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. Here, we describe the outbreak and use sequence data with Bayesian phylodynamic methods to explore SARS-CoV-2 transmission in minks...

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Published inNature communications Vol. 12; no. 1; pp. 6802 - 12
Main Authors Lu, Lu, Sikkema, Reina S., Velkers, Francisca C., Nieuwenhuijse, David F., Fischer, Egil A. J., Meijer, Paola A., Bouwmeester-Vincken, Noortje, Rietveld, Ariene, Wegdam-Blans, Marjolijn C. A., Tolsma, Paulien, Koppelman, Marco, Smit, Lidwien A. M., Hakze-van der Honing, Renate W., van der Poel, Wim H. M., van der Spek, Arco N., Spierenburg, Marcel A. H., Molenaar, Robert Jan, Rond, Jan de, Augustijn, Marieke, Woolhouse, Mark, Stegeman, J. Arjan, Lycett, Samantha, Oude Munnink, Bas B., Koopmans, Marion P. G.
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 23.11.2021
Nature Publishing Group
Nature Portfolio
Subjects
45
45/47
45/77
49/91
631/181/735
631/326/421
631/326/596/2562
631/326/596/4130
692/700/478/174
Amino Acid Sequence
Amino acid substitution
Amino acids
Animal Diseases - epidemiology
Animal Diseases - transmission
Animal Diseases - virology
Animal human relations
Animals
Bayes Theorem
Bayesian analysis
COVID-19
COVID-19 - epidemiology
COVID-19 - transmission
COVID-19 - virology
Disease Outbreaks
Dispersal
Epidemiology
Evolution, Molecular
Farms
Farmworkers
Humanities and Social Sciences
Humans
Mink - virology
multidisciplinary
Mustela
Netherlands - epidemiology
Outbreaks
Pandemics
Personnel
Phylogeny
SARS-CoV-2 - genetics
SARS-CoV-2 - isolation & purification
SARS-CoV-2 - physiology
Science
Science (multidisciplinary)
Sequence Analysis, Protein
Severe acute respiratory syndrome coronavirus 2
Spike Glycoprotein, Coronavirus - classification
Spike Glycoprotein, Coronavirus - genetics
Spike protein
Statistical analysis
Viral diseases
Whole genome sequencing
Netherlands
Online AccessGet full text
ISSN2041-1723
2041-1723
DOI10.1038/s41467-021-27096-9

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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. SARS-CoV-2 was detected in mink farms in the Netherlands in the first wave of the pandemic with evidence of human-to-mink and mink-to-human transmission. Here, the authors investigate this outbreak using phylodynamic analysis and show that personnel links and spatial proximity are predictors of transmission between farms.
AbstractList SARS-CoV-2 was detected in mink farms in the Netherlands in the first wave of the pandemic with evidence of human-to-mink and mink-to-human transmission. Here, the authors investigate this outbreak using phylodynamic analysis and show that personnel links and spatial proximity are predictors of transmission between farms.
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.SARS-CoV-2 was detected in mink farms in the Netherlands in the first wave of the pandemic with evidence of human-to-mink and mink-to-human transmission. Here, the authors investigate this outbreak using phylodynamic analysis and show that personnel links and spatial proximity are predictors of transmission between farms.
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.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.
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.
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. SARS-CoV-2 was detected in mink farms in the Netherlands in the first wave of the pandemic with evidence of human-to-mink and mink-to-human transmission. Here, the authors investigate this outbreak using phylodynamic analysis and show that personnel links and spatial proximity are predictors of transmission between farms.
ArticleNumber 6802
Author Velkers, Francisca C.
Fischer, Egil A. J.
Nieuwenhuijse, David F.
van der Spek, Arco N.
Hakze-van der Honing, Renate W.
Molenaar, Robert Jan
Stegeman, J. Arjan
Lycett, Samantha
Rietveld, Ariene
Wegdam-Blans, Marjolijn C. A.
van der Poel, Wim H. M.
Spierenburg, Marcel A. H.
Woolhouse, Mark
Lu, Lu
Meijer, Paola A.
Rond, Jan de
Tolsma, Paulien
Oude Munnink, Bas B.
Koopmans, Marion P. G.
Smit, Lidwien A. M.
Bouwmeester-Vincken, Noortje
Augustijn, Marieke
Sikkema, Reina S.
Koppelman, Marco
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  email: m.koopmans@erasmusmc.nl
  organization: Erasmus MC, Department of Viroscience, WHO Collaborating Centre
BackLink https://www.ncbi.nlm.nih.gov/pubmed/34815406$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
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2021. The Author(s).
