Adaptation, spread and transmission of SARS-CoV-2 in farmed minks and associated humans in the Netherlands.

Lu Lu1 Reina S Sikkema2 Francisca C Velkers3 David F Nieuwenhuijse2 Egil A J Fischer3 Paola A Meijer3 Noortje Bouwmeester-Vincken4 Ariene Rietveld5 Marjolijn C A Wegdam-Blans6 Paulien Tolsma7 Marco Koppelman8 Lidwien A M Smit9 Renate W Hakze-van der Honing10 Wim H M van der Poel10 Arco N van der Spek11 Marcel A H Spierenburg11 Robert Jan Molenaar12 Jan de Rond12 Marieke Augustijn12 Mark Woolhouse1 J Arjan Stegeman3 Samantha Lycett13 Bas B Oude Munnink2 Marion P G Koopmans14
Affiliations 14 institutions
  1. Usher Institute, University of Edinburgh, Edinburgh, UK.
  2. Erasmus MC, Department of Viroscience, WHO Collaborating Centre, Rotterdam, the Netherlands.
  3. Department Population Health Sciences, Faculty of Veterinary Medicine, Utrecht University, Utrecht, the Netherlands.
  4. Municipal Health Service GGD Limburg-Noord, Venlo, the Netherlands.
  5. Municipal Health Service GGD Hart voor Brabant, Tilburg, the Netherlands.
  6. Stichting PAMM, Veldhoven, the Netherlands.
  7. Municipal Health Service GGD Brabant-Zuidoost, Eindhoven, the Netherlands.
  8. Sanquin Blood Supply Foundation, Amsterdam, the Netherlands.
  9. Institute for Risk Assessment Sciences (IRAS), Utrecht University, Utrecht, the Netherlands.
  10. Wageningen Bioveterinary Research, Lelystad, the Netherlands.
  11. Netherlands Food and Consumer Product Safety Authority (NVWA), Utrecht, the Netherlands.
  12. GD Animal Health, Deventer, the Netherlands.
  13. Roslin Institute, University of Edinburgh, Edinburgh, UK.
  14. Erasmus MC, Department of Viroscience, WHO Collaborating Centre, Rotterdam, the Netherlands. [email protected].

Abstract

In the first wave of the COVID-19 pandemic (April 2020), SARS-CoV-2 was detected in farmed minks and genomic sequencing was performed on mink farms and farm personnel. Here, we describe the outbreak and use sequence data with Bayesian phylodynamic methods to explore SARS-CoV-2 transmission in minks and humans on farms. High number of farm infections (68/126) in minks and farm workers (>50% of farms) were detected, with limited community spread. Three of five initial introductions of SARS-CoV-2 led to subsequent spread between mink farms until November 2020. Viruses belonging to the largest cluster acquired an amino acid substitution in the receptor binding domain of the Spike protein (position 486), evolved faster and spread longer and more widely. Movement of people and distance between farms were statistically significant predictors of virus dispersal between farms. Our study provides novel insights into SARS-CoV-2 transmission between mink farms and highlights the importance of combining genetic information with epidemiological information when investigating outbreaks at the animal-human interface.

Supporting text Virus Host Location
Evolution, Molecular 176 Farms 30 Amino Acid Sequence 128 Animal Diseases 9 Animals 1948 Bayes Theorem 32 COVID-19 425 Disease Outbreaks 170 Humans 1440 Mink 48 Netherlands 12 Phylogeny 805 SARS-CoV-2 453 Sequence Analysis, Protein 9 Spike Glycoprotein, Coronavirus 274 spike protein, SARS-CoV-2 157

Evidence records

5 total
Zoonotic Surveillance
1 records · 1 evidence types
Evidence type
1 records
OVE5386
Key finding

SARS-CoV-2 viral RNA was detected in farmed minks and farm personnel during the first COVID-19 wave in the Netherlands.

Virus
Host
Location
Supporting text

In the first wave of the COVID-19 pandemic (April 2020), SARS-CoV-2 was detected in farmed minks and genomic sequencing was performed on mink farms and farm personnel.

Method
viral RNA detection | genomic sequencing
Sample type
farm samples | human samples
Geographic raw
Netherlands
Country inferred
NLD
Transmission Evidence
2 records · 1 evidence types
Evidence type
2 records
OVE5387
Key finding

An outbreak investigation combining genomic and epidemiological data identified SARS-CoV-2 transmission between farmed minks and associated humans in the Netherlands during April–November 2020.

Virus
Host
Location
Supporting text

Adaptation, spread and transmission of SARS-CoV-2 in farmed minks and associated humans in the Netherlands. In the first wave of the COVID-19 pandemic (April 2020), SARS-CoV-2 was detected in farmed minks and genomic sequencing was performed on mink farms and farm personnel.

Method
genomic sequencing | Bayesian phylodynamic analysis | epidemiological investigation
Transmission direction
animal-to-human
Geographic raw
Netherlands
Country inferred
NLD
Outbreak setting
mink farms
Outbreak time
April–November 2020
Outbreak scale
68 of 126 farms affected; >50% of farms with infected workers
OVE5392
Key finding

SARS-CoV-2 spread between mink farms in the Netherlands during the first wave of the COVID-19 pandemic.

Virus
Host
Location
Supporting text

Three of five initial introductions of SARS-CoV-2 led to subsequent spread between mink farms until November 2020.

Method
genomic sequencing | Bayesian phylodynamic analysis | epidemiological correlation
Geographic raw
Netherlands
Functional Mechanism
1 records · 1 evidence types
Evidence type
1 records
OVE5391
Key finding

SARS-CoV-2 detected in farmed minks in the Netherlands acquired a Spike receptor binding domain substitution at position 486, associated with faster evolution and wider spread among mink farms.

Virus
Host
Not specified
Location
Not specified
Supporting text

In the first wave of the COVID-19 pandemic (April 2020), SARS-CoV-2 was detected in farmed minks and genomic sequencing was performed on mink farms and farm personnel. Viruses belonging to the largest cluster acquired an amino acid substitution in the receptor binding domain of the Spike protein (position 486), evolved faster and spread longer and more widely.

Genes or proteins
Spike protein | receptor binding domain
Mutations
position 486 substitution
Mechanism types
receptor binding | host-range expansion | transmission fitness
Genomic Evolution
1 records · 1 evidence types
Evidence type
1 records
OVE5390
Key finding

Phylogenetic analysis showed five separate SARS-CoV-2 introductions into Dutch mink farms, of which three led to subsequent viral spread between farms until November 2020.

Virus
Host
Location
Not specified
Supporting text

Three of five initial introductions of SARS-CoV-2 led to subsequent spread between mink farms until November 2020.

Analysis methods
phylogenetic analysis | Bayesian phylodynamic methods