American mink (Neogale vison) are susceptible to SARS-CoV-2, but little is known about virus circulation in mink since 2021. Here, in the first active surveillance study of SARS-CoV-2 in apparently healthy farmed mink in the United States, we find a ~0.9% (760/85,656) RT-PCR positivity rate among nasal swabs collected in 18 farms across six states during 2022-2023. Phylogenetic analysis of 293 viral genome sequences shows that human-adapted SARS-CoV-2 variants (e.g., Omicron) repeatedly spill over into mink. Surprisingly, the detection of a Delta lineage virus (AY.39) on a mink farm four months after its last detection in humans within the same state suggests prolonged unsampled transmission. The spread of mink-adapted AY.39 viruses from a mink farm to neighboring free-ranging white-tailed deer represents a rare instance of SARS-CoV-2 transmission between livestock and wildlife. These findings demonstrate the value of active surveillance for identifying subclinical infections and interspecies transmission between humans, mink, and wildlife.
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SARS-CoV-2 Delta variant re-emerges in US farmed mink and free-ranging white-tailed deer in 2022-2023
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Persistence of SARS-CoV-2 Alpha Variant in White-Tailed Deer, Ohio, USA
Free-ranging white-tailed deer (WTD) are highly susceptible to the SARS-CoV-2 virus. Through an opportunistic sampling of WTD in northeast Ohio, USA, during January-March 2023, we identified 6 SARS-CoV-2 lineages from 36 sequences using the pangolin lineages tool, including the B.1.1.7 lineage (Alpha variant) and BQ.1.1, BQ.1.1.63, BQ.1.1.67, BQ.1.23, and XBB.1.5.35 lineages (Omicron variant). The Alpha variant, introduced by a single human-to-deer transmission event, was detected in 5 WTD in January 2023, more than 1 year after the most recent detection of the Alpha variant in humans in Ohio (August 2021). A genetically similar B.1.1.7 lineage virus from WTD in a nearby county in Pennsylvania was positioned with our Ohio deer transmission cluster, suggesting deer-to-deer transmission. The persistence of the Alpha variant in WTD in Ohio warrants continued surveillance to monitor if WTD can become a reservoir for displaced SARS-CoV-2 variants.
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Accelerated evolution of SARS-CoV-2 in free-ranging white-tailed deer
The zoonotic origin of the COVID-19 pandemic virus highlights the need to fill the vast gaps in our knowledge of SARS-CoV-2 ecology and evolution in non-human hosts. Here, we detected that SARS-CoV-2 was introduced from humans into white-tailed deer more than 30 times in Ohio, USA during November 2021-March 2022. Subsequently, deer-to-deer transmission persisted for 2-8 months, disseminating across hundreds of kilometers. Newly developed Bayesian phylogenetic methods quantified how SARS-CoV-2 evolution is not only three-times faster in white-tailed deer compared to the rate observed in humans but also driven by different mutational biases and selection pressures. The long-term effect of this accelerated evolutionary rate remains to be seen as no critical phenotypic changes were observed in our animal models using white-tailed deer origin viruses. Still, SARS-CoV-2 has transmitted in white-tailed deer populations for a relatively short duration, and the risk of future changes may have serious consequences for humans and livestock.
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SARS-CoV-2 Neutralizing Antibodies in Free-Ranging Fallow Deer (Dama dama) and Red Deer (Cervus elaphus) in Suburban and Rural Areas in Spain
Effective control of zoonotic infectious diseases requires identifying the animal species involved in the infectious cycle as transmitters or reservoirs where the pathogen could persist and evolve, increasing the risk of reintroduction of new variants in humans and animals. Multiple surveillance studies have detected the presence of severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) or specific antibodies in free-ranging white-tailed deer (Odocoileus virginianus) in North America, being the wild mammal species with the most reported cases of SARS-CoV-2 infection. However, so far, all attempts to detect the infection in European cervids have been unsuccessful. In this study, we demonstrated the presence of specific antibodies against SARS-CoV-2 in European fallow deer (Dama dama) and red deer (Cervus elaphus) in Spain. However, all samples of European roe deer (Capreolus capreolus), taxonomically related to the American white-tailed deer, were seronegative for the virus. We tested 215 serum samples from roe deer (n = 116), red deer (n = 63), and fallow deer (n = 36) collected in eight provinces of central-southern Spain between 2017 and 2022. We first screened sera by a surrogate virus neutralization test (sVNT) ELISA based on the binding of the receptor-binding domain of SARS-CoV-2 to the angiotensin-converting enzyme 2 (ACE2) receptor and then confirmed positive samples by a conventional virus neutralization test (cVNT) against the Alpha, Delta, and Omicron variants. Four fallow deer and two red deer samples were seropositive in both neutralization assays. Four samples of fallow deer and one of red deer, collected in a suburban park near Madrid in February 2022, had antibodies against the Alpha, Delta, and Omicron variants, while a seropositive sample of red deer, collected in a rural area in February 2021, was specific for the Delta variant. All samples collected before the start of the pandemic in Spain were seronegative for sVNT, which also indicates that there are not cross-reactive antibodies potentially elicited by other viruses antigenically related to SARS-CoV-2. The results indicate probable human-to-deer transmission of SARS-CoV-2, but do not clarify whether there was subsequent spread within herds.
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The Evolution of SARS-CoV-2 and Influenza A Virus at the Human–Animal Interface
In the wake of the COVID-19 pandemic, there has never been stronger universal recognition of the need for more studies of virus spillover at the human–animal interface to combat the growing threat of emerging zoonotic diseases. We learned a great deal from the 2009 H1N1 pandemic and prior influenza pandemics about the molecular changes that allow certain viruses to overcome these host-restriction barriers. Moreover, large-scale genomic sequencing is beginning to expose the high frequency of virus spillover between humans and animals and refine our understanding of its bidirectional nature. For example, it turns out humans actually transmit more flu to pigs than the reverse, turning swine into breeding grounds for new chimeric viruses with genetic components from humans, birds, and pigs. Intensified surveillance during the COVID-19 pandemic revealed that reverse zoonosis transmission from humans to animals occurs not only in livestock and pets with high contact rates but also to wildlife, including white-tailed deer, exposing blind spots in our understanding of the human–animal interface for pandemic pathogens.
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SARS-CoV-2 infection in free-ranging white-tailed deer
Humans have infected a wide range of animals with SARS-CoV-21-5, but the establishment of a new natural animal reservoir has not been observed. Here we document that free-ranging white-tailed deer (Odocoileus virginianus) are highly susceptible to infection with SARS-CoV-2, are exposed to multiple SARS-CoV-2 variants from humans and are capable of sustaining transmission in nature. Using real-time PCR with reverse transcription, we detected SARS-CoV-2 in more than one-third (129 out of 360, 35.8%) of nasal swabs obtained from O. virginianus in northeast Ohio in the USA during January to March 2021. Deer in six locations were infected with three SARS-CoV-2 lineages (B.1.2, B.1.582 and B.1.596). The B.1.2 viruses, dominant in humans in Ohio at the time, infected deer in four locations. We detected probable deer-to-deer transmission of B.1.2, B.1.582 and B.1.596 viruses, enabling the virus to acquire amino acid substitutions in the spike protein (including the receptor-binding domain) and ORF1 that are observed infrequently in humans. No spillback to humans was observed, but these findings demonstrate that SARS-CoV-2 viruses have been transmitted in wildlife in the USA, potentially opening new pathways for evolution. There is an urgent need to establish comprehensive ‘One Health’ programmes to monitor the environment, deer and other wildlife hosts globally.