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What are the origins of novel human infectious diseases like COVID-19?

By EJ Milner-Gulland, Lauren Coad, Yuhan Li, Kelly Malsch, Munib Khanyari, Hollie Booth from the Interdisciplinary Centre for Conservation Sciencem University of Oxford

Originally published the UKRI website

Sunda pangolin. Photo by Dan Challender and Save Vietnam Wildlife

Several of the earliest reported cases of COVID-19 were linked to a wet market in Wuhan city, China, which sold a range of fresh food produce, including wildlife. Although there is not enough evidence yet to say how the new coronavirus jumped from its original host (probably a bat) to humans, there have been previous examples of viruses originating in wild animals causing disease epidemics in people. Understanding the link between wild and domestic animals and COVID-19 is important for managing the current pandemic and future outbreaks of infectious diseases.

Several of the earliest reported cases of COVID-19 were vendors at a “wet market” in Wuhan, China. It has been reported that the virus was first transmitted from an animal host to humans at this market, though this has not yet been proven.[1]

“Wet market” is a term used across various parts of the world, notably in China and Southeast Asia, for a food market in which individual retailers sell fresh products such as vegetables, fruits and fresh meat, providing an essential food source to many. The “wet” here is historically to distinguish from “dry markets” that sell non-perishable goods such as fabrics, electronics, grains, dried food (e.g. dried mushrooms) and household products, and also because of the use of water for cooling the produce and cleaning floors and surfaces. Chinese “wet markets” include some that sell fruits and vegetables in a setting more like a European farmer’s market, while others sell a wider array of meat and live animals, both wild and domestic, often kept in crowded and unhygienic conditions. “Wet markets” have been implicated in SARS (via civets) and H5N1 influenza (“bird flu”) via domestic poultry.[2]

Beyond “wet markets”, a wide variety of other markets that sell live, wild animals operate across the world. The animals sold in these markets can be wild-sourced or captive-bred, for use as food, medicine, pets and ornaments, and the markets are of varying degrees of legality, biosafety, sustainability and social legitimacy. Wildlife markets range from live bird markets for poultry and pets (e.g. in Indonesia, Vietnam and Egypt), to bushmeat markets for subsistence (e.g. in Cameroon and Ghana) to Traditional Chinese Medicine markets (e.g. in China and Singapore). Markets such as these can make substantial contributions to food security and livelihoods. For example, the Chinese Academy of Engineering stated in 2016 that captive-bred wildlife sold for food in China contributed $14 billion to the economy, and employed six million people. The Wuhan market which is at the centre of the COVID-19 outbreak predominately sold seafood, along with other animal products including live, wild and domesticated species for meat.

One proposed route of transmission for COVID-19 involves bats and pangolins, although it is not known whether pangolins were being sold at the Wuhan seafood market at the time. Bats are natural reservoirs of coronaviruses[3]; a pangolin could have been the intermediate host, although the exact route of transmission of COVID-19 to humans remains unknown.[4][5] Further research is needed to be sure of how the virus got into humans, and to understand the role of wildlife and markets in transmission.

Historically, over two-thirds of zoonotic viruses (viruses that are transmitted between animals and humans) have originated in wild animals, most frequently rodents, bats and primates.[6] The transmission of zoonotic diseases primarily occurs when there is close contact between humans and animals. Even dead animals can pass on diseases to people and other animals if their carcasses are fresh and if people consume the meat or handle the dead animals in an unhygienic way. These risks have led to calls for more stringent bio-safety rules in relation to the sale and trade of live animals, as well as calls to stop wildlife being traded in markets altogether. As a result of COVID-19, the Chinese government has now banned farming and trade of almost all terrestrial wild animals for human consumption; only a few species (such as those on the List of Genetic Resource of Livestock and Poultry) are exempt.[7]

While there are clearly disease risks from the wildlife trade, wildlife markets are only one source of infections from animals. Human health is intricately connected to wildlife and their habitats. The destruction of natural forests brings people and wildlife into contact in a way that can promote the spread of zoonotic diseases, such as Nipah virus infection which is carried by fruit-eating bats in Asia.[8][9] In addition, nearly half of all the infectious zoonotic diseases that have emerged in humans since 1940 have come directly from domestic livestock, even if they originated in wild animals.[10] For example, the 2009-10 swine flu pandemic came from domestic pigs. International food supply chains, the movement of people globally, and unprecedented changes in pathogen life cycles due to climate change, further facilitate the conditions for emergence and spread of diseases.[10]

