Fatal swine acute diarrhoea syndrome caused by an HKU2-related coronavirus of bat origin.

Peng Zhou1 Hang Fan2 Tian Lan3,4 Xing-Lou Yang1 Wei-Feng Shi5 Wei Zhang1 Yan Zhu1 Ya-Wei Zhang2 Qing-Mei Xie3,4 Shailendra Mani6 Xiao-Shuang Zheng1 Bei Li1 Jin-Man Li2 Hua Guo1 Guang-Qian Pei2 Xiao-Ping An2 Jun-Wei Chen3,4 Ling Zhou3,4 Kai-Jie Mai3,4 Zi-Xian Wu3,4 Di Li3,4 Danielle E Anderson6 Li-Biao Zhang7 Shi-Yue Li8 Zhi-Qiang Mi2 Tong-Tong He2 Feng Cong9 Peng-Ju Guo9 Ren Huang9 Yun Luo1 Xiang-Ling Liu1 Jing Chen1 Yong Huang2 Qiang Sun2 Xiang-Li-Lan Zhang2 Yuan-Yuan Wang2 Shao-Zhen Xing2 Yan-Shan Chen3,4 Yuan Sun3,4 Juan Li5 Peter Daszak10 Lin-Fa Wang11 Zheng-Li Shi12 Yi-Gang Tong13,14 Jing-Yun Ma15,16
Affiliations 16 institutions
  1. CAS Key Laboratory of Special Pathogens and Biosafety, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan, China.
  2. Beijing Institute of Microbiology and Epidemiology, Beijing, China.
  3. College of Animal Science, South China Agricultural University, Guangzhou, China.
  4. Key Laboratory of Animal Health Aquaculture and Environmental Control, Guangzhou, China.
  5. Key Laboratory of Etiology and Epidemiology of Emerging Infectious Diseases in Universities of Shandong, Taishan Medical College, Taian, China.
  6. Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore, Singapore.
  7. Guangdong Key Laboratory of Animal Conservation and Resource Utilization, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Guangdong Institute of Applied Biological Resources, Guangzhou, China.
  8. School of Public Health, Wuhan University, Wuhan, China.
  9. Guangdong Key Laboratory of Laboratory Animals, Guangdong Laboratory Animals Monitoring Institute, Guangzhou, China.
  10. EcoHealth Alliance, New York, NY, USA. [email protected].
  11. Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore, Singapore. [email protected].
  12. CAS Key Laboratory of Special Pathogens and Biosafety, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan, China. [email protected].
  13. Beijing Institute of Microbiology and Epidemiology, Beijing, China. [email protected].
  14. School of Life Sciences, North China University of Science and Technology, Tangshan, China. [email protected].
  15. College of Animal Science, South China Agricultural University, Guangzhou, China. [email protected].
  16. Key Laboratory of Animal Health Aquaculture and Environmental Control, Guangzhou, China. [email protected].

Abstract

Cross-species transmission of viruses from wildlife animal reservoirs poses a marked threat to human and animal health 1 . Bats have been recognized as one of the most important reservoirs for emerging viruses and the transmission of a coronavirus that originated in bats to humans via intermediate hosts was responsible for the high-impact emerging zoonosis, severe acute respiratory syndrome (SARS) 2-10 . Here we provide virological, epidemiological, evolutionary and experimental evidence that a novel HKU2-related bat coronavirus, swine acute diarrhoea syndrome coronavirus (SADS-CoV), is the aetiological agent that was responsible for a large-scale outbreak of fatal disease in pigs in China that has caused the death of 24,693 piglets across four farms. Notably, the outbreak began in Guangdong province in the vicinity of the origin of the SARS pandemic. Furthermore, we identified SADS-related CoVs with 96-98% sequence identity in 9.8% (58 out of 591) of anal swabs collected from bats in Guangdong province during 2013-2016, predominantly in horseshoe bats (Rhinolophus spp.) that are known reservoirs of SARS-related CoVs. We found that there were striking similarities between the SADS and SARS outbreaks in geographical, temporal, ecological and aetiological settings. This study highlights the importance of identifying coronavirus diversity and distribution in bats to mitigate future outbreaks that could threaten livestock, public health and economic growth.

