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

Lu Lu; Reina S. Sikkema; Francisca C. Velkers; David F. Nieuwenhuijse; Egil A.J. Fischer; Paola A. Meijer; Noortje Bouwmeester-Vincken; Ariene Rietveld; Marjolijn C.A. Wegdam-Blans; Paulien Tolsma; Marco Koppelman; Lidwien A.M. Smit; Renate W. Hakze-van der Honing; Wim H.M. van der Poel; Arco N. van der Spek; Marcel A.H. Spierenburg; Robert Jan Molenaar; Jan de Rond; Marieke Augustijn; Mark Woolhouse; J. Arjan Stegeman; Samantha Lycett; Bas B. Oude Munnink; Marion P.G. Koopmans

doi:10.1038/s41467-021-27096-9

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

Lu Lu, Reina S. Sikkema, Francisca C. Velkers, David F. Nieuwenhuijse, Egil A.J. Fischer, Paola A. Meijer, Noortje Bouwmeester-Vincken, Ariene Rietveld, Marjolijn C.A. Wegdam-Blans, Paulien Tolsma, Marco Koppelman, Lidwien A.M. Smit, Renate W. Hakze-van der Honing, Wim H.M. van der Poel, Arco N. van der Spek, Marcel A.H. Spierenburg, Robert Jan Molenaar, Jan de Rond, Marieke Augustijn, Mark WoolhouseJ. Arjan Stegeman, Samantha Lycett, Bas B. Oude Munnink, Marion P.G. Koopmans^*

^*Corresponding author for this work

Virology

Research output: Contribution to journal › Article › Academic › peer-review

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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.

Original language	English
Article number	6802
Journal	Nature Communications
Volume	12
Issue number	1
DOIs	https://doi.org/10.1038/s41467-021-27096-9
Publication status	Published - 23 Nov 2021

Bibliographical note

Funding Information:
We acknowledge the authors, originating and submitting laboratories of the sequences from GISAID’s EpiCov Database on which the phylogenetic analysis was based (see Supplementary Data 1). All submitters of data may be contacted directly via the GISAID website www.gisaid.org. This work is supported by European Union’s Horizon 2020 research and innovation programme under Grant No. 874735 (VEO), received by L.L., S.L., M.W., R.S.S., B.B.O.M., M.P.G.K. and D.F.N., as well as ZonMW under Grant No.10150062010005, received by R.S.S., D.F.N., M.P.G.K. and B.B.O.M. The mink farm outbreak investigation was funded by the Dutch Ministries of Health, Welfare and Sport, and of Agriculture, Nature and Food Quality under Grant No. 1400011731, 1400011746 and 1400010752, received by R.S., F.C.V., D.F.M., E.A.J.F., P.A.M., L.A.M.S., R.W.H.H., W.H.M.P., R.J.M., J.R., M.A., J.A.S., B.O.M. and M.P.G.K.; S.L. is additionally supported by Biotechnology and Biological Sciences Research Council (BBSRC) programme grant to Roslin Institute (Award Number BBS/E/D/20002173.

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© 2021, The Author(s).

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Adaptation, spread and transmission of SARS-CoV-2 in farmed minks and associated humans in the NetherlandsFinal published version, 6.25 MBLicence: CC BY

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Lu, L., Sikkema, R. S., Velkers, F. C., Nieuwenhuijse, D. F., Fischer, E. A. J., Meijer, P. A., Bouwmeester-Vincken, N., Rietveld, A., Wegdam-Blans, M. C. A., Tolsma, P., Koppelman, M., Smit, L. A. M., Hakze-van der Honing, R. W., van der Poel, W. H. M., van der Spek, A. N., Spierenburg, M. A. H., Molenaar, R. J., Rond, J. D., Augustijn, M., ... Koopmans, M. P. G. (2021). Adaptation, spread and transmission of SARS-CoV-2 in farmed minks and associated humans in the Netherlands. Nature Communications, 12(1), Article 6802. https://doi.org/10.1038/s41467-021-27096-9

@article{f23bde6cf29b4beb8f94a8a860bf6f96,

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

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.",

author = "Lu Lu and Sikkema, {Reina S.} and Velkers, {Francisca C.} and Nieuwenhuijse, {David F.} and Fischer, {Egil A.J.} and Meijer, {Paola A.} and Noortje Bouwmeester-Vincken and Ariene Rietveld and Wegdam-Blans, {Marjolijn C.A.} and Paulien Tolsma and Marco Koppelman and Smit, {Lidwien A.M.} and {Hakze-van der Honing}, {Renate W.} and {van der Poel}, {Wim H.M.} and {van der Spek}, {Arco N.} and Spierenburg, {Marcel A.H.} and Molenaar, {Robert Jan} and Rond, {Jan de} and Marieke Augustijn and Mark Woolhouse and Stegeman, {J. Arjan} and Samantha Lycett and {Oude Munnink}, {Bas B.} and Koopmans, {Marion P.G.}",

