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

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.

Lack of detection of SARS-CoV-2 in British wildlife 2020-21 and first description of a stoat (Mustela erminea) Minacovirus

“…The detection of another coronavirus in this study, however, indicates that the methods used and sample preservation were adequate for viral detection, at least at high prevalence, even in small populations of samples. Our study is also in line with other European wildlife studies indicating absence of widespread SARS-CoV-2 circulation in wild small carnivores and rodents, including wild American mink (Davoust, Guérin et al 2022, Keller, Peter et al 2022, Sikkema, Begeman et al 2022, Villanueva-Saz, Giner et al 2022, Wernike, Drewes et al 2022, Carmona, Burgos et al 2023, Zamperin, Festa et al 2023). Detection of SARS-CoV-2 in one Eurasian river otter in lung tissue and nasal swabs and detection of a Eurasian badger specific coronavirus in lung tissue from similar post mortem monitoring programmes indicates that lungs are an appropriate target tissue for coronavirus monitoring in those species (Padilla-Blanco, Aguiló-Gisbert et al 2022, Zamperin, Festa et al 2023).…”

“…Thus far, no infection with SARS-CoV-2 has been reported in Horseshoe bats ( Rhinopholus spp) in Britain or mainland Europe (Orłowska, Smreczak et al 2022, Sander, Moreira-Soto et al 2022, Apaa, Withers et al 2023) although other related coronaviruses have been detected in these species. Reports in European deer prior to 2022 all failed to detect any exposure (Holding, Otter et al 2022, Moreira-Soto, Walzer et al 2022, Wernike, Fischer et al 2022), however 57% of fallow deer in Dublin seroconverted in early 2022 (Purves, Brown et al 2023) and sporadic seropositivity in fallow and red deer in Spain in 2021-22 has also been reported (Encinas, Escalera et al 2023) Wild animal surveillance studies in mainland Europe have indicated sporadic detection in wild mustelids, including by qPCR in wild American mink ( N.vison) , particularly near farmed mink outbreaks, and one otter ( L. lutra ) (Aguiló-Gisbert, Padilla-Blanco et al 2021, Padilla-Blanco, Aguiló-Gisbert et al 2022, Sikkema, Begeman et al 2022). Serological evidence of exposure has been described in 3/14 pine martens ( M. martes ) and 2/10 badgers ( M. meles ) (Davoust, Guérin et al 2022), but other studies found no evidence of infection in 48 polecats ( Mustela putorius ), 163 badgers or cricetid and murid rodents (694 M. glareolus , 2 Microtus arvalis , 27 M. musculus , 97 R. norvegicus and 8 Apodemus species) (Wernike, Drewes et al 2022, Carmona, Burgos et al 2023, Zamperin, Festa et al 2023).…”

Avian influenza overview December 2022 – March 2023

“…The feed of the minks included raw poultry by-products, but there had been no HPAI A(H5N1) virus outbreaks in the region from where these by-products were obtained, whereas several HPAI A(H5N1) cases in yellow-legged gulls and northern gannets were detected in that region. Given that the open housing system of mink farming is known to allow the access to wildlife including wild birds into the farms, and that direct contact with mink is possible (European Food Safety et al, 2021;Sikkema et al, 2022), the mink may have been in contact with infected wild birds that were attracted to the mink feed. However, it is difficult to explain all the infections of mink by bird-to-mink contact.…”

Lack of detection of SARS-CoV-2 in British wildlife 2020–21 and first description of a stoat (Mustela erminea) Minacovirus

“…Reports in European deer prior to 2022 all failed to detect any exposure [31][32][33], but 57 % of fallow deer in Dublin, Ireland, seroconverted in early 2022 [34] and sporadic seropositivity in fallow and red deer in Spain in 2021-22 has also been reported [35]. Wild animal surveillance studies in mainland Europe have indicated sporadic detection in wild mustelids, including by quantitative (q)PCR in wild American mink (N. vison), particularly near farmed mink outbreaks, and one otter (L. lutra) [36][37][38]. Serological evidence of exposure has been described in 3/14 pine martens (Martes martes) and 2/10 badgers (Meles meles) [39], but other studies found no evidence of infection in 48 polecats (Mustela putorius), 163 badgers or cricetid and murid rodents (694 Myodes glareolus, two Microtus arvalis, 27 Mus musculus, 97 R. norvegicus and eight Apodemus species) [40][41][42].…”