SARS-CoV-2 infection in free-ranging white-tailed deer ( Odocoileus virginianus )

  1. Vanessa L. Hale
  2. Patricia M. Dennis
  3. Dillon S. McBride
  4. Jaqueline M. Nolting
  5. Christopher Madden
  6. Devra Huey
  7. Margot Ehrlich
  8. Jennifer Grieser
  9. Jenessa Winston
  10. Dusty Lombardi
  11. Stormy Gibson
  12. Linda Saif
  13. Mary L. Killian
  14. Kristina Lantz
  15. Rachel Tell
  16. Mia Torchetti
  17. Suelee Robbe-Austerman
  18. Martha I. Nelson
  19. Seth A. Faith
  20. Andrew S. Bowman

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Abstract

Human-to-animal spillover of SARS-CoV-2 virus has occurred in a wide range of animals, but thus far, the establishment of a new natural animal reservoir has not been detected. Here, we detected SARS-CoV-2 virus using rRT-PCR in 129 out of 360 (35.8%) free-ranging white-tailed deer ( Odocoileus virginianus ) from northeast Ohio (USA) sampled between January-March 2021. Deer in 6 locations were infected with at least 3 lineages of SARS-CoV-2 (B.1.2, B.1.596, B.1.582). The B.1.2 viruses, dominant in Ohio at the time, spilled over multiple times into deer populations in different locations. Deer-to-deer transmission may have occurred in three locations. The establishment of a natural reservoir of SARS-CoV-2 in white-tailed deer could facilitate divergent evolutionary trajectories and future spillback to humans, further complicating long-term COVID-19 control strategies.

One-Sentence Summary

A significant proportion of SARS-CoV-2 infection in free-ranging US white-tailed deer reveals a potential new reservoir.

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  1. ScreenIT

    SciScore for 10.1101/2021.11.04.467308: (What is this?)

    Please note, not all rigor criteria are appropriate for all manuscripts.

    Table 1: Rigor

    Ethicsnot detected.
    Sex as a biological variablenot detected.
    Randomizationnot detected.
    Blindingnot detected.
    Power Analysisnot detected.

    Table 2: Resources

    No key resources detected.

    Results from OddPub: We did not detect open data. We also did not detect open code. Researchers are encouraged to share open data when possible (see Nature blog).

    Results from LimitationRecognizer: An explicit section about the limitations of the techniques employed in this study was not found. We encourage authors to address study limitations.

    Results from TrialIdentifier: No clinical trial numbers were referenced.

    Results from Barzooka: We did not find any issues relating to the usage of bar graphs.

    Results from JetFighter: We did not find any issues relating to colormaps.

    Results from rtransparent:
    • Thank you for including a conflict of interest statement. Authors are encouraged to include this statement when submitting to a journal.
    • Thank you for including a funding statement. Authors are encouraged to include this statement when submitting to a journal.
    • No protocol registration statement was detected.

    Results from scite Reference Check: We found no unreliable references.

    About SciScore

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  2. NCRC

    Our take

    In this preprint that has not yet been peer-reviewed, the authors show that free-living deer populations in Ohio are becoming infected with SARS-CoV-2. This marks the first evidence of SARS-CoV-2 spread within wild animal populations; another paper showing similar results from deer in Iowa was published contemporaneously. The high prevalence (>30%) of viral RNA detection in both studies, plus evidence of distinct viral lineages present in multiple deer within study sites, suggest that multiple human-to-deer spillover events have occurred and that the virus is likely spreading among deer. It is not clear from these studies how animals are becoming exposed to the virus, how transmission between deer occurs, and how widespread and efficient deer-to-deer transmission is in wild populations and more longitudinal studies will be needed to answer these questions.

    Study design

    other

    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.

    Study strengths

    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.

    Limitations

    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).

    Value added

    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.

  3. Version published to 10.1101/2021.11.04.467308v1 on bioRxiv