it can successfully infect one chicken in the farm, it can quickly spread through the rest. Furthermore, substandard living conditions, such as concrete floors used in some pig farming, can impair natural instincts like foraging. Denying animals these evolutionary behaviours can result in stress-induced immunosuppression, rendering them more vulnerable to infection.

We do not need to look back very far to find a pandemic which highlights the risk of zoonotic disease transmission from farmed animals. In early 2009, an outbreak of H1N1 influenza A in pigs, ‘swine flu’, was transmitted to humans in Mexico and quickly spread throughout North America and the rest of the world. Before the introduction of a vaccine in late 2009, this pandemic was estimated to have infected around 11–21% of the world’s population. Over 17,000 deaths were confirmed, with some models estimating a death rate of over 150,000 people worldwide in the year following the start of the outbreak.

H1N1 is an influenza A virus made up of eight segments of viral RNA, which carry the information needed to allow the virus to survive and replicate within the cells of an infected animal. As the virus multiplies, small mistakes can be introduced into this RNA. Over time, these mutations can lead to the creation of a viral strain which differs enough from the original strain that the immune system can no longer recognise and fight it. Influenza A can also undergo more striking changes, where two or more viruses can exchange segments and form a new ‘mosaic’ virus. This is known as ‘antigenic shift’. Strains which arise from this antigenic shift are more likely to cause pandemics. Not only does the change happen suddenly but it is often a significant change, meaning there is little chance of pre-existing immunity in the population.

Pigs are particularly well placed to host antigenic shifts and are often referred to as ‘mixing vessels’ due to their susceptibility to infections by both avian and human viruses. This means that if a pig is infected with a human, avian, or swine influenzas at the same time, these viruses could combine to form a new strain of virus which is capable of crossing the species barrier and infecting a new host species. In work published in Nature, researchers traced the family tree of the H1N1 strain responsible for the 2009 pandemic, showing that it was made up of multiple influenza A strains that had been circulating amongst pig farms in North America and Eurasia for decades. The journey of these viruses to Mexican pig farms, where they eventually recombined to form the 2009 strain, follows the movement of live pigs across continents for global trade. The worldwide trade of any live animals, whether wild or domesticated, increases the chances of bringing viruses together with the potential to form a deadly strain.

With the Food and Agriculture Organization of the United Nations stating in a 2013 report ‘livestock health is the weakest link in our global health chain’, it is evident that to prevent future pandemics livestock populations must be prioritised. In the wake of the 2009 H1N1 pandemic, Dr Garcia-Sastre, director of the Icahn School of Medicine’s Center for Research on Influenza Pathogenesis, told Science Daily, ‘We need to monitor the viruses that are circulating, and try to stop mixing influenza strains from different geographic locations’. The importance of such screening is underscored by the results of influenza virus surveillance of pigs in China during 2011–2018. Published in the Proceedings of the National Academy of Sciences in June, the results show that a new strain of H1N1 with the potential to infect humans has been circulating in pigs since 2016. Early warning of the emergence of strains with epidemic potential is vital for preventative measures.

There are multiple strategies already employed to reduce the risks of an outbreak. These measures include quarantining of new animals and extensive hygiene training of staff as well as the development of vaccines for both livestock and humans. Other innovative research could see the development of transgenic livestock which has been genetically modified so that it is unable to spread disease or, better still, become infected in the first place.

The rapid growth of factory farming is juxtaposed with an increasing interest in a more plant-based diet. A survey conducted by the Vegan Society reported that more than 20% of Britons have reduced their meat consumption during the COVID-19 lockdown, citing reasons such as reduced meat availability in supermarkets as well as health, environmental, and animal rights concerns. A recent report, carried out by a team of global experts, made more than 100 suggestions of how to reduce the risk of another pandemic, including adoption of a more plant-based diet. Reduced demand for both wildlife and domestic farming could lead to a decreased need for the agricultural intensification of the past decade, in turn lessening the risk of disease spillover from animals to the human population.

From factory farms to homeowners with their own flocks of chickens and everything in between, there is no denying the risk that while our attention is focused on wet markets, the next pandemic virus could be making its way into existence in farm animals.

A further human interaction with animals that may be overlooked is right within our own homes. The risk of zoonotic transmission from pets gained traction in light of the COVID-19 pandemic when at one point it was thought that pets may be able to spread the virus to their owners.

Zoonotic Diseases Hidden Right Under Our Noses?

As revealed through photos of dogs donning face masks during the COVID-19 pandemic, pets are important parts of many people’s lives. Dogs and cats have been close companions of ours for more than 10 millennia, gaining their present status as pets, or more fondly as family members, within households in modern society. The global trade in wildlife is estimated to be worth US$30.6–42.8 billion annually, of which approximately US$22.8 billion is legal and substantially driven by the global demand for pets. In fact, about 50% of adults in the UK own a pet, with 26% of UK adults owning dogs and 24% owning cats.

However, like their wild counterparts, common household pets can also be carriers of various viral diseases. Rabies infections are among the most commonly known of these diseases, accounting for anywhere between 30,000-70,000 deaths annually worldwide, the majority of which are caused by dog bites in developing countries. Although rabies among domestic dogs in the developed world is largely under control, more than 99% of human rabies infections continue to be canine-related in many other parts of the world.

