The role live animal markets and the trade in exotic animals have played in the emergence of deadly coronavirus outbreaks.
The SARS Coronavirus and Wet Markets
Below is an approximation of this video’s audio content. To see any graphs, charts, graphics, images, and quotes to which Dr. Greger may be referring, watch the above video.
SARS was the first new global disease outbreak of the 21st century, which went on to cause about 8,000 cases and about 800 deaths. Many of the first cases of SARS were tied to the same kind of place most of the first cases of COVID-19 were linked to: live animal “wet” markets in China.
Freshly slaughtered animals are thought to be more nutritious by many regional consumers, and some seek ye-wei, the “wild taste,” believing the consumption of exotic animals bestows benefits to health and social status. This convergence—fresh slaughter with exotic animals—leads to a perfect storm for disease transmission, where crowded cages in these wet markets are contaminated with the blood, urine, and feces of countless species mixed together in a potential cauldron of contagion.
There was a vast expansion of the wildlife trade in the 1990s to supply the emerging urban middle-class demand, driven, according to the World Bank, predominantly by demand for wild animal products in China. Many of the wild animals, typically while alive, enter China through Vietnam from Laos, where the wildlife meat trade rose to become the second-largest income source for rural families. Markets there sell a ton of animals (literally), many of which are critically endangered.
Then, as demand surpassed supply, the cross-country wildlife trade was supplemented with the creation of intensive captive production farms, where a menagerie of wild animals are often raised under poor sanitation in unnatural stocking densities before being transported and caged at markets for sale. Fourteen million people are involved in China’s wildlife farming industry, valued at 74 billion dollars.
The genetic building blocks for the SARS virus have since been identified from 11 different strains of coronaviruses found in Chinese bats, but there are bat-borne coronaviruses around the world. The reason China in particular has been ground zero for multiple jumps of deadly human coronavirus epidemics may be because of these wet markets.
In the case of SARS, the intermediate host appeared to be the masked palm civet, a cat-like animal prized for its meat. In addition to being raised for their flesh, civet cat penis is soaked in rice wine for use as an aphrodisiac. These animals also produce the most expensive coffee in the world. So-called fox-dung coffee is produced by feeding coffee beans to captive civets and then…recovering the partially digested beans from their feces. I don’t know if you can see, but those are actually civet turds. “A musk-like substance of buttery consistency secreted by the anal glands gives the coffee its characteristic flavor and smell.” One might say this unique drink is good to the last dropping.
Coronaviruses acquired from civets in live animal markets were almost identical to the SARS virus. While civets at wildlife farms supplying the live markets were found largely free of infection, up to 80 percent of sampled civets at the markets showed evidence of exposure. This suggests that most infections happened at the market, perhaps due to a combination of crowded interspecies mixing and the immunosuppressive effect of stress.
Live animal markets not only allow for cross-species transmission, viral amplification, and human exposure, but viral modification too. The SARS coronavirus exploited opportunities provided by wet markets in southern China to adapt to the palm civet and human. Apparently, civets were not just passive conduits for the virus; they appear to be incubators for human-adapting mutations in the virus itself.
The virus uses its corona of spikes like a key in a lock to latch onto host receptors to gain entry into its victims’ cells. To switch from infecting one species to another, the genes that code for the spikes have to mutate to fit into the new host’s receptors. A new lock requires a new key.
Both the SARS coronavirus and SARS coronavirus 2, the virus that causes COVID-19, attach to a specific enzyme coating the cells of our lungs. By the time a mishmash of bat coronaviruses made it into civets, the docking spikes of the virus were only two mutations away from locking in the configuration that bound to human receptors, and then the human-to-human SARS epidemic was born.
After the initial SARS outbreak ended in 2003, new human cases were confirmed, tied to a restaurant serving civets. Unlike most of the previous cases, the new victims presented with mild symptoms, and didn’t seem to pass it on. Viruses sampled from palm civets at both a local market and the restaurant were found to be nearly identical to those discovered in the new, milder human cases. The new civet viruses shared only one of the two civet-to-human spike mutations found in all of the new human patients, but none of the previous year’s civet’s coronaviruses. These findings suggest that intermediate hosts can help transform coronaviruses from the primordial reservoir in bats into greater human infectivity.
Yes, bats are trapped for meat in Asia, and many bat hunters do report getting bitten. Yes, the handling and consumption of undercooked bat meat is still practiced in China, Guam, and other parts of Asia. But it appears intermediate hosts may be needed as a stepping stone for bat coronaviruses to adapt to humans to trigger a human pandemic. And it’s hard to imagine a system that could be better designed to facilitate this process than a live animal wet market.