References

  1. Cohen J. Wuhan seafood market may not be source of novel virus spreading globally. Science. 2020 Jan. DOI: 10.1126/science.abb0611.
  2. Webster RG. Wet markets—a continuing source of severe acute respiratory syndrome and influenza? The Lancet. 2004 Jan;363(9404):234-236. DOI: 10.1016/S0140-6736(03)15329-9.
  3. Maxmen A. Bats are global reservoir for deadly coronaviruses. Nature. 2017 Jun;546(7658):340. DOI: 10.1038/nature.2017.22137.
  4. Lam TT, Shum MH, Zhu HC, et al. Identifying SARS-CoV-2-related coronaviruses in Malayan pangolins. Nature. 2020 Mar. DOI: 10.1038/s41586-020-2169-0.
  5. Li X, Zai J, Zhao Q, et al. Evolutionary history, potential intermediate animal host, and cross-species analyses of SARS-CoV-2. Journal of Medical Virology. 2020 Feb. DOI: 10.1002/jmv.25731.
  6. Johnson CK, Hitchens PL, Pandit PS, et al. Global shifts in mammalian population trends reveal key predictors of virus spillover risk. Proceedings B. 2020 Apr;287(1924):20192736. DOI: 10.1098/rspb.2019.2736.
  7. Xinhua News Agency. China’s legislature adopts decision on banning illegal trade, consumption of wildlife. Xinhua Net. 2020 Feb.
  8. Allen T, Murray K, Zambrana-Torrelio C, et al. Global correlates of emerging zoonoses: Anthropogenic, environmental, and biodiversity risk factors. International Journal of Infectious Diseases. 2016 Dec;53(Suppl):21. DOI: 10.1016/j.ijid.2016.11.057.
  9. Epstein JH, Field HE, Luby S, Pulliam JR, Daszak P. Nipah virus: impact, origins, and causes of emergence. Current Infectious Disease Reports. 2006 Jan;8(1):59-65. DOI: 10.1007/s11908-006-0036-2.
  10. Rohr JR, Barrett CB, Civitello DJ, et al. Emerging human infectious diseases and the links to global food production. Nature Sustainability. 2019 Jun;2(6):445-456. DOI: 10.1038/s41893-019-0293-3.

On COVID-19, and rebalancing our relationship with nature

By Hollie Booth, Interdisciplinary Centre for Conservation Science, University of Oxford

Originally posted on the Interdisciplinary Centre for Conservation Science

2020 was supposed to be a super year for nature. Instead we got a pandemic.

Arguably, it is our strained relationship with nature that got us in to this mess. The evidence is fairly conclusive that the Sars-CoV-2 virus that causes COVID-19 first made its way in to a human vector in a wet market in Wuhan, Hubei Province, China. The original animal reservoir for the virus was probably bats. Available evidence suggests the virus first passed from bats to an unconfirmed intermediary host (maybe pangolins) and then from the intermediary to humans (Fig. 1), probably because someone ate the intermediary host.

Fig. 1. Socio-ecological system of food production

Fig. 1. A simplified schematic of how the socio-ecological system of food production lead to COVID-19 in humans

This zoonotic infection was therefore made possible due to two human follies: first, expanding human populations (and associated agribusiness) into undisturbed ecosystems, leading to the step 1 interface. Secondly, consumption of animals, leading to the step 2 interface. Note I use the word ‘animals’ here, since while many have been quick to point the finger at ‘wildlife trade’ and China’s ‘exotic’ eating habits, domestic animals such as poultry and livestock cannot be entirely ruled out as vectors (as they have been for previous zoonoses). Live animal markets, and inter-mingling of live animal trade with food products, likely doesn’t help.

So, what does this mean for our relationship with nature?

