Detection of SARS-CoV-2 Omicron variant (B.1.1.529) infection of white-tailed deer

White-tailed deer (Odocoileus virginianus) are highly susceptible to infection by SARS-CoV-2, with multiple reports of widespread spillover of virus from humans to free-living deer. While the recently emerged SARS-CoV-2 B.1.1.529 Omicron variant of concern (VoC) has been shown to be notably more transmissible amongst humans, its ability to cause infection and spillover to non-human animals remains a challenge of concern. We found that 19 of the 131 (14.5%; 95% CI: 0.10–0.22) white-tailed deer opportunistically sampled on Staten Island, New York, between December 12, 2021, and January 31, 2022, were positive for SARS-CoV-2 specific serum antibodies using a surrogate virus neutralization assay, indicating prior exposure. The results also revealed strong evidence of age-dependence in antibody prevalence. A significantly (χ2, p < 0.001) greater proportion of yearling deer possessed neutralizing antibodies as compared with fawns (OR=12.7; 95% CI 4–37.5). Importantly, SARS-CoV-2 nucleic acid was detected in nasal swabs from seven of 68 (10.29%; 95% CI: 0.0–0.20) of the sampled deer, and whole-genome sequencing identified the SARS-CoV-2 Omicron VoC (B.1.1.529) is circulating amongst the white-tailed deer on Staten Island. Phylogenetic analyses revealed the deer Omicron sequences clustered closely with other, recently reported Omicron sequences recovered from infected humans in New York City and elsewhere, consistent with human to deer spillover. Interestingly, one individual deer was positive for viral RNA and had a high level of neutralizing antibodies, suggesting either rapid serological conversion during an ongoing infection or a “breakthrough” infection in a previously exposed animal. Together, our findings show that the SARS-CoV-2 B.1.1.529 Omicron VoC can infect white-tailed deer and highlights an urgent need for comprehensive surveillance of susceptible animal species to identify ecological transmission networks and better assess the potential risks of spillback to humans. Key Findings These studies provide strong evidence of infection of free-living white-tailed deer with the SARS-CoV-2 B.1.1.529 Omicron variant of concern on Staten Island, New York, and highlight an urgent need for investigations on human-to-animal-to-human spillovers/spillbacks as well as on better defining the expanding host-range of SARS-CoV-2 in non-human animals and the environment.

[1]  S. Mallapaty Where did Omicron come from? Three key theories , 2022, Nature.

[2]  Su Datt Lam,et al.  Transmission of SARS-CoV-2 from humans to animals and potential host adaptation , 2022, Nature Communications.

[3]  James J. Davis,et al.  Multiple spillovers from humans and onward transmission of SARS-CoV-2 in white-tailed deer , 2022, Proceedings of the National Academy of Sciences.

[4]  G. Ichihara,et al.  Higher viral load and infectivity increase risk of aerosol transmission for Delta and Omicron variants of SARS-CoV-2. , 2022, Swiss medical weekly.

[5]  M. Mulumba,et al.  SARS-CoV-2 Reverse Zoonoses to Pumas and Lions, South Africa , 2022, Viruses.

[6]  J. Andriesen,et al.  High Rate of Asymptomatic Carriage Associated with Variant Strain Omicron , 2021, medRxiv.

[7]  M. Nelson,et al.  SARS-CoV-2 infection in free-ranging white-tailed deer , 2021, Nature.

[8]  J. Morrill,et al.  SARS-CoV-2 Neutralizing Antibodies in White-Tailed Deer from Texas , 2021, Vector borne and zoonotic diseases.

[9]  E. Marqueze,et al.  Nucleocapsid (N) Gene Mutations of SARS-CoV-2 Can Affect Real-Time RT-PCR Diagnostic and Impact False-Negative Results , 2021, Viruses.

[10]  J. Richt,et al.  Natural and Experimental SARS-CoV-2 Infection in Domestic and Wild Animals , 2021, Viruses.

[11]  R. Gibbs,et al.  Transmission event of SARS-CoV-2 delta variant reveals multiple vaccine breakthrough infections , 2021, BMC Medicine.

[12]  A. García-Sastre,et al.  Infection and transmission of ancestral SARS-CoV-2 and its alpha variant in pregnant white-tailed deer , 2021, bioRxiv.

[13]  Julianna B. Lenoch,et al.  SARS-CoV-2 exposure in wild white-tailed deer (Odocoileus virginianus) , 2021, Proceedings of the National Academy of Sciences.

[14]  James J. Davis,et al.  Trajectory of Growth of Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Variants in Houston, Texas, January through May 2021, Based on 12,476 Genome Sequences , 2021, The American Journal of Pathology.

[15]  James J. Davis,et al.  Delta Variants of SARS-CoV-2 Cause Significantly Increased Vaccine Breakthrough COVID-19 Cases in Houston, Texas , 2021, The American Journal of Pathology.