In response to the SARS outbreak, the Chinese government implemented strict controls over the wildlife market, including a ban on the sale of civet cats. Though the permanent closure of live animal markets has been called the “strongest deterrent to another zoonotic disease outbreak,” within months, the ban was lifted, and trade resumed as before. Civets were back on the menu.
Had authorities in China learned its lesson from SARS and listened to experts and enacted a permanent ban on live animal markets, it’s possible humanity would not now be suffering the worst pandemic in a century.
Please consider volunteering to help out on the site.
- To KK, Hung IF, Chan JF, Yuen KY. From SARS coronavirus to novel animal and human coronaviruses. J Thorac Dis. 2013;5 Suppl 2:S103-8.
- Xu RH, He JF, Evans MR, et al. Epidemiologic clues to SARS origin in China. Emerging Infect Dis. 2004;10(6):1030-7.
- Li Q, Guan X, Wu P, et al. Early Transmission Dynamics in Wuhan, China, of Novel Coronavirus-Infected Pneumonia. N Engl J Med. 2020;382(13):1199-207.
- Fan Y, Zhao K, Shi ZL, Zhou P. Bat Coronaviruses in China. Viruses. 2019;11(3).
- Field HE. Bats and emerging zoonoses: henipaviruses and SARS. Zoonoses Public Health. 2009;56(6-7):278-84.
- Malta M, Rimoin AW, Strathdee SA. The coronavirus 2019-nCoV epidemic: Is hindsight 20/20?. EClinicalMedicine. 2020;20:100289.
- Bell D, Roberton S, Hunter PR. Animal origins of SARS coronavirus: possible links with the international trade in small carnivores. Philos Trans R Soc Lond, B, Biol Sci. 2004;359(1447):1107-14.
- Going, going, gone …The illegal trade in wildlife in East and Southeast Asia. World Bank. 2005.
- Duckworth JW, Salter RE, Khounboline K. Wildlife in Lao PDR: 1999 status report. Vientiane: IUCN-The World Conservation Union, Wildlife Conservation Society, Centre for Protected Areas and Watershed Management. 1999.
- Greatorex ZF, Olson SH, Singhalath S, et al. Wildlife Trade and Human Health in Lao PDR: An Assessment of the Zoonotic Disease Risk in Markets. PLoS ONE. 2016;11(3):e0150666.
- Arranz A, Huang H. China’s wildlife trade. South China Morning Post. March 4, 2020.
- Hu B, Zeng LP, Yang XL, et al. Discovery of a rich gene pool of bat SARS-related coronaviruses provides new insights into the origin of SARS coronavirus. PLoS Pathog. 2017;13(11):e1006698.
- Wong ACP, Li X, Lau SKP, Woo PCY. Global Epidemiology of Bat Coronaviruses. Viruses. 2019;11(2).
- Xu Y. Unveiling the Origin and Transmission of 2019-nCoV. Trends Microbiol. 2020;28(4):239-40.
- Jumhawan U, Putri SP, Yusianto, Bamba T, Fukusaki E. Quantification of coffee blends for authentication of Asian palm civet coffee (Kopi Luwak) via metabolomics: A proof of concept. J Biosci Bioeng. 2016;122(1):79-84.
- Guan Y, Zheng BJ, He YQ, et al. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science. 2003;302(5643):276-8.
- Tu C, Crameri G, Kong X, et al. Antibodies to SARS coronavirus in civets. Emerging Infect Dis. 2004;10(12):2244-8.
- Zhao GP. SARS molecular epidemiology: a Chinese fairy tale of controlling an emerging zoonotic disease in the genomics era. Philos Trans R Soc Lond, B, Biol Sci. 2007;362(1482):1063-81.
- Wan Y, Shang J, Graham R, Baric RS, Li F. Receptor Recognition by the Novel Coronavirus from Wuhan: an Analysis Based on Decade-Long Structural Studies of SARS Coronavirus. J Virol. 2020;94(7).
- Qu XX, Hao P, Song XJ, et al. Identification of two critical amino acid residues of the severe acute respiratory syndrome coronavirus spike protein for its variation in zoonotic tropism transition via a double substitution strategy. J Biol Chem. 2005;280(33):29588-95.