It reminds us how intertwined we are with nature, and how the choices we make about our food systems and broader human-nature relations can have rippling global impacts. COVID-19 evolved in the socio-ecological system of food production in China, which has undoubtedly been influenced by global market forces. It is a co-product of relentless human innovation for consumption and trade, and nature’s relentless capacity for adaption and evolution.

It reminds us that nature is not caring, kind and simply here for our benefit. In certain socio-ecological systems, nature has the capacity to be terrifying and destructive to humans, just as we can reap destruction on nature.

It reminds us how dependent we are on a habitable planet, and that the current globalised economic system is not de-coupled from nature and immutable to its impacts. Rather, our relationship with nature needs to be re-balanced. Some argue that this is sufficient justification for increasing separation of humans and nature, for example through closing wildlife markets in their entirety. Yet this fails to sufficiently acknowledge the complexity and precariousness of human-nature relations. Humans depends on wildlife for food security and livelihoods, just as some species depend, in part, on human use for their survival. This creates a false dichotomy and decoupling of ‘natural’ and ‘human’ systems, yet the two do not operate in isolation, and we are often required to trade one off against the other. As such, stopping use of wildlife would have negative impacts for nature and people. For example:

In turn, this may exacerbate risks to human health due to increased food insecurity, increased interfaces between animal agriculture and undisturbed ecosystems (more of step 1), and potential increases in illegal and unregulated wildlife trade (more of step 2).

Fig 2. Factors that increase the risk of zoonoses are complex and inter-twined

Fig. 2. The factors that increase the risk of zoonoses are complex and inter-twined, changing one aspect of our human-nature relationship will inevitably impact another. Source: UNEP.

Whether to increase regulation of wildlife markets in response to COVID-19 is an open question and requires examining the likely impact of different policies on public health, biodiversity, animal welfare and broader socio-economic issues. Moreover, it requires a critical analysis of the proximate vs. ultimate causes of zoonotic disease emergence. Other factors such as urbanization, population density, socio-economic status and agriculture play major significant roles in zoonotic disease emergence. Interestingly, while many are quick to point the finger at China’s eating habits in this instance, the majority of human infectious diseases emerged for the first time in northerly latitudes, with a hotspot in Europe. As such, regulation of wildlife markets is not a panacea for preventing emergence of zoonoses, it is one piece in the complex puzzle of our human-nature relationship (Fig. 2).

It also reminds us that while nature can be cruel, it can also provide solace during times of distress. With an estimated 2.9 billion people in some form of lockdown, we may not be able to interact with people, but at least we can find solitude in nature (at least we can in the UK, during our ‘one exercise per day’ allowance), and appreciate the simple things in life (Fig. 3). This may provide an opportunity to reconnect with our values, reflect on the sustainability of our choices, and transition towards new ways to live, work and organise the global economy.

Fig. 3. Reconnecting with nature

Fig. 3. Reconnecting with nature can help us to cope with social isolation, and reflect on what’s important

Our relationship with nature got us in to this mess, but it can also get us out of it. On an individual level, for those of us who are lucky enough to be fit and healthy, we can disconnect from the hubbub of our work lives and reconnect with ourselves and nature. On a societal level, we can learn lessons from this tragedy, to reset our relationship with nature, and find creative ways to live more happy and sustainable lives, which can benefit public health, nature and our ever inter-twined socio-ecological system.

[With thanks to Dan Challender, Munib Kahnyari and E.J. Milner-Gulland for their helpful inputs to an earlier draft] 

China’s Announcement on Wildlife Trade – What’s New and What Does It Mean?

By Yuhan Li and the Oxford Martin Programme on the Illegal Wildlife Trade team, University of Oxford

Originally published on the Interdisciplinary Centre for Conservation Science

A “wild” public health issue

Menu of a wild meat restaurant in the seafood market, where civet, bamboo rat and other animals were sold. Photo source: weibo

Menu of a wild meat restaurant in Wuhan Huanan seafood market, where civet, bamboo rat and other animals were sold. Photo credit: weibo

To date, COVID-19 has caused over than 2800 deaths in China and has spread to 50 countries [1,2]. The evidence currently suggests the virus was first transmitted to humans at a seafood market in Wuhan, Hubei province, as many early confirmed cases involved individuals that had contact with this market, and 93.9%(31/33) of environmental samples taken from the western region of the market were found with COVID-19 [3]. In addition to seafood, fresh meat and live wild animals were being sold and slaughtered in this market, and coronaviruses are known to jump from some species (e.g., bat, camel, civet) to people [4]. These indicate that the virus might have stemmed from wild animals on sale at the market [3]. However, the intermediate host of COVID-19 is still unclear at this stage. Following the outbreak, the market was shut down by the government on January 1st, 2020, but the consumption of wildlife in China has drawn unprecedented public attention ever since, both within China and internationally, given the severe public health implications of the outbreak.