Supporting text Virus Host Location
Alphacoronavirus 29 Animal Diseases 9 Animals 1948 Biodiversity 10 China 229 Chiroptera 371 Coronavirus Infections 171 Diarrhea 29 Disease Reservoirs 149 Genome, Viral 317 Humans 1440 Jejunum 2 Phylogeny 805 Severe Acute Respiratory Syndrome 22 Spatio-Temporal Analysis 9 Swine 258 Zoonoses 397

Evidence records

5 total
Zoonotic Surveillance
2 records · 2 evidence types
Evidence type
1 records
OVE2923
Key finding

SADS-related coronaviruses were detected in anal swabs from bats, predominantly horseshoe bats (Rhinolophus spp.), in Guangdong province with 96–98% sequence identity.

Virus
Host
Location
Supporting text

We identified SADS-related CoVs with 96–98% sequence identity in 9.8% (58 out of 591) of anal swabs collected from bats in Guangdong province during 2013–2016, predominantly in horseshoe bats (Rhinolophus spp.).

Method
sequence identity analysis | viral RNA detection
Sample type
anal swabs
Geographic raw
Guangdong province
Country inferred
CHN
Evidence type
1 records
OVE2924
Key finding

SADS-related coronaviruses were predominantly detected in horseshoe bats (Rhinolophus spp.) in Guangdong province, which are recognized reservoirs of SARS-related coronaviruses.

Virus
Host
Location
Supporting text

Furthermore, we identified SADS-related CoVs with 96-98% sequence identity in 9.8% (58 out of 591) of anal swabs collected from bats in Guangdong province during 2013-2016, predominantly in horseshoe bats (Rhinolophus spp.) that are known reservoirs of SARS-related CoVs.

Method
field sampling | PCR screening | sequence identity comparison
Sample type
anal swabs
Geographic raw
Guangdong province
Country inferred
CHN
Transmission Evidence
2 records · 2 evidence types
Evidence type
1 records
OVE2922
Key finding

Swine acute diarrhoea syndrome coronavirus (SADS‑CoV) was identified as the etiological agent of a large‑scale fatal outbreak in pigs in China.

Virus
Host
Location
Supporting text

Here we provide virological, epidemiological, evolutionary and experimental evidence that a novel HKU2‑related bat coronavirus, swine acute diarrhoea syndrome coronavirus (SADS‑CoV), is the aetiological agent that was responsible for a large‑scale outbreak of fatal disease in pigs in China that has caused the death of 24,693 piglets across four farms.

Method
virological | epidemiological | evolutionary | experimental
Transmission direction
animal-to-animal
Geographic raw
China (Guangdong province)
Outbreak setting
pig farms
Outbreak time
2013–2016
Outbreak scale
death of 24,693 piglets across four farms
Evidence type
1 records
OVE2926
Key finding

An HKU2-related bat coronavirus (SADS-CoV) was transmitted from bats to pigs, representing a cross-species transmission event causing fatal swine disease in China.

Virus
Host
Location
Supporting text

Here we provide virological, epidemiological, evolutionary and experimental evidence that a novel HKU2-related bat coronavirus, swine acute diarrhoea syndrome coronavirus (SADS-CoV), is the aetiological agent that was responsible for a large-scale outbreak of fatal disease in pigs in China.

Method
virological analysis | epidemiological investigation | evolutionary analysis | experimental evidence
Study design
virological, epidemiological, evolutionary and experimental evidence study
Transmission direction
animal-to-animal
Geographic raw
China
Country inferred
CHN
Genomic Evolution
1 records · 1 evidence types
Evidence type
1 records
OVE2925
Key finding

Phylogenetic comparison showed that swine acute diarrhoea syndrome coronavirus (SADS-CoV) is closely related to HKU2-related bat coronaviruses, indicating a bat evolutionary origin.

Virus
Host
Location
Not specified
Supporting text

Here we provide virological, epidemiological, evolutionary and experimental evidence that a novel HKU2-related bat coronavirus, swine acute diarrhoea syndrome coronavirus (SADS-CoV), is the aetiological agent that was responsible for a large-scale outbreak of fatal disease in pigs in China.

Analysis methods
phylogenetic analysis | sequence identity comparison