Emergence and spread of SARS-CoV-2 variants from farmed mink to humans and back during the epidemic in Denmark, June-November 2020.

Thomas Bruun Rasmussen1 Amanda Gammelby Qvesel1,2,3 Anders Gorm Pedersen2,3 Ann Sofie Olesen1 Jannik Fonager1 Morten Rasmussen1 Raphael Niklaus Sieber4 Marc Stegger4 Francisco Fernando Calvo-Artavia5 Marlies Jilles Francine Goedknegt2 Esben Rahbek Thuesen2,3 Louise Lohse1 Sten Mortensen5 Anders Fomsgaard1 Anette Boklund6 Anette Bøtner6 Graham J Belsham6
Affiliations 6 institutions
  1. Department of Virus and Microbiological Special Diagnostics, Statens Serum Institut, Copenhagen, Denmark.
  2. Department of Health Technology, Section for Bioinformatics, Technical University of Denmark, Kgs. Lyngby, Denmark.
  3. PandemiX Center, Department of Science and Environment, Roskilde University, Roskilde, Denmark.
  4. Department of Bioinformatics, Statens Serum Institut, Copenhagen, Denmark.
  5. Danish Veterinary and Food Administration, Ministry of Environment and Food, Glostrup, Denmark.
  6. Department of Veterinary and Animal Sciences, University of Copenhagen, Frederiksberg, Denmark.

Abstract

The severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) not only caused the COVID-19 pandemic but also had a major impact on farmed mink production in several European countries. In Denmark, the entire population of farmed mink (over 15 million animals) was culled in late 2020. During the period of June to November 2020, mink on 290 farms (out of about 1100 in the country) were shown to be infected with SARS-CoV-2. Genome sequencing identified changes in the virus within the mink and it is estimated that about 4000 people in Denmark became infected with these mink virus variants. However, the routes of transmission of the virus to, and from, the mink have been unclear. Phylogenetic analysis revealed the generation of multiple clusters of the virus within the mink. Detailed analysis of changes in the virus during replication in mink and, in parallel, in the human population in Denmark, during the same time period, has been performed here. The majority of cases in mink involved variants with the Y453F substitution and the H69/V70 deletion within the Spike (S) protein; these changes emerged early in the outbreak. However, further introductions of the virus, by variants lacking these changes, from the human population into mink also occurred. Based on phylogenetic analysis of viral genome data, we estimate, using a conservative approach, that about 17 separate examples of mink to human transmission occurred in Denmark but up to 59 such events (90% credible interval: (39-77)) were identified using parsimony to count cross-species jumps on transmission trees inferred using Bayesian methods. Using the latter approach, 136 jumps (90% credible interval: (117-164)) from humans to mink were found, which may underlie the farm-to-farm spread. Thus, transmission of SARS-CoV-2 from humans to mink, mink to mink, from mink to humans and between humans were all observed.

Supporting text Virus Host Location
COVID-19 425 Mink 48 Phylogeny 805 SARS-CoV-2 453 Animals 1948 Betacoronavirus 78 Coronavirus Infections 171 Denmark 7 Farms 30 Genome, Viral 317 Humans 1440 Pandemics 108 Spike Glycoprotein, Coronavirus 274 SARS-CoV-2 variants 86

Evidence records

4 total
Zoonotic Surveillance
1 records · 1 evidence types
Evidence type
1 records
OVE8180
Key finding

SARS-CoV-2 was detected in mink on 290 farms in Denmark between June and November 2020.

Virus
Host
Location
Supporting text

During the period of June to November 2020, mink on 290 farms (out of about 1100 in the country) were shown to be infected with SARS-CoV-2.

Method
viral RNA detection | genome sequencing
Sample type
farm surveillance samples
Geographic raw
Denmark
Country inferred
DNK
Transmission Evidence
1 records · 1 evidence types
Evidence type
1 records
OVE8182
Key finding

Phylogenetic analysis estimated 17 to 59 mink-to-human transmission events of SARS-CoV-2 in Denmark.

Virus
Host
Location
Supporting text

Based on phylogenetic analysis of viral genome data, we estimate, using a conservative approach, that about 17 separate examples of mink to human transmission occurred in Denmark but up to 59 such events ... were identified using parsimony to count cross-species jumps on transmission trees inferred using Bayesian methods.

Method
Bayesian transmission tree reconstruction | parsimony-based cross-species jump counting
Study design
phylogenetic inference of viral genomes
Transmission direction
animal-to-human
Geographic raw
Denmark
Country inferred
DNK
Functional Mechanism
1 records · 1 evidence types
Evidence type
1 records
OVE8181
Key finding

SARS-CoV-2 variants infecting Danish mink carried the Y453F substitution and H69/V70 deletion in the Spike protein, indicating host-associated molecular adaptation during early outbreak spread.

Virus
Host
Not specified
Location
Not specified
Supporting text

The majority of cases in mink involved variants with the Y453F substitution and the H69/V70 deletion within the Spike (S) protein; these changes emerged early in the outbreak.

Genes or proteins
Spike protein | S protein
Receptors
ACE2
Mutations
Y453F | H69/V70 deletion
Mechanism types
receptor binding | host-range expansion
Genomic Evolution
1 records · 1 evidence types
Evidence type
1 records