In 2008, a fisherman landing on the Bali peninsula of Indonesia unknowingly introduced a rabies epidemic to the island by bringing his dog who was incubating the virus, leading to over 130 human deaths. Although Bali was historically rabies-free until 2008, activities such as pet trade and dog adoption between countries can lead to the accidental emergence or re-emergence of the virus, even in countries that have eradicated canine rabies.

Dogs are just the tip of the iceberg. Many small pet animals can also carry diseases transmittable to humans, including reptiles and rodents. One of the most popular choices for small pets is the Syrian or golden hamster. A survey by the American Veterinary Association in 2012 suggested that more than a million individuals owned pet hamsters in the US.

Golden hamsters were carriers of the lymphocytic choriomeningitis (LCM) virus, which infected 48 lab staff at the University of Rochester Medical Center between 1971–1973. Dozens of pet hamster-associated LCM cases have been identified since, with 181 cases being reported within three years in the US during the mid-1970s, prompting the release of a national alert by the CDC. This marked the adorable household pet as a major link to human disease, largely through airborne infection.

In humans, LCM can lead to severe symptoms, such as brain inflammation and other neurological symptoms. While human-to-human transmission of the LCM virus appeared to be rare, a disturbing development in 2005 surfaced — a severe and most often fatal LCM was identified among transplant patients. Four organ recipients had their LCM traced back to transmission from an organ donor who kept golden hamsters as pets. These pets were later found to have been sourced from the same commercial hamster breeding and distribution location where the outbreak began. As alarming as that is, LCM virus transmission through solid organ transplant continues to be a rare phenomenon, albeit a formidable one.

It is no surprise that the exotic pet trade also comes with similar risks. The term ‘exotic pets’ does not have a set definition, but here it refers to animals that are non-native to a region and can be domesticated or wild.

Ownership of these pets have been on the rise since the 2007 modification to The Dangerous Wild Animals Act (1976). Previously, owners had to acquire licenses to keep specific exoctic species as pets in the UK. However, this requirement was removed for some species on the list. As a result, the increased convenience of owning these exotic animals encouraged the trade and led to the emergence of new zoonotic infections.

An example of these infections is the 2003 outbreak of human monkeypox in Texas. This disease was previously unrecorded in the Western hemisphere. It was brought over by an international shipment of pet prairie dogs from Ghana to Texas. In Wisconsin, the first case was a three-year-old girl who was bitten by her infected pet prairie dog and was sent to hospital with monkeypox symptoms. Eventually, 80 other patients fell victim to the disease. According to the WHO, although monkeypox was once considered a rare disease confined within remote rainforests in central and western Africa, it is now the most important orthopoxvirus infection in humans following the eradication of the closely related smallpox virus.

Outside of the home, several zoonotic outbreaks have also been linked to zoos, particularly petting zoos where visitors can freely approach and feed animals. Animal exhibits were associated with over 25 outbreaks of human infectious diseases between 1990–2000 alone. For example, the Komodo dragon at a Colorado Zoo was the starting point for a salmonella outbreak in 1996 with 65 cases identified, in which most patients were children. Surprisingly, it had nothing to do with directly interacting with this near-mythical beast itself — it was associated with touching the wooden barrier around its exhibit.

These are all nightmarish cases, but are also relatively rare and preventable. Similar to livestock, adequate surveillance and control policies for breeding facilities, distribution centres, and laboratories can lower the risk of human infection. For example, periodic testing of these animals may lead to early identification of potential infections, before animal-to-human transmission occurs.

On an individual level, maintaining basic hygiene practices such as proper handwashing can keep owners and pets healthy. Bringing pets to the vet for regular check-ups, tests, and vaccinations can also be great opportunities to ask and learn more about the risks involved with having pets, how to responsibly care for them, and how to appropriately deal with their waste products. This is especially important to consider for the young, elderly, and immunocompromised, who may be more prone to infection.

Despite the risks of zoonotic infections, pets continue to hold a special place in many of our hearts. Taking appropriate precautions can decrease the risk of transmission of zoonotic illnesses, allowing us to safely enjoy our companionship with animals.

Across the globe, we rely on animals for food, companionship, and survival. Our interactions with them — be it pangolins, pigs, or pets — provide a myriad of benefits, but if unregulated may also plague us with disease. We are quick to vilify specific species or people in the wake of a pandemic, but it is up to all of us to safely mediate our interactions with nature. Investing in understanding the mechanisms through which zoonotic diseases spillover, taking steps to minimise those risks and prevent indiscriminate natural resource use will protect us and the flora and fauna around us. Our collective survival depends on this finely balanced co-existence. Zoonotic diseases have the power to take thousands of lives, cause widespread panic, immense economic loss, and shake the world to its core. In all this destruction, perhaps there is one seed of hope — an opportunity for us to review our relationship with the natural world and with each other.

Article by Tatjana Baleta, Hazel Walker, and Anna Tran. Artwork by Rianna Man.