Literature detail

Investigations into SARS-CoV-2 and other coronaviruses on mink farms in France late in the first year of the COVID-19 pandemic.

Marine Wasniewski1 Franck Boué2 Céline Richomme2 Etienne Simon-Lorière3 Sylvie Van der Werf4,5 Flora Donati4,5 Vincent Enouf4,5,6 Yannick Blanchard7 Véronique Beven7 Estelle Leperchois8,9 Bryce Leterrier8,9 Sandrine Corbet9 Meriadeg Le Gouil8,9 Elodie Monchatre-Leroy10 Evelyne Picard-Meyer1
Affiliations 10 institutions
  1. Lyssavirus Unit, Nancy Laboratory for Rabies and Wildlife, ANSES, Malzéville, France.
  2. Wildlife Surveillance and Eco-epidemiology Unit, Nancy Laboratory for Rabies and Wildlife, ANSES, Malzéville, France.
  3. G5 Evolutionary Genomics of RNA Viruses, Institut Pasteur, Université Paris Cité, Paris, France.
  4. Molecular Genetics of RNA Viruses, CNRS UMR 3569, Institut Pasteur, Université Paris Cité, Paris, France.
  5. National Reference Center for Respiratory Viruses, Institut Pasteur, Université Paris Cité, Paris, France.
  6. Mutualized Platform of Microbiology, Pasteur International Bioresources Network, Institut Pasteur, Université Paris Cité, Paris, France.
  7. Unit of Viral Genetics and Biosafety, Ploufragan-Plouzané-Niort Laboratory, ANSES, Ploufragan, France.
  8. DYNAMICURE INSERM U1311 UNIROUEN, Université de Caen, Caen, France.
  9. Virology Department, Caen University Hospital, Caen, France.
  10. Nancy Laboratory for Rabies and Wildlife, ANSES, Malzéville, France.
PMID 37624818 2023 PLoS One eng epublish
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Article

Publication summary

Soon after the beginning of the COVID-19 pandemic in early 2020, the Betacoronavirus SARS-CoV-2 infection of several mink farms breeding American minks (Neovison vison) for fur was detected in various European countries. The risk of a new reservoir being formed and of a reverse zoonosis from minks quickly became a major concern. The aim of this study was to investigate the four French mink farms to see whether SARS-CoV-2 was circulating there in late 2020. The investigations took place during the slaughtering period, thus facilitating different types of sampling (swabs and blood). On one of the four mink farms, 96.6% of serum samples were positive when tested with a SARS-CoV-2 ELISA coated with purified N protein recombinant antigen, and 54 out of 162 (33%) pharyngo-tracheal swabs were positive by RT-qPCR. The genetic variability among 12 SARS-CoV-2 genomes sequenced from this farm indicated the co-circulation of several lineages at the time of sampling. All the SARS-CoV-2 genomes detected were nested within the 20A clade (Nextclade), together with SARS-CoV-2 genomes from humans sampled during the same period. The percentage of SARS-CoV-2 seropositivity by ELISA varied between 0.3 and 1.1% on the other three farms. Interestingly, among these three farms, 11 pharyngo-tracheal swabs and 3 fecal pools from two farms were positive by end-point RT-PCR for an Alphacoronavirus very similar to a mink coronavirus sequence observed on Danish farms in 2015. In addition, a mink Caliciviridae was identified on one of the two farms positive for Alphacoronavirus. The clinical impact of these inapparent viral infections is not known. The co-infection of SARS-CoV-2 with other viruses on mink farms could help explain the diversity of clinical symptoms noted on different infected farms in Europe. In addition, the co-circulation of an Alphacoronavirus and SARS-CoV-2 on a mink farm would potentially increase the risk of viral recombination between alpha and betacoronaviruses as already suggested in wild and domestic animals, as well as in humans.

Alphacoronavirus COVID-19 Animals Asymptomatic Infections Farms France Humans Mink Pandemics SARS-CoV-2

Structured evidence records

Evidence records

7 total
2 records
Extraction confidence 0.90
Key finding

Sequencing of 12 SARS-CoV-2 genomes from French mink revealed several co-circulating lineages within the 20A clade associated with human genomes from the same period.