- Wang M, Yan M, Xu H, et al. SARS-CoV infection in a restaurant from palm civet. Emerging Infect Dis. 2005;11(12):1860-5.
- Song HD, Tu CC, Zhang GW, et al. Cross-host evolution of severe acute respiratory syndrome coronavirus in palm civet and human. Proc Natl Acad Sci USA. 2005;102(7):2430-5.
- Holmes KV. Structural biology. Adaptation of SARS coronavirus to humans. Science. 2005;309(5742):1822-3.
- Sheahan T, Rockx B, Donaldson E, Corti D, Baric R. Pathways of cross-species transmission of synthetically reconstructed zoonotic severe acute respiratory syndrome coronavirus. J Virol. 2008;82(17):8721-32.
- Nahar N, Asaduzzaman M, Mandal UK, et al. Hunting Bats for Human Consumption in Bangladesh. Ecohealth. 2020;17(1):139-51.
- Chan JF, To KK, Tse H, Jin DY, Yuen KY. Interspecies transmission and emergence of novel viruses: lessons from bats and birds. Trends Microbiol. 2013;21(10):544-55.
- Ashour HM, Elkhatib WF, Rahman MM, Elshabrawy HA. Insights into the Recent 2019 Novel Coronavirus (SARS-CoV-2) in Light of Past Human Coronavirus Outbreaks. Pathogens. 2020;9(3).
- Zhong NS, Zeng GQ. Pandemic planning in China: applying lessons from severe acute respiratory syndrome. Respirology. 2008;13(Suppl 1):33-35.
- Peeri NC, Shrestha N, Rahman MS, et al. The SARS, MERS and novel coronavirus (COVID-19) epidemics, the newest and biggest global health threats: what lessons have we learned?. Int J Epidemiol. 2020.
- Normile D, Yimin D. Infectious diseases. Civets back on China's menu. Science. 2003;301(5636):1031.
Motion graphics by AvoMedia
Image credit: Mindy McAdams via flickr. Image has been modified.
Below is an approximation of this video’s audio content. To see any graphs, charts, graphics, images, and quotes to which Dr. Greger may be referring, watch the above video.
SARS was the first new global disease outbreak of the 21st century, which went on to cause about 8,000 cases and about 800 deaths. Many of the first cases of SARS were tied to the same kind of place most of the first cases of COVID-19 were linked to: live animal “wet” markets in China.
Freshly slaughtered animals are thought to be more nutritious by many regional consumers, and some seek ye-wei, the “wild taste,” believing the consumption of exotic animals bestows benefits to health and social status. This convergence—fresh slaughter with exotic animals—leads to a perfect storm for disease transmission, where crowded cages in these wet markets are contaminated with the blood, urine, and feces of countless species mixed together in a potential cauldron of contagion.
There was a vast expansion of the wildlife trade in the 1990s to supply the emerging urban middle-class demand, driven, according to the World Bank, predominantly by demand for wild animal products in China. Many of the wild animals, typically while alive, enter China through Vietnam from Laos, where the wildlife meat trade rose to become the second-largest income source for rural families. Markets there sell a ton of animals (literally), many of which are critically endangered.
Then, as demand surpassed supply, the cross-country wildlife trade was supplemented with the creation of intensive captive production farms, where a menagerie of wild animals are often raised under poor sanitation in unnatural stocking densities before being transported and caged at markets for sale. Fourteen million people are involved in China’s wildlife farming industry, valued at 74 billion dollars.
The genetic building blocks for the SARS virus have since been identified from 11 different strains of coronaviruses found in Chinese bats, but there are bat-borne coronaviruses around the world. The reason China in particular has been ground zero for multiple jumps of deadly human coronavirus epidemics may be because of these wet markets.
In the case of SARS, the intermediate host appeared to be the masked palm civet, a cat-like animal prized for its meat. In addition to being raised for their flesh, civet cat penis is soaked in rice wine for use as an aphrodisiac. These animals also produce the most expensive coffee in the world. So-called fox-dung coffee is produced by feeding coffee beans to captive civets and then…recovering the partially digested beans from their feces. I don’t know if you can see, but those are actually civet turds. “A musk-like substance of buttery consistency secreted by the anal glands gives the coffee its characteristic flavor and smell.” One might say this unique drink is good to the last dropping.
Coronaviruses acquired from civets in live animal markets were almost identical to the SARS virus. While civets at wildlife farms supplying the live markets were found largely free of infection, up to 80 percent of sampled civets at the markets showed evidence of exposure. This suggests that most infections happened at the market, perhaps due to a combination of crowded interspecies mixing and the immunosuppressive effect of stress.