note = "Funding Information: We acknowledge the authors, originating and submitting laboratories of the sequences from GISAID{\textquoteright}s EpiCov Database on which the phylogenetic analysis was based (see Supplementary Data 1). All submitters of data may be contacted directly via the GISAID website www.gisaid.org. This work is supported by European Union{\textquoteright}s Horizon 2020 research and innovation programme under Grant No. 874735 (VEO), received by L.L., S.L., M.W., R.S.S., B.B.O.M., M.P.G.K. and D.F.N., as well as ZonMW under Grant No.10150062010005, received by R.S.S., D.F.N., M.P.G.K. and B.B.O.M. The mink farm outbreak investigation was funded by the Dutch Ministries of Health, Welfare and Sport, and of Agriculture, Nature and Food Quality under Grant No. 1400011731, 1400011746 and 1400010752, received by R.S., F.C.V., D.F.M., E.A.J.F., P.A.M., L.A.M.S., R.W.H.H., W.H.M.P., R.J.M., J.R., M.A., J.A.S., B.O.M. and M.P.G.K.; S.L. is additionally supported by Biotechnology and Biological Sciences Research Council (BBSRC) programme grant to Roslin Institute (Award Number BBS/E/D/20002173. Publisher Copyright: {\textcopyright} 2021, The Author(s).",

year = "2021",

month = nov,

day = "23",

doi = "10.1038/s41467-021-27096-9",

language = "English",

volume = "12",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Nature Research",

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Lu, L, Sikkema, RS, Velkers, FC, Nieuwenhuijse, DF, Fischer, EAJ, Meijer, PA, Bouwmeester-Vincken, N, Rietveld, A, Wegdam-Blans, MCA, Tolsma, P, Koppelman, M, Smit, LAM, Hakze-van der Honing, RW, van der Poel, WHM, van der Spek, AN, Spierenburg, MAH, Molenaar, RJ, Rond, JD, Augustijn, M, Woolhouse, M, Stegeman, JA, Lycett, S, Oude Munnink, BB & Koopmans, MPG 2021, 'Adaptation, spread and transmission of SARS-CoV-2 in farmed minks and associated humans in the Netherlands', Nature Communications, vol. 12, no. 1, 6802. https://doi.org/10.1038/s41467-021-27096-9

TY - JOUR

T1 - Adaptation, spread and transmission of SARS-CoV-2 in farmed minks and associated humans in the Netherlands

AU - Lu, Lu

AU - Sikkema, Reina S.

AU - Velkers, Francisca C.

AU - Nieuwenhuijse, David F.

AU - Fischer, Egil A.J.

AU - Meijer, Paola A.

AU - Bouwmeester-Vincken, Noortje

AU - Rietveld, Ariene

AU - Wegdam-Blans, Marjolijn C.A.

AU - Tolsma, Paulien

AU - Koppelman, Marco

AU - Smit, Lidwien A.M.

AU - Hakze-van der Honing, Renate W.

AU - van der Poel, Wim H.M.

AU - van der Spek, Arco N.

AU - Spierenburg, Marcel A.H.

AU - Molenaar, Robert Jan

AU - Rond, Jan de

AU - Augustijn, Marieke

AU - Woolhouse, Mark

AU - Stegeman, J. Arjan

AU - Lycett, Samantha

AU - Oude Munnink, Bas B.

AU - Koopmans, Marion P.G.

N1 - Funding Information: We acknowledge the authors, originating and submitting laboratories of the sequences from GISAID’s EpiCov Database on which the phylogenetic analysis was based (see Supplementary Data 1). All submitters of data may be contacted directly via the GISAID website www.gisaid.org. This work is supported by European Union’s Horizon 2020 research and innovation programme under Grant No. 874735 (VEO), received by L.L., S.L., M.W., R.S.S., B.B.O.M., M.P.G.K. and D.F.N., as well as ZonMW under Grant No.10150062010005, received by R.S.S., D.F.N., M.P.G.K. and B.B.O.M. The mink farm outbreak investigation was funded by the Dutch Ministries of Health, Welfare and Sport, and of Agriculture, Nature and Food Quality under Grant No. 1400011731, 1400011746 and 1400010752, received by R.S., F.C.V., D.F.M., E.A.J.F., P.A.M., L.A.M.S., R.W.H.H., W.H.M.P., R.J.M., J.R., M.A., J.A.S., B.O.M. and M.P.G.K.; S.L. is additionally supported by Biotechnology and Biological Sciences Research Council (BBSRC) programme grant to Roslin Institute (Award Number BBS/E/D/20002173. Publisher Copyright: © 2021, The Author(s).

PY - 2021/11/23

Y1 - 2021/11/23

N2 - 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.

AB - 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.

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VL - 12

JO - Nature Communications

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

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