[16]  O. Pybus,et al.  Assignment of epidemiological lineages in an emerging pandemic using the pangolin tool , 2021, Virus evolution.

[17]  R. Gibbs,et al.  Transmission event of SARS-CoV-2 delta variant reveals multiple vaccine breakthrough infections , 2021, BMC Medicine.

[18]  K. Korn,et al.  SARS-CoV-2 N gene dropout and N gene Ct value shift as indicator for the presence of B.1.1.7 lineage in a commercial multiplex PCR assay , 2021, Clinical Microbiology and Infection.

[19]  James J. Davis,et al.  Sequence Analysis of 20,453 Severe Acute Respiratory Syndrome Coronavirus 2 Genomes from the Houston Metropolitan Area Identifies the Emergence and Widespread Distribution of Multiple Isolates of All Major Variants of Concern , 2021, The American Journal of Pathology.

[20]  J. Tang,et al.  Clinical performance of Roche cobas 6800, Luminex ARIES, MiRXES Fortitude Kit 2.1, Altona RealStar, and Applied Biosystems TaqPath for SARS‐CoV‐2 detection in nasopharyngeal swabs , 2021, Journal of medical virology.

[21]  Megan M. Sheehan,et al.  Reinfection Rates among Patients who Previously Tested Positive for COVID-19: a Retrospective Cohort Study , 2021, medRxiv.

[22]  M. Palmer,et al.  Susceptibility of White-Tailed Deer (Odocoileus virginianus) to SARS-CoV-2 , 2021, Journal of Virology.

[23]  A. Venkatakrishnan,et al.  Long-term SARS-CoV-2 RNA shedding and its temporal association to IgG seropositivity , 2020, Cell death discovery.

[24]  A. Pandya,et al.  Emerging diagnostic tools for detection of COVID-19 and perspective , 2020, Biomedical Microdevices.

[25]  E. Hobbs,et al.  Animals and SARS‐CoV‐2: Species susceptibility and viral transmission in experimental and natural conditions, and the potential implications for community transmission , 2020, Transboundary and emerging diseases.

[26]  Andreas R. Pfenning,et al.  Broad host range of SARS-CoV-2 predicted by comparative and structural analysis of ACE2 in vertebrates , 2020, Proceedings of the National Academy of Sciences.

[27]  Harjeet Singh,et al.  Coronavirus Pathogenesis and the Emerging Pathogen Severe Acute Respiratory Syndrome , 2020 .

[28]  M. Chen,et al.  A SARS-CoV-2 surrogate virus neutralization test based on antibody-mediated blockage of ACE2–spike protein–protein interaction , 2020, Nature Biotechnology.

[29]  A. Rai,et al.  Types of Assays for SARS-CoV-2 Testing: A Review , 2020, Laboratory medicine.

[30]  A. Venkatakrishnan,et al.  Long-term SARS-CoV-2 RNA Shedding and its Temporal Association to IgG Seropositivity , 2020, Cell Death Discovery.

[31]  M. Koopmans,et al.  SARS-CoV-2 infection in farmed minks, the Netherlands, April and May 2020 , 2020, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[32]  E. Holmes,et al.  A new coronavirus associated with human respiratory disease in China , 2020, Nature.

[33]  Rick L. Stevens,et al.  The PATRIC Bioinformatics Resource Center: expanding data and analysis capabilities , 2019, Nucleic Acids Res..

[34]  Ryan R. Wick,et al.  Performance of neural network basecalling tools for Oxford Nanopore sequencing , 2019, Genome Biology.

[35]  Karthik Gangavarapu,et al.  An amplicon-based sequencing framework for accurately measuring intrahost virus diversity using PrimalSeq and iVar , 2018, Genome Biology.

[36]  Heng Li,et al.  Minimap2: pairwise alignment for nucleotide sequences , 2017, Bioinform..

[37]  Stefan Elbe,et al.  Data, disease and diplomacy: GISAID's innovative contribution to global health , 2017, Global challenges.

[38]  Ralph S. Baric,et al.  Recombination, Reservoirs, and the Modular Spike: Mechanisms of Coronavirus Cross-Species Transmission , 2009, Journal of Virology.

[39]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[40]  S. Weiss,et al.  Coronavirus Pathogenesis and the Emerging Pathogen Severe Acute Respiratory Syndrome Coronavirus , 2005, Microbiology and Molecular Biology Reviews.

[41]  H. Yen,et al.  Transmission of SARS-CoV-2 (Variant Delta) from Pet Hamsters to Humans and Onward Human Propagation of the Adapted Strain: A Case Study , 2022, SSRN Electronic Journal.

[42]  Peer Bork,et al.  Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation , 2007, Bioinform..