Live animal markets not only allow for cross-species transmission, viral amplification, and human exposure, but viral modification too. The SARS coronavirus exploited opportunities provided by wet markets in southern China to adapt to the palm civet and human. Apparently, civets were not just passive conduits for the virus; they appear to be incubators for human-adapting mutations in the virus itself.
The virus uses its corona of spikes like a key in a lock to latch onto host receptors to gain entry into its victims’ cells. To switch from infecting one species to another, the genes that code for the spikes have to mutate to fit into the new host’s receptors. A new lock requires a new key.
Both the SARS coronavirus and SARS coronavirus 2, the virus that causes COVID-19, attach to a specific enzyme coating the cells of our lungs. By the time a mishmash of bat coronaviruses made it into civets, the docking spikes of the virus were only two mutations away from locking in the configuration that bound to human receptors, and then the human-to-human SARS epidemic was born.
After the initial SARS outbreak ended in 2003, new human cases were confirmed, tied to a restaurant serving civets. Unlike most of the previous cases, the new victims presented with mild symptoms, and didn’t seem to pass it on. Viruses sampled from palm civets at both a local market and the restaurant were found to be nearly identical to those discovered in the new, milder human cases. The new civet viruses shared only one of the two civet-to-human spike mutations found in all of the new human patients, but none of the previous year’s civet’s coronaviruses. These findings suggest that intermediate hosts can help transform coronaviruses from the primordial reservoir in bats into greater human infectivity.
Yes, bats are trapped for meat in Asia, and many bat hunters do report getting bitten. Yes, the handling and consumption of undercooked bat meat is still practiced in China, Guam, and other parts of Asia. But it appears intermediate hosts may be needed as a stepping stone for bat coronaviruses to adapt to humans to trigger a human pandemic. And it’s hard to imagine a system that could be better designed to facilitate this process than a live animal wet market.
In response to the SARS outbreak, the Chinese government implemented strict controls over the wildlife market, including a ban on the sale of civet cats. Though the permanent closure of live animal markets has been called the “strongest deterrent to another zoonotic disease outbreak,” within months, the ban was lifted, and trade resumed as before. Civets were back on the menu.
Had authorities in China learned its lesson from SARS and listened to experts and enacted a permanent ban on live animal markets, it’s possible humanity would not now be suffering the worst pandemic in a century.
Please consider volunteering to help out on the site.
- To KK, Hung IF, Chan JF, Yuen KY. From SARS coronavirus to novel animal and human coronaviruses. J Thorac Dis. 2013;5 Suppl 2:S103-8.
- Xu RH, He JF, Evans MR, et al. Epidemiologic clues to SARS origin in China. Emerging Infect Dis. 2004;10(6):1030-7.
- Li Q, Guan X, Wu P, et al. Early Transmission Dynamics in Wuhan, China, of Novel Coronavirus-Infected Pneumonia. N Engl J Med. 2020;382(13):1199-207.
- Fan Y, Zhao K, Shi ZL, Zhou P. Bat Coronaviruses in China. Viruses. 2019;11(3).
- Field HE. Bats and emerging zoonoses: henipaviruses and SARS. Zoonoses Public Health. 2009;56(6-7):278-84.
- Malta M, Rimoin AW, Strathdee SA. The coronavirus 2019-nCoV epidemic: Is hindsight 20/20?. EClinicalMedicine. 2020;20:100289.
- Bell D, Roberton S, Hunter PR. Animal origins of SARS coronavirus: possible links with the international trade in small carnivores. Philos Trans R Soc Lond, B, Biol Sci. 2004;359(1447):1107-14.
- Going, going, gone …The illegal trade in wildlife in East and Southeast Asia. World Bank. 2005.
- Duckworth JW, Salter RE, Khounboline K. Wildlife in Lao PDR: 1999 status report. Vientiane: IUCN-The World Conservation Union, Wildlife Conservation Society, Centre for Protected Areas and Watershed Management. 1999.
- Greatorex ZF, Olson SH, Singhalath S, et al. Wildlife Trade and Human Health in Lao PDR: An Assessment of the Zoonotic Disease Risk in Markets. PLoS ONE. 2016;11(3):e0150666.
- Arranz A, Huang H. China’s wildlife trade. South China Morning Post. March 4, 2020.
