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

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.

[1]  F. Balloux,et al.  The past, current and future epidemiological dynamic of SARS-CoV-2 , 2022, Oxford open immunology.

[2]  T. Sironen,et al.  Severe Acute Respiratory Syndrome Coronavirus 2 in Farmed Mink (Neovison vison), Poland , 2021, Emerging infectious diseases.

[3]  M. Ciccozzi,et al.  Update on the Phylodynamics of SADS-CoV , 2021, Life.

[4]  M. Koopmans,et al.  Adaptation, spread and transmission of SARS-CoV-2 in farmed minks and associated humans in the Netherlands , 2021, Nature Communications.

[5]  D. Raoult,et al.  Mink, SARS-CoV-2, and the Human-Animal Interface , 2021, Frontiers in Microbiology.

[6]  F. Vitale,et al.  A pre- and during Pandemic Survey of Sars-Cov-2 Infection in Stray Colony and Shelter Cats from a High Endemic Area of Northern Italy , 2021, Viruses.

[7]  L. Van Hoovels,et al.  Diagnostic and analytical performance evaluation of ten commercial assays for detecting SARS-CoV-2 humoral immune response , 2021, Journal of Immunological Methods.

[8]  N. Pavio,et al.  Characterization of a Cell Culture System of Persistent Hepatitis E Virus Infection in the Human HepaRG Hepatic Cell Line , 2021, Viruses.

[9]  N. Landau,et al.  Decreased neutralization of SARS-CoV-2 global variants by therapeutic anti-spike protein monoclonal antibodies , 2021, bioRxiv.

[10]  B. Graham,et al.  mRNA-1273 vaccine induces neutralizing antibodies against spike mutants from global SARS-CoV-2 variants , 2021, bioRxiv.

[11]  S. Mortensen,et al.  SARS-CoV-2 in Danish Mink Farms: Course of the Epidemic and a Descriptive Analysis of the Outbreaks in 2020 , 2021, Animals : an open access journal from MDPI.

[12]  Thomas M. Keane,et al.  Twelve years of SAMtools and BCFtools , 2020, GigaScience.

[13]  Hualan Chen,et al.  Replication, pathogenicity, and transmission of SARS-CoV-2 in minks , 2020, National science review.

[14]  T. Halasa,et al.  SARS-CoV-2 Transmission between Mink (Neovison vison) and Humans, Denmark , 2020, Emerging infectious diseases.

[15]  M. Koopmans,et al.  Transmission of SARS-CoV-2 on mink farms between humans and mink and back to humans , 2020, Science.

[16]  S. Lesellier,et al.  Hamster and ferret experimental infection with intranasal low dose of a single strain of SARS-CoV-2 , 2020, bioRxiv.

[17]  M. Hornef,et al.  Determination of SARS-CoV-2 antibodies with assays from Diasorin, Roche and IDvet , 2020, Journal of Virological Methods.

[18]  Andrew D Smith,et al.  Improvements to the ARTIC multiplex PCR method for SARS-CoV-2 genome sequencing using nanopore , 2020, bioRxiv.

[19]  M. Koopmans,et al.  Clinical and Pathological Findings in SARS-CoV-2 Disease Outbreaks in Farmed Mink (Neovison vison) , 2020, Veterinary pathology.

[20]  M. Koopmans,et al.  SARS-CoV-2 infection in farmed minks, the Netherlands, April and May 2020 , 2020, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[21]  P. Pourquier,et al.  First detection and genome sequencing of SARS‐CoV‐2 in an infected cat in France , 2020, Transboundary and emerging diseases.

[22]  Sudhir Kumar,et al.  Molecular Evolutionary Genetics Analysis (MEGA) for macOS. , 2020, Molecular biology and evolution.

[23]  Victor M Corman,et al.  Detection of 2019 novel coronavirus (2019-nCoV) by real-time RT-PCR , 2020, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[24]  E. Holmes,et al.  Shared Common Ancestry of Rodent Alphacoronaviruses Sampled Globally , 2019, Viruses.

[25]  Heng Li,et al.  Minimap2: pairwise alignment for nucleotide sequences , 2017, Bioinform..

[26]  Ryan R. Wick,et al.  Completing bacterial genome assemblies with multiplex MinION sequencing , 2017, bioRxiv.

[27]  P. Massin,et al.  Emerging highly pathogenic H5 avian influenza viruses in France during winter 2015/16: phylogenetic analyses and markers for zoonotic potential , 2017, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[28]  G. Gao,et al.  Epidemiology, Genetic Recombination, and Pathogenesis of Coronaviruses , 2016, Trends in Microbiology.

[29]  G. Hullinger,et al.  Causes of mortality in farmed mink in the Intermountain West, North America , 2015, Journal of veterinary diagnostic investigation : official publication of the American Association of Veterinary Laboratory Diagnosticians, Inc.

[30]  S. Brisse,et al.  AlienTrimmer: a tool to quickly and accurately trim off multiple short contaminant sequences from high-throughput sequencing reads. , 2013, Genomics.

[31]  K. Katoh,et al.  MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability , 2013, Molecular biology and evolution.

[32]  Steven L Salzberg,et al.  Fast gapped-read alignment with Bowtie 2 , 2012, Nature Methods.

[33]  Hua Wu,et al.  Complete Genome Sequence of a Mink Calicivirus in China , 2012, Journal of Virology.

[34]  Heng Li,et al.  A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data , 2011, Bioinform..

[35]  S. Puechmaille,et al.  SARS-Coronavirus ancestor’s foot-prints in South-East Asian bat colonies and the refuge theory , 2011, Infection, Genetics and Evolution.

[36]  E. Ghedin,et al.  Molecular characterization of a new species in the genus Alphacoronavirus associated with mink epizootic catarrhal gastroenteritis. , 2011, The Journal of general virology.

[37]  O. Gascuel,et al.  SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. , 2010, Molecular biology and evolution.

[38]  A. Rambaut,et al.  BEAST: Bayesian evolutionary analysis by sampling trees , 2007, BMC Evolutionary Biology.

[39]  S. Ho,et al.  Relaxed Phylogenetics and Dating with Confidence , 2006, PLoS biology.

[40]  J. Evermann,et al.  Ultrastructure of newly recognized caliciviruses of the dog and mink , 2005, Archives of Virology.

[41]  L. Saif,et al.  Detection and molecular characterization of cultivable caliciviruses from clinically normal mink and enteric caliciviruses associated with diarrhea in mink , 2001, Archives of Virology.