Study population and setting
In light of previous studies finding that white-tailed deer (Odocoileus virginianus) are susceptible to infection with SARS-CoV-2 and capable of indirect transmission in an experimental setting (https://doi.org/10.1128/JVI.00083-21 [https://doi.org/10.1128/JVI.00083-21]) and that free-living deer populations in four US states show serological evidence of SARS-CoV-2 (https://doi.org/10.1073/pnas.2114828118 [https://doi.org/10.1073/pnas.2114828118]), the authors of this study wanted to test whether deer are actively infected with SARS-CoV-2 in Ohio, USA. Between January and March 2021, 360 wild white-tailed deer were culled at nine study sites in northeast Ohio as part of a deer population management program. Nasal swabs were collected from each carcass in the field. Viral RNA was detected in nasal swab samples by real-time polymerase chain reaction (RT-PCR) targeting the SARS-CoV-2 envelope gene; additional RT-PCR assays were performed targeting other genes confirmed the results of the first assay. Presumptive positive samples following RT-PCR screening were sent to the National Veterinary Services Laboratories for whole genome sequencing. After assembly and cleaning, the genomes were assigned to SARS-CoV-2 genetic lineages according to the Pangolin program. Phylogenetic analysis was then performed to compare the genomes from deer to a background dataset compiled from GISAID that included all SARS-Cov-2 sequences from human cases in Ohio during the study period.
Summary of Main Findings
From the 360 nasal swabs collected from deer, 129 (35.8%) were positive for SARS-CoV-2 RNA by RT-PCR over the whole study period. Prevalence estimates varied from 9% to 75% depending on the site and date of sampling. Male deer were more likely to test positive than female deer (chi-squared = 25.45, p-value < 0.0005), and the highest prevalence estimates were observed at four sites nearby urban areas with higher human population densities. Whole genome sequences were obtained from 14 samples across six sites, with lineages including B.1.2, B.1.596, and B.1.582; no Alpha (B.1.1.7) or Delta (B.1.617.2) variants identified. Several sites had multiple deer infected with the same lineage, suggesting deer-to-deer viral transmission. The largest cluster had seven deer sequenced that fell together into clade B.1.596 and had unique amino acid substitutions and deletions that distinguished the genomes from related SARS-CoV-2 genotypes from human cases in the same lineage. Additionally, three distinct clusters of B.1.2 genotypes in deer were detected at different sites, suggesting independent spillover events. Considering all the distinct phylogenetic clusters identified in deer, the authors estimated that there had been at least six independent spillover events from humans to deer that occurred prior to the study period, likely during the winter surge of human SARS-CoV-2 cases in Ohio.
The sample collection was fortuitous, occurring several weeks after the peak in the winter surge of SARS-CoV-2 in Ohio, when human-to-deer transmission would presumably have been the highest. The collection of samples from multiple sites and the full genome sequencing was important to determining that multiple human-to-deer transmission events had occurred and that unique variants of some lineages (e.g., B.1.596) were likely spreading between deer at some sites.
A similar preprint about SARS-CoV-2 RNA detection in white-tailed deer in Iowa was posted only days before this article (https://doi.org/10.1101/2021.10.31.466677), reporting multiple SARS-CoV-2 lineages in the sampled deer, including B.1.2 and B.1.596. However, because the two studies were posted so close together in time, it is unknown whether genotypes in these lineages are shared between deer populations in the two states, which might suggest specific adaptation of the virus to deer, as happened in outbreaks of SARS-CoV-2 in farmed mink. For Ohio sites where only one deer sample was sequenced, it unknown whether deer-to-deer transmission was occurring or not. Moreover, the dynamics of deer-to-deer transmission and whether infection is causing disease and mortality in deer within the Ohio sites cannot be inferred from the limited genetic data. More longitudinal surveillance will be needed. Finally, it is unclear from this study alone how deer are become exposed (e.g., direct exposure to humans in yards or during hunting, or indirectly through contaminated water or trash) and transmitting the virus to each other (e.g., direct contact, airborne, or environmental).
This study provides direct evidence that free-living white-tailed deer are becoming infected with SARS-CoV-2 via direct or indirect contact with infected humans or contaminated materials. The results corroborate similar findings published contemporaneously (https://doi.org/10.1101/2021.10.31.466677 [https://doi.org/10.1101/2021.10.31.466677]), wherein 94/283 (33.2%) sampled deer (151 free-living and 132 captive) in Iowa between April 2020 and January 2021 were positive for SARS-CoV-2 RNA by RT-PCR. Because white-tailed deer are widespread in the United States and live in areas spanning the rural-urban spectrum, sometimes at high densities, there are likely many opportunities for exposure to SARS-CoV-2 circulating in human populations. If similar human-to-deer transmission events are occurring in many other states, and if deer-to-deer transmission is efficient, then this presents a risk that SARS-CoV-2 may become established in deer populations and potentially lead to deer-to-human transmission events.