- Hu B, Zeng LP, Yang XL, et al. Discovery of a rich gene pool of bat SARS-related coronaviruses provides new insights into the origin of SARS coronavirus. PLoS Pathog. 2017;13(11):e1006698.
- Wong ACP, Li X, Lau SKP, Woo PCY. Global Epidemiology of Bat Coronaviruses. Viruses. 2019;11(2).
- Xu Y. Unveiling the Origin and Transmission of 2019-nCoV. Trends Microbiol. 2020;28(4):239-40.
- Jumhawan U, Putri SP, Yusianto, Bamba T, Fukusaki E. Quantification of coffee blends for authentication of Asian palm civet coffee (Kopi Luwak) via metabolomics: A proof of concept. J Biosci Bioeng. 2016;122(1):79-84.
- Guan Y, Zheng BJ, He YQ, et al. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science. 2003;302(5643):276-8.
- Tu C, Crameri G, Kong X, et al. Antibodies to SARS coronavirus in civets. Emerging Infect Dis. 2004;10(12):2244-8.
- Zhao GP. SARS molecular epidemiology: a Chinese fairy tale of controlling an emerging zoonotic disease in the genomics era. Philos Trans R Soc Lond, B, Biol Sci. 2007;362(1482):1063-81.
- Wan Y, Shang J, Graham R, Baric RS, Li F. Receptor Recognition by the Novel Coronavirus from Wuhan: an Analysis Based on Decade-Long Structural Studies of SARS Coronavirus. J Virol. 2020;94(7).
- Qu XX, Hao P, Song XJ, et al. Identification of two critical amino acid residues of the severe acute respiratory syndrome coronavirus spike protein for its variation in zoonotic tropism transition via a double substitution strategy. J Biol Chem. 2005;280(33):29588-95.
- Wang M, Yan M, Xu H, et al. SARS-CoV infection in a restaurant from palm civet. Emerging Infect Dis. 2005;11(12):1860-5.
- Song HD, Tu CC, Zhang GW, et al. Cross-host evolution of severe acute respiratory syndrome coronavirus in palm civet and human. Proc Natl Acad Sci USA. 2005;102(7):2430-5.
- Holmes KV. Structural biology. Adaptation of SARS coronavirus to humans. Science. 2005;309(5742):1822-3.
- Sheahan T, Rockx B, Donaldson E, Corti D, Baric R. Pathways of cross-species transmission of synthetically reconstructed zoonotic severe acute respiratory syndrome coronavirus. J Virol. 2008;82(17):8721-32.
- Nahar N, Asaduzzaman M, Mandal UK, et al. Hunting Bats for Human Consumption in Bangladesh. Ecohealth. 2020;17(1):139-51.
- Chan JF, To KK, Tse H, Jin DY, Yuen KY. Interspecies transmission and emergence of novel viruses: lessons from bats and birds. Trends Microbiol. 2013;21(10):544-55.
- Ashour HM, Elkhatib WF, Rahman MM, Elshabrawy HA. Insights into the Recent 2019 Novel Coronavirus (SARS-CoV-2) in Light of Past Human Coronavirus Outbreaks. Pathogens. 2020;9(3).
- Zhong NS, Zeng GQ. Pandemic planning in China: applying lessons from severe acute respiratory syndrome. Respirology. 2008;13(Suppl 1):33-35.
- Peeri NC, Shrestha N, Rahman MS, et al. The SARS, MERS and novel coronavirus (COVID-19) epidemics, the newest and biggest global health threats: what lessons have we learned?. Int J Epidemiol. 2020.
- Normile D, Yimin D. Infectious diseases. Civets back on China's menu. Science. 2003;301(5636):1031.
Motion graphics by AvoMedia
Image credit: Mindy McAdams via flickr. Image has been modified.
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The SARS Coronavirus and Wet Markets
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Content URLDoctor's Note
This is the 2nd in a 17-video series on pandemics and COVID-19. First, we looked at Where Do Deadly Coronaviruses Like MERS-CoV Come From?
We continue exploring the sources of these viruses next, in:
- Where Did the COVID-19 Coronavirus Come From?
- The Last Coronavirus Pandemic May Have Been Caused by Livestock
You can download the whole series (for free) right now on DrGreger.org and take an even deeper dive in my new book How to Survive a Pandemic (note: all my proceeds from this book are donated to pandemic prevention charities such as the Good Food Institute, Plant-Based Foods Association, A Well-Fed World, and the Center for Infectious Disease Research and Policy).
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