Risks of SARS-CoV-2 transmission between free-ranging animals and captive mink in the Netherlands

Reina S. Sikkema*, Lineke Begeman, Rene Janssen, Wendy J. Wolters, Corine Geurtsvankessel, Erwin de Bruin, Renate W. Hakze-van der Honing, Phaedra Eble, Wim H. M. van der Poel, Judith M. A. van den Brand, Roy Slaterus, Maurice La Haye, Marion P. G. Koopmans, Francisca Velkers, Thijs Kuiken

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

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Abstract

In the Netherlands, 69 of the 126 (55%) mink farms in total became infected with SARS-CoV-2 in 2020. Despite strict biosecurity measures and extensive epidemiological investigations, the main transmission route remained unclear. A better understanding of SARS-CoV-2 transmission between mink farms is of relevance for countries where mink farming is still common practice and can be used as a case study to improve future emerging disease preparedness. We assessed whether SARS-CoV-2 spilled over from mink to free-ranging animals, and whether free-ranging animals may have played a role in farm-to-farm transmission in the Netherlands. The study encompassed farm visits, farm questionnaires, expert workshops and SARS-CoV-2 RNA and antibody testing of samples from target animal species (bats, birds and free-ranging carnivores). In this study, we show that the open housing system of mink allowed access to birds, bats and most free-ranging carnivores, and that direct and indirect contact with mink was likely after entry, especially for free-ranging carnivores and birds. This allowed SARS-CoV-2 exposure to animals entering the mink farm, and subsequent infection or mechanical carriage by the target animal species. Moreover, mink can escape farms in some cases, and two SARS-CoV-2-positive mink were found outside farm premises. No other SARS-CoV-2-RNA-positive free-ranging animals were detected, suggesting there was no abundant circulation in the species tested during the study period. To investigate previous SARS-CoV-2 infections, SARS-CoV-2 antibody detection using lung extracts of carcasses was set up and validated. One tested beech marten did have SARS-CoV-2 antibodies, but the closest SARS-CoV-2-infected mink farm was outside of its home range, making infection at a mink farm unlikely. Knowing that virus exchange between different species and the formation of animal reservoirs affects SARS-CoV-2 evolution, continued vigilance and monitoring of mink farms and surrounding wildlife remains vital.

Original languageEnglish
Pages (from-to)3339-3349
Number of pages11
JournalTransboundary and Emerging Diseases
Volume69
Issue number6
Early online date21 Aug 2022
DOIs
Publication statusPublished - Nov 2022

Bibliographical note

Funding Information:
We thank all volunteers from the Zoonoses in the Night (ZITN) network, the Dutch Mammal Society and Wageningen Bioveterinary Research (WBVR) for the collection of bat samples and carcasses. Specifically, we thank Sjef Demaret, Jan Jeucken, Chris Driesen, Bernd-Jan Bulsink, Carlo Wijnen, Rob Voesten, Jan van Loon, Bernadette van Noort, Ton Populier, Antoinette van Wilgen, Peter Lina and Erik van Weezep. Also, we thank the Dutch Wildlife Health Centre (DWHC) for coordinating and performing autopsies and collecting samples from dead mustelids. Marco van der Bildt, Vera Mols, Peter van der Run, Anne van der Linden, Lenneke van Rijn and Irina Chestakova of ErasmusMC are thanked for their laboratory analyses and technical support. The input during the expert meetings of veterinarians Cobi Dijkshoorn, Pieter Jacobs, Edwin Vries, Leon Pouwels, Debora Smits, Sjaak de Wit, Manon Houben, Robert Jan Molenaar, Jan de Rond and Marieke Augustijn provided valuable context and information. Bas Hissel and Jacintha van Dijk (SOVON) are thanked for their contribution to the risk assessment for birds. All involved mink farmers are thanked for their cooperation. This study was done as part of the larger One Health investigation of SARS-CoV-2 infections of mink in the Netherlands. We thank all involved researchers and experts who were not specifically mentioned here above: Marieke Augustijn, Jan de Rond and Robert Jan Molenaar (Royal GD), Bas Oude Munnink (Erasmus MC), Arco van der Spek and Marcel Spierenburg (NVWA), Lidwien Smit, Paola Meijer and Arjan Stegeman (Utrecht University). 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. 1400011746. RS and MK receive funding from the European Union's Horizon 2020 Research and Innovation Programme (Grant No. 874735 [VEO]).

Funding Information:
We thank all volunteers from the Zoonoses in the Night (ZITN) network, the Dutch Mammal Society and Wageningen Bioveterinary Research (WBVR) for the collection of bat samples and carcasses. Specifically, we thank Sjef Demaret, Jan Jeucken, Chris Driesen, Bernd‐Jan Bulsink, Carlo Wijnen, Rob Voesten, Jan van Loon, Bernadette van Noort, Ton Populier, Antoinette van Wilgen, Peter Lina and Erik van Weezep. Also, we thank the Dutch Wildlife Health Centre (DWHC) for coordinating and performing autopsies and collecting samples from dead mustelids. Marco van der Bildt, Vera Mols, Peter van der Run, Anne van der Linden, Lenneke van Rijn and Irina Chestakova of ErasmusMC are thanked for their laboratory analyses and technical support. The input during the expert meetings of veterinarians Cobi Dijkshoorn, Pieter Jacobs, Edwin Vries, Leon Pouwels, Debora Smits, Sjaak de Wit, Manon Houben, Robert Jan Molenaar, Jan de Rond and Marieke Augustijn provided valuable context and information. Bas Hissel and Jacintha van Dijk (SOVON) are thanked for their contribution to the risk assessment for birds. All involved mink farmers are thanked for their cooperation. This study was done as part of the larger One Health investigation of SARS‐CoV‐2 infections of mink in the Netherlands. We thank all involved researchers and experts who were not specifically mentioned here above: Marieke Augustijn, Jan de Rond and Robert Jan Molenaar (Royal GD), Bas Oude Munnink (Erasmus MC), Arco van der Spek and Marcel Spierenburg (NVWA), Lidwien Smit, Paola Meijer and Arjan Stegeman (Utrecht University). 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. 1400011746. RS and MK receive funding from the European Union's Horizon 2020 Research and Innovation Programme (Grant No. 874735 [VEO]).

Publisher Copyright:
© 2022 The Authors. Transboundary and Emerging Diseases published by Wiley-VCH GmbH.

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