On February 24th 2020, China’s top legislature adopted a decision to “thoroughly ban the illegal trading of wildlife and eliminate the consumption of wild animals to safeguard people’s lives and health.” The decision has binding force and it took effect on the same day as its promulgation, i.e., February 24th [5,6].

This article provides a detailed explanation of this decision and is based on discussions within the Oxford Martin Programme on the Illegal Wildlife Trade at the University of Oxford and consultations with Shanshui Conservation Center, based at Peking University in China.

Consumption of terrestrial wild animals for edible uses prohibited

As COVID-19 is assumed to have close links with the consumption of wild animals, the new decision prohibits the eating of terrestrial wild animals, including those that are bred or reared in captivity. Hunting, trading and transporting terrestrial wild animals for the purpose of consumption is also prohibited [6].

This is a big move. Previously, only the 402 species on the List of Wild Animals Under State Priority Conservation were banned from consumption as wild meat in China [7]. However, this list is outdated and does not correspond to the conservation status of some species [8]. Consumption of other wild terrestrial animals was permitted, subject to obtaining appropriate certificates (e.g., hunting, breeding, quarantine, trade) from the government. However, this certification system was sometimes poorly implemented. Buying a certificate and using it for “laundering” of wild-caught animals was possible [9].

Which species which are currently consumed are not included in these new measures?

Although this new ban was quickly celebrated by the media and some in the international conservation community, there are several nuances and exceptions that must be clarified.

  • Aquatic wildlife, expect these banned from edible use by the Wildlife Protection Law (2018), is exempt, because the National People’s Congress (NPC) views “fishing as a natural resource and an important agricultural product, as well as a common international practise” [5]. This means, for example, sea cucumbers and other widely consumed species will continue to be traded under the same rules as before.
  • Wild plants are not included in the ban.
  • Farmed amphibians and reptiles on the List of National Key Protected Aquatic Wild Animals for Farming and the List of National Key Protected Economic Aquatic Animals and Plants Resources, such as the giant salamander, softshell turtle and crocodile, currently can still be consumed, until new regulations from the Ministry of Agriculture are annouced[17].
  • Farmed, terrestrial animals on the List of Genetic Resource of Livestock and Poultry can now be traded for food consumption. A publicly available version of this list can be found in a report to UN Food and Agriculture Organisation, and includes various breeds of pig, chicken, duck, goose, special poultry (e.g., ostrich), cattle, sheep, goat, horse, donkey, rabbit and deer [10]. Mink and raccoon dog are also on the list, possibly due to demand for their pelts. Previously, some species not in the list could be farmed (e.g., civets and bamboo rats) but farming these species is now illegal, if they are to be consumed as food. The Chinese government plans to revise this list and the changes would impact certain species and industries.

What about non-edible uses?

The saiga horns are used in Traditional Chinese Medicine. Photo credit: the Saiga Resource Centre

Saiga horns are used in Traditional Chinese Medicine. Photo credit:  the Saiga Resource Centre

Non-edible use of wild terrestrial animals, such as scientific research, medicinal use, and display, are still regulated by existing laws, such as the Wildlife Protection Law (2018) and the Traditional Chinese Medicine Law (2016) [5]. For example, it remains legal to use processed pangolin scales from a certificated source, or bear bile from legal farms for medical purposes, or stockpiled saiga horn. This means that a substantial number of species of conservation concern are unaffected by the ban.

What about the illegal trade?