Virus
Location
Not specified
Supporting text

The genetic variability among 12 SARS-CoV-2 genomes sequenced from this farm indicated the co-circulation of several lineages at the time of sampling. All the SARS-CoV-2 genomes detected were nested within the 20A clade (Nextclade), together with SARS-CoV-2 genomes from humans sampled during the same period.

Analysis methods
genome sequencing; phylogenetic analysis
Extraction confidence 0.85
Key finding

RT-PCR and sequence similarity identified Alphacoronavirus strains in French mink closely related to a 2015 Danish mink coronavirus sequence.

Location
Not specified
Supporting text

Among these three farms, 11 pharyngo-tracheal swabs and 3 fecal pools from two farms were positive by end-point RT-PCR for an Alphacoronavirus very similar to a mink coronavirus sequence observed on Danish farms in 2015.

Analysis methods
RT-PCR; sequence similarity analysis
2 records
Extraction confidence 0.95
Key finding

SARS-CoV-2 was detected by serology and RT-qPCR in mink samples on one of four French mink farms surveyed in late 2020.

Virus
Location
Supporting text

The aim of this study was to investigate the four French mink farms to see whether SARS-CoV-2 was circulating there in late 2020. ... 96.6% of serum samples were positive when tested with a SARS-CoV-2 ELISA coated with purified N protein recombinant antigen, and 54 out of 162 (33%) pharyngo-tracheal swabs were positive by RT-qPCR.

Method
ELISA; RT-qPCR
Sample type
serum; pharyngo-tracheal swab
Geographic raw
France
Country inferred
France
Extraction confidence 0.95
Key finding

Alphacoronavirus related to a previously detected mink coronavirus was found by RT-PCR in pharyngo-tracheal swabs and fecal pools from French mink farms.

Location
Supporting text

Among these three farms, 11 pharyngo-tracheal swabs and 3 fecal pools from two farms were positive by end-point RT-PCR for an Alphacoronavirus very similar to a mink coronavirus sequence observed on Danish farms in 2015.

Method
end-point RT-PCR
Sample type
pharyngo-tracheal swab; fecal pool
Geographic raw
France
Country inferred
France
1 records
Extraction confidence 0.60
Key finding

Co-circulation of Alphacoronavirus and SARS-CoV-2 on mink farms in France was noted and linked to a potential risk of recombination between alpha and betacoronaviruses.

Host
Not specified
Location
Not specified
Supporting text

The co-circulation of an Alphacoronavirus and SARS-CoV-2 on a mink farm would potentially increase the risk of viral recombination between alpha and betacoronaviruses as already suggested in wild and domestic animals, as well as in humans.

Event type
recombination
1 records
Extraction confidence 0.95
Key finding

High SARS-CoV-2 seropositivity was found among American mink on one French farm (96.6% positive by ELISA), indicating prior viral exposure and infection.

Virus
Location
Not specified
Supporting text

On one of the four mink farms, 96.6% of serum samples were positive when tested with a SARS-CoV-2 ELISA coated with purified N protein recombinant antigen, while the percentage of SARS-CoV-2 seropositivity by ELISA varied between 0.3 and 1.1% on the other three farms.

Method
ELISA
Sample type
serum
1 records
Extraction confidence 0.90
Key finding

SARS-CoV-2 infection identified in farmed American minks in France, with genomic evidence linking mink viruses to human lineages, indicating a human-to-mink spillback event.

Virus
Location
Supporting text

Soon after the beginning of the COVID-19 pandemic in early 2020, the Betacoronavirus SARS-CoV-2 infection of several mink farms breeding American minks (Neovison vison) for fur was detected in various European countries. ... All the SARS-CoV-2 genomes detected were nested within the 20A clade (Nextclade), together with SARS-CoV-2 genomes from humans sampled during the same period.

Method
ELISA; RT-qPCR; sequencing
Study design
field surveillance
Transmission direction
human-to-animal
Geographic raw
France
Country inferred
France