The Author(s) 2021. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Copyright_xml – notice: The Author(s) 2021
– notice: 2021. The Author(s).
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BaeleGImproving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertaintyMol. Biol. Evol.201229215721671:CAS:528:DC%2BC38Xht1KjsbvL10.1093/molbev/mss084
Tchesnokova, V. et al. Acquisition of the L452R mutation in the ACE2-binding interface of spike protein triggers recent massive expansion of SARS-Cov-2 variants. J Clin Microbiol. 2021;59:e0092121. https://doi.org/10.1128/JCM.00921-21 (2021).
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PetersenEComparing SARS-CoV-2 with SARS-CoV and influenza pandemicsLancet Infect. Dis.202020e238e2441:CAS:528:DC%2BB3cXhtlegu7rE10.1016/S1473-3099(20)30484-9
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References_xml – reference: Davies, N. G. et al. Estimated transmissibility and impact of SARS-CoV-2 lineage B.1.1.7 in England. Science372, eabg3055. (2021).
– reference: Boklund, A. et al. SARS-CoV-2 in Danish mink farms: course of the epidemic and a descriptive analysis of the outbreaks in 2020. Animals (Basel)11, 164 (2021).
– reference: LanJStructure of the SARS-CoV-2 spike receptor-binding domain bound to the ACE2 receptorNature20205812152202020Natur.581..215L1:CAS:528:DC%2BB3cXoslOqtL8%3D10.1038/s41586-020-2180-5
– reference: Bayarri-Olmos, R. et al. The SARS-CoV-2 Y453F mink variant displays a pronounced increase in ACE-2 affinity but does not challenge antibody neutralization. J. Biol. Chem.296, 100536 (2021).
– reference: BaeleGImproving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertaintyMol. Biol. Evol.201229215721671:CAS:528:DC%2BC38Xht1KjsbvL10.1093/molbev/mss084
– reference: BoenderGJRisk maps for the spread of highly pathogenic avian influenza in poultryPLoS Comput. Biol.20073e712007PLSCB...3...71B237304710.1371/journal.pcbi.0030071
– reference: LemeyPRambautADrummondAJSuchardMABayesian phylogeography finds its rootsPLoS Comput. Biol.20095e10005202009PLSCB...5E0520L255930010.1371/journal.pcbi.1000520
– reference: de Rooij, M. M. T. et al. Occupational and environmental exposure to SARS-CoV-2 in and around infected mink farms. Occupational and environmental medicine. https://doi.org/10.1136/oemed-2021-107443 (2021).
– reference: Suchard, M. A. et al. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol. 4, vey016 (2018).
– reference: Corman, V. M. et al. Detection of 2019 novel coronavirus (2019-nCoV) by real-time RT-PCR. Euro Surveill. 25, 2000045 (2020).
– reference: MacLean, O. A., Orton, R. J., Singer, J. B. & Robertson, D. L. No evidence for distinct types in the evolution of SARS-CoV-2. Virus Evol. 6, veaa034 (2020).
– reference: Montagutelli, X. et al. The B1.351 and P.1 variants extend SARS-CoV-2 host range to mice. Preprint at bioRxivhttps://doi.org/10.1101/2021.03.18.436013 (2021).
– reference: Motozono, C. et al. SARS-CoV-2 spike L452R variant evades cellular immunity and increases infectivity. Cell Host & Microbe, https://doi.org/10.1016/j.chom.2021.06.006 (2021).
– reference: LiXEvolutionary history, potential intermediate animal host, and cross-species analyses of SARS-CoV-2J. Med Virol.2020926026111:CAS:528:DC%2BB3cXntlelsrw%3D10.1002/jmv.25731
– reference: BouckaertRBEAST 2.5: an advanced software platform for Bayesian evolutionary analysisPLoS Comput. Biol.201915e10066501:CAS:528:DC%2BC1MXhtlWlsLzO10.1371/journal.pcbi.1006650
– reference: MinhBQIQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic eraMol. Biol. Evol.202037153015341:CAS:528:DC%2BB3cXis1egsLbL10.1093/molbev/msaa015
– reference: KoopmansMSARS-CoV-2 and the human-animal interface: outbreaks on mink farmsLancet Infect. Dis.20212118191:CAS:528:DC%2BB3cXisVerurvO10.1016/S1473-3099(20)30912-9
– reference: BoenderGJNodelijkGHagenaarsTJElbersARWde JongMCMLocal spread of classical swine fever upon virus introduction into The Netherlands: mapping of areas at high riskBMC Vet. Res.2008410.1186/1746-6148-4-9
– reference: Aguilo-Gisbert, J. et al. First description of SARS-CoV-2 infection in two feral American mink (Neovison vison) caught in the Wild. Animals (Basel)11, 1422 (2021).