Some wildlife trade is already illegal (e.g., tiger, ivory) in China, and the Chinese government has announced it will clamp down further on such trade with “aggravated punishment”, suggesting stronger penalties will be used for illegal wildlife trade. In the existing Criminal Law and its interpretation (2014), if the circumstances are especially serious, life imprisonment or death shall be sentenced [11].

Further details are not currently available but should become clear in forthcoming legislation. Since the rise of COVID-19, the Chinese government has investigated over 600 cases of wildlife crime [12], and hopefully, this greater focus on law enforcement will become the norm.

What about the Chinese public’s views?

"Say No to Wild Meat Consumption", a poster from Shanshui Conservation Center

“Say No to Wild Meat Consumption”, a poster from Shanshui Conservation Center

Since the outbreak of the virus, several Chinese conservation organisations have developed a questionnaire to understand public attitudes and circulated it on Chinese social media (e.g., wechat, weibo), receiving over 100,000 responses. Among the respondents, 88% resided in urban areas, 32% have seen people eating wild animals in the past year, and 96.4% said they supported a ban on consumption of all wild animals. Those against the ban believed that “the industry of some wildlife farming is very mature”, and that  “some wildlife farming can bring income.” In terms of banning all trade in wild animals, including food consumption, medicinal use and others, more than 90% of the respondents expressed a willingness to support this [13]. Whether this is a short-term attitude because of the current situation, and whether it is shared by more rural, less internet-savvy people, remains to be seen.

 

Winners and losers

Certain species will definitely gain from this decision, assuming that it is well enforced. These are terrestrial wild mammal species which are legal to hunt and consume, and which are currently potentially being threatened due to this consumption. Species which fall into this category include civets and bats (both of which, by the way, have been implicated in previous epidemics). Others (particularly aquatic species and those used legally in Traditional Chinese Medicine) will not benefit from this legislation. The crack-down on breaches of existing laws may also help species traded illegally. However, the markets have not been permanently closed as yet, and so the public health, animal welfare and conservation concerns which they produce are still there.

A wild civet. Photo credit to Chinese Felid Conservation Alliance

A wild civet. Photo credit to Chinese Felid Conservation Alliance

People in the farmed wild animal industry could face severe economic losses as a result of this new legislation. Previously, the farming of certain wildlife species was encouraged by the government to help alleviate poverty [14]. The wildlife farming industry is estimated to have created employment for more than 14 million people and worth over £56 billion, with pelt production (e.g., mink, raccoon dog, fox) representing 74.8% and food consumption involving species such as the giant salamander, frog and blue peacock, 24% [15]. The National People’s Congress spokesman stated that local governments should guide these farmers towards other industries and provide compensation for their losses [5]. Meanwhile, what happens to the captive-bred animals remains uncertain, with potential implications for animal welfare.

What next?

Using pangolin scales is still legal in China. Photo credit: Gregg Yan, wikimedia commons

Using pangolin scales is still legal in China. Photo credit: Gregg Yan, wikimedia commons

This decision may be just the start of a series of new pieces of legislation, which authorize provincial and city-level governments to implement their own measures. For example, one day after its promulgation, the Shenzhen government released a draft proposal for regional management, suggesting that the ban on animal consumption might extend to pet animals, such as cats and dogs [16]. The National People’s Congress also plans to revise the Wildlife Protection Law (2018) and other wildlife-related laws this year, which will have a long-term impact. These forthcoming legislative changes will need continued attention and efforts by Chinese NGOs and the public to make sure that the changes are as effective as possible.

It has taken so much human suffering to bring attention to this issue. However, the speed with which this new decision has been taken offers hope that the lessons of COVID-19 will be learned.

Special thanks to Melissa Arias, Dan Challender, E.J. Milner-Gulland, Xuesong Han, Amy Hinsley, Xilin Jiang, Zhi Lu, Xiao Mao, Jessica Philips, Michael ’t Sas-Rolfes, Terry Townshend, Lingyun Xiao, for their valuable comments and edits to this blog. 

References:

[1]      新冠肺炎病例实时地图 Live map of COVID-19 in China. The Paper. /2020-02-28. https://projects.thepaper.cn/thepaper-cases/839studio/feiyan/.

