Farmed fur animals harbour viruses with zoonotic spillover potential.

Jin Zhao1 Wenbo Wan1 Kang Yu1,2 Philippe Lemey3 John H-O Pettersson4,5,6 Yuhai Bi7 Meng Lu1 Xinxin Li8 Zhuohang Chen1 Mengdi Zheng8 Ge Yan2 JianJun Dai2 Yuxing Li1 Ayidana Haerheng1 Na He1 Changchun Tu9 Marc A Suchard10 Edward C Holmes11,12 Wan-Ting He13 Shuo Su14
Affiliations 14 institutions
  1. Department of Epidemiology, School of Public Health, Shanghai Institute of Infectious Disease and Biosecurity, Fudan University, Shanghai, China.
  2. State Key Laboratory of Natural Medicines, School of Pharmacy, China Pharmaceutical University, Nanjing, China.
  3. Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory for Clinical and Epidemiological Virology, KU Leuven, Leuven, Belgium.
  4. Clinical Microbiology, Department of Medical Sciences, University of Uppsala, Uppsala, Sweden.
  5. Clinical Microbiology and Hospital Hygiene, Uppsala University Hospital, Uppsala, Sweden.
  6. Department of Microbiology and Immunology, Peter Doherty Institute for Infection and Immunity, University of Melbourne, Melbourne, Victoria, Australia.
  7. CAS Key Laboratory of Pathogen Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences (CAS), Beijing, China.
  8. Jiangsu Engineering Laboratory of Animal Immunology, Institute of Immunology, College of Veterinary Medicine, Academy for Advanced Interdisciplinary Studies, Nanjing Agricultural University, Nanjing, China.
  9. Changchun Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Changchun, China.
  10. Department of Biostatistics, Fielding School of Public Health, and Departments of Biomathematics and Human Genetics, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA.
  11. School of Medical Sciences, The University of Sydney, Sydney, New South Wales, Australia.
  12. Laboratory of Data Discovery for Health Limited, Hong Kong SAR, China.
  13. State Key Laboratory of Natural Medicines, School of Pharmacy, China Pharmaceutical University, Nanjing, China. [email protected].
  14. Department of Epidemiology, School of Public Health, Shanghai Institute of Infectious Disease and Biosecurity, Fudan University, Shanghai, China. [email protected].

Abstract

Animals such as raccoon dogs, mink and muskrats are farmed for fur and are sometimes used as food or medicinal products1,2, yet they are also potential reservoirs of emerging pathogens3. Here we performed single-sample metatranscriptomic sequencing of internal tissues from 461 individual fur animals that were found dead due to disease. We characterized 125 virus species, including 36 that were novel and 39 at potentially high risk of cross-species transmission, including zoonotic spillover. Notably, we identified seven species of coronaviruses, expanding their known host range, and documented the cross-species transmission of a novel canine respiratory coronavirus to raccoon dogs and of bat HKU5-like coronaviruses to mink, present at a high abundance in lung tissues. Three subtypes of influenza A virus-H1N2, H5N6 and H6N2-were detected in the lungs of guinea pig, mink and muskrat, respectively. Multiple known zoonotic viruses, such as Japanese encephalitis virus and mammalian orthoreovirus4,5, were detected in guinea pigs. Raccoon dogs and mink carried the highest number of potentially high-risk viruses, while viruses from the Coronaviridae, Paramyxoviridae and Sedoreoviridae families commonly infected multiple hosts. These data also reveal potential virus transmission between farmed animals and wild animals, and from humans to farmed animals, indicating that fur farming represents an important transmission hub for viral zoonoses.

Supporting text Virus Host Location
Animal Fur 1 Animals, Domestic 35 Animals, Wild 187 Disease Reservoirs 149 Host Specificity 133 Viral Zoonoses 65 Animals 1949 Arvicolinae 16 Chiroptera 372 Coronavirus 92 Dogs 177 Encephalitis Virus, Japanese 8 Guinea Pigs 21 Humans 1441 Influenza A virus 186 Lung 65 Mink 48 Orthoreovirus 6 Phylogeny 805 Raccoon Dogs 6

Evidence records

8 total
Zoonotic Surveillance
6 records · 1 evidence types
Evidence type
6 records
OVE8373
Key finding

Metatranscriptomic sequencing of internal tissues from farmed fur animals that died of disease detected 125 virus species, including 36 novel viruses.

Virus
Host
Location
Not specified
Supporting text

We performed single-sample metatranscriptomic sequencing of internal tissues from 461 individual fur animals that were found dead due to disease. We characterized 125 virus species, including 36 that were novel.

Method
metatranscriptomic sequencing
Sample type
internal tissues
OVE8374
Key finding

Influenza A virus H1N2 subtype was detected in lungs of guinea pigs.

Virus
Host
Location
Not specified
Supporting text

Three subtypes of influenza A virus—H1N2, H5N6 and H6N2—were detected in the lungs of guinea pig, mink and muskrat, respectively.

Method
viral detection
Sample type
lungs
OVE8375
Key finding

Influenza A virus H5N6 subtype was detected in lungs of mink.

Virus
Host
Location
Not specified
Supporting text

Three subtypes of influenza A virus—H1N2, H5N6 and H6N2—were detected in the lungs of guinea pig, mink and muskrat, respectively.

Method
viral detection
Sample type
lungs
OVE8376
Key finding

Influenza A virus H6N2 subtype was detected in lungs of muskrats.

Virus
Host
Location
Not specified
Supporting text

Three subtypes of influenza A virus—H1N2, H5N6 and H6N2—were detected in the lungs of guinea pig, mink and muskrat, respectively.

Method
viral detection
Sample type
lungs
Transmission Evidence
2 records · 1 evidence types
Evidence type
2 records
OVE8379
Key finding

A novel canine respiratory coronavirus was transmitted from dogs to raccoon dogs.

Virus
Host
Location
Not specified
Supporting text

documented the cross-species transmission of a novel canine respiratory coronavirus to raccoon dogs

Method
metatranscriptomic sequencing
Study design
metatranscriptomic sequencing survey
Transmission direction
animal-to-animal
OVE8380
Key finding

Bat HKU5-like coronaviruses were transmitted from bats to mink.

Virus
Host
Location
Not specified
Supporting text

documented the cross-species transmission ... of bat HKU5-like coronaviruses to mink, present at a high abundance in lung tissues

Method
metatranscriptomic sequencing
Study design
metatranscriptomic sequencing survey
Transmission direction
animal-to-animal