– reference: BoklundAMonitoring of SARS-CoV-2 infection in mustelidsEFSA J.202119e064591:CAS:528:DC%2BB3MXns1Ogsbo%3D337173557926496
– reference: Giner, J. et al. SARS-CoV-2 seroprevalence in household domestic ferrets (Mustela putorius furo). Animals (Basel)11, 667 (2021).
– reference: El Masry, I. et al. The likelihood of exposure of humans or animals to SARS-CoV-2 from wild, livestock, companion and aquatic animals: qualitative exposure assessment. FAO Animal Production and Health. Paper 181 (FAO, 2020).
– reference: LiHMinimap2: pairwise alignment for nucleotide sequencesBioinformatics201834309431001:CAS:528:DC%2BC1MXhtVamu73J10.1093/bioinformatics/bty191
– reference: Larsen, H. D. et al. Preliminary report of an outbreak of SARS-CoV-2 in mink and mink farmers associated with community spread, Denmark, June to November 2020. Euro Surveill.26, 2100009 (2021).
– reference: ChawSMThe origin and underlying driving forces of the SARS-CoV-2 outbreakJ. Biomed. Sci.202027731:CAS:528:DC%2BB3cXhtFSqtbfN10.1186/s12929-020-00665-8
– reference: Liu, Z. et al. Identification of SARS-CoV-2 spike mutations that attenuate monoclonal and serum antibody neutralization Cell Host Microbehttps://doi.org/10.1016/j.chom.2021.01.014 (2021).
– reference: van Aart, A. E. et al. SARS-CoV-2 infection in cats and dogs in infected mink farms. Transbound Emerg. Dis.https://doi.org/10.1111/tbed.14173 (2021).
– reference: Van der Heijden, HMJF et al. Serological screening of Dutch mink for SARS-CoV2 by ELISA, in preparation. (2021).
– reference: O’BrienJDMininVNSuchardMALearning to count: robust estimates for labeled distances between molecular sequencesMol. Biol. Evol.20092680181410.1093/molbev/msp003
– reference: ShrinerSASARS-CoV-2 exposure in escaped mink, Utah, USAEmerg. Infect. Dis.2021279889901:CAS:528:DC%2BB3MXhtlWgtbjO10.3201/eid2703.204444
– reference: PetersenEComparing SARS-CoV-2 with SARS-CoV and influenza pandemicsLancet Infect. Dis.202020e238e2441:CAS:528:DC%2BB3cXhtlegu7rE10.1016/S1473-3099(20)30484-9
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Snippet 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...
SARS-CoV-2 was detected in mink farms in the Netherlands in the first wave of the pandemic with evidence of human-to-mink and mink-to-human transmission. Here,...
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45/47
45/77
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631/181/735
631/326/421
631/326/596/2562
631/326/596/4130
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Amino Acid Sequence
Amino acid substitution
Amino acids
Animal Diseases - epidemiology
Animal Diseases - transmission
Animal Diseases - virology
Animal human relations
Animals
Bayes Theorem
Bayesian analysis
COVID-19
COVID-19 - epidemiology
COVID-19 - transmission
COVID-19 - virology
Disease Outbreaks
Dispersal
Epidemiology
Evolution, Molecular
Farms
Farmworkers
Humanities and Social Sciences
Humans
Mink - virology
multidisciplinary
Mustela
Netherlands - epidemiology
Outbreaks
Pandemics
Personnel
Phylogeny
SARS-CoV-2 - genetics
SARS-CoV-2 - isolation & purification
SARS-CoV-2 - physiology
Science
Science (multidisciplinary)
Sequence Analysis, Protein
Severe acute respiratory syndrome coronavirus 2
Spike Glycoprotein, Coronavirus - classification
Spike Glycoprotein, Coronavirus - genetics
Spike protein
Statistical analysis
Viral diseases
Whole genome sequencing
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Title Adaptation, spread and transmission of SARS-CoV-2 in farmed minks and associated humans in the Netherlands
URI https://link.springer.com/article/10.1038/s41467-021-27096-9
https://www.ncbi.nlm.nih.gov/pubmed/34815406
https://www.proquest.com/docview/2601151992
https://www.proquest.com/docview/2601995876
https://pubmed.ncbi.nlm.nih.gov/PMC8611045
https://doaj.org/article/6d32ab4b74c24337a5d889e4f5b33778
Volume 12
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