[2]      The world gets ready – Covid-19 is now in 50 countries, and things will get worse. The Economist. 2020/2020-02-28. https://www.economist.com/briefing/2020/02/29/covid-19-is-now-in-50-countries-and-things-will-get-worse.

[3]      China detects large quantity of novel coronavirus at Wuhan seafood market. Xinhua. 2020/2020-02-28. http://www.xinhuanet.com/english/2020-01/27/c_138735677.htm.

[4]      Cohen J. Mining coronavirus genomes for clues to the outbreak’s origins. Science, American Association for the Advancement of Science (AAAS), 2020.

[5]      全面禁止非法野生动物交易 革除滥食野生动物陋习——全国人大常委会法工委有关部门负责人答记者问Interview with the Legislative Affairs Commission of the Standing Committee of the National People’s Congress. Xinhua. 2020/2020-02-28. http://www.xinhuanet.com/politics/2020-02/24/c_1125620750.htm.

[6]      China’s legislature adopts decision on banning illegal trade, consumption of wildlife. Xinhua. 2020/2020-02-25. http://www.xinhuanet.com/english/2020-02/24/c_138814139.htm.

[7]      那些没有且无法被检疫的肉，你真的敢吃吗？Meat without quarantine certificate, you dare to eat? Shanshui Conservation Center. 2020/2020-02-25. http://www.shanshui.org/information/1961/.

[8]      野生动物保护名录，一把刻度模糊的卡尺 Wild animal protection list, a ruler with blurred numbers. Shanshui Conservation Center. /2020-02-28. http://www.shanshui.org/information/1906/.

[9]      养殖技术成熟，就可以开放市场了吗？Can the market be opened if farming techniques are mature? Shanshui Conservation Center. /2020-02-28. https://mp.weixin.qq.com/s/HuguwEKlm35qO80sWpCCwg.

[10]    中华人民共和国农业部 Ministry of Agriculture P R of C. 中国畜禽遗传资源状况Genetic Resource of Livestock and Poultry of China. 2003.

[11]    最高人民法院最高人民检察院关于办理走私刑事案件适用法律若干问题的解释 Interpretations of the Supreme People’s Court and the Supreme People’s Procuratorate on several issues concerning the application of law in handling criminal cases of smuggling. 2014/2020-02-28. http://www.court.gov.cn/shenpan-xiangqing-7081.html.

[12]    新华时评:用法治革除吃“野味”的陋习 Xinhua commentary: use the rule of law to remove the bad habits of eating wild animals. Xinhua. 2020/2020-02-28. http://www.xinhuanet.com/politics/2020-02/24/c_1125620829.htm.

[13]    野生动物修法调查 | 22天，10万份问卷，聊聊这些民间的声音 Survey on the revision of laws on wildlife: 22 days, 100,000 responses, voices from the public. Shanshui Conservation Center. 2020/2020-02-28. http://www.shanshui.org/information/1926/.

[14]    野生动植物产业助力江西省林业精准扶贫 Wildlife industries help poverty alleviation in Jiangxi. 2018/2020-02-28. http://www.forestry.gov.cn/main/5383/20180111/1066442.html.

[15]    中国工程院 Chinese Academy of Engineering. 中国野生动物养殖产业可持续发展战略研究Research on Sustainable Development Strategy of Chinese Wild Animal Farming Industry. 2017.

[16]    关于《深圳经济特区全面禁止食用野生动物条例（草案征求意见稿）》公开征求意见的公告Announcement on the public consultation on the 《Shenzhen Special Economic Zone Regulations on the Comprehensive Ban on Eating Wild Animals (Consultation Draft)》. 2020/2020-02-28. http://www.szrd.gov.cn/szrd_zyfb/szrd_zyfb_tzgg/202002/t20200225_19026852.htm.

[17]    甲鱼等还能吃吗？农业农村部：将进一步明确养殖两栖爬行动物禁食范围 Can softshell turtles still be consumed? Ministry of Agriculture and Rural Affairs: will announce further clarification on farmed reptiles and amphibians. 2020/2020-02-29.http://www.xinhuanet.com/2020-02/27/c_1125634919.htm

Resources

What are the origins of novel human infectious diseases like COVID-19?

Coronavirus: why a blanket ban on wildlife trade would not be the right response