Multiple spillovers from humans and onward transmission of SARS-CoV-2 in white-tailed deer.

Suresh V Kuchipudi1,2,3 Meera Surendran-Nair4,3 Rachel M Ruden5,6 Michele Yon4 Ruth H Nissly4,3 Kurt J Vandegrift7 Rahul K Nelli6 Lingling Li4 Bhushan M Jayarao4 Costas D Maranas8 Nicole Levine3,9 Katriina Willgert10 Andrew J K Conlan10 Randall J Olsen11,12,13 James J Davis14 James M Musser11,12,13 Peter J Hudson7 Vivek Kapur15,2,9
Affiliations 15 institutions
  1. Animal Diagnostic Laboratory, Department of Veterinary and Biomedical Sciences, The Pennsylvania State University, University Park, PA 16802
  2. [email protected] [email protected].
  3. Huck Institutes of Life Sciences, The Pennsylvania State University, University Park, PA 16802.
  4. Animal Diagnostic Laboratory, Department of Veterinary and Biomedical Sciences, The Pennsylvania State University, University Park, PA 16802.
  5. Wildlife Bureau, Iowa Department of Natural Resources, Des Moines, IA 50319.
  6. Department of Veterinary Diagnostic and Production Animal Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011.
  7. The Center for Infectious Disease Dynamics, Department of Biology and Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA 16802.
  8. Department of Chemical Engineering, The Pennsylvania State University, University Park, PA 16802.
  9. Department of Animal Science, The Pennsylvania State University, University Park, PA 16802.
  10. Disease Dynamics Unit, Department of Veterinary Medicine, University of Cambridge, Cambridge CB3 0ES, United Kingdom.
  11. Laboratory of Molecular and Translational Human Infectious Disease Research, Center for Infectious Diseases, Department of Pathology and Genomic Medicine, Houston Methodist Research Institute, Houston Methodist Hospital, Houston, TX 77030.
  12. Department of Pathology and Laboratory Medicine, Weill Cornell Medical College, New York, NY 10021.
  13. Department of Microbiology and Immunology, Weill Cornell Medical College, New York, NY 10021.
  14. University of Chicago Consortium for Advanced Science and Engineering, University of Chicago and Division of Data Science and Learning, Argonne National Laboratory, Lemont, IL 60439.
  15. Huck Institutes of Life Sciences, The Pennsylvania State University, University Park, PA 16802

Abstract

Many animal species are susceptible to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection and could act as reservoirs; however, transmission in free-living animals has not been documented. White-tailed deer, the predominant cervid in North America, are susceptible to SARS-CoV-2 infection, and experimentally infected fawns can transmit the virus. To test the hypothesis that SARS-CoV-2 is circulating in deer, 283 retropharyngeal lymph node (RPLN) samples collected from 151 free-living and 132 captive deer in Iowa from April 2020 through January of 2021 were assayed for the presence of SARS-CoV-2 RNA. Ninety-four of the 283 (33.2%) deer samples were positive for SARS-CoV-2 RNA as assessed by RT-PCR. Notably, following the November 2020 peak of human cases in Iowa, and coinciding with the onset of winter and the peak deer hunting season, SARS-CoV-2 RNA was detected in 80 of 97 (82.5%) RPLN samples collected over a 7-wk period. Whole genome sequencing of all 94 positive RPLN samples identified 12 SARS-CoV-2 lineages, with B.1.2 (n = 51; 54.5%) and B.1.311 (n = 19; 20%) accounting for ∼75% of all samples. The geographic distribution and nesting of clusters of deer and human lineages strongly suggest multiple human-to-deer transmission events followed by subsequent deer-to-deer spread. These discoveries have important implications for the long-term persistence of the SARS-CoV-2 pandemic. Our findings highlight an urgent need for a robust and proactive "One Health" approach to obtain enhanced understanding of the ecology, molecular evolution, and dissemination of SARS-CoV-2.

Supporting text Virus Host Location
animal reservoir 5 deer 47 One Health 98 SARS-CoV-2 550 spillover 105 Animals 1948 COVID-19 425 Deer 46 Disease Reservoirs 149 Humans 1440 SARS-CoV-2 453 Zoonoses 397

Evidence records

3 total
Zoonotic Surveillance
1 records · 1 evidence types
Evidence type
1 records
OVE5583
Key finding

SARS-CoV-2 RNA was detected by RT-PCR in 94 of 283 retropharyngeal lymph node samples from free-living and captive white-tailed deer in Iowa.

Virus
Host
Location
Supporting text

To test the hypothesis that SARS-CoV-2 is circulating in deer, 283 retropharyngeal lymph node (RPLN) samples collected from 151 free-living and 132 captive deer in Iowa from April 2020 through January of 2021 were assayed for the presence of SARS-CoV-2 RNA. Ninety-four of the 283 (33.2%) deer samples were positive for SARS-CoV-2 RNA as assessed by RT-PCR.

Method
RT-PCR
Sample type
retropharyngeal lymph node samples
Geographic raw
Iowa
Country inferred
USA
Transmission Evidence
1 records · 1 evidence types
Evidence type
1 records
OVE5585
Key finding

Phylogenetic evidence supports multiple human-to-deer spillback events of SARS-CoV-2 in Iowa.

Virus
Host
Location
Supporting text

White-tailed deer, the predominant cervid in North America, are susceptible to SARS-CoV-2 infection. To test the hypothesis that SARS-CoV-2 is circulating in deer, 283 retropharyngeal lymph node (RPLN) samples collected from 151 free-living and 132 captive deer in Iowa from April 2020 through January of 2021 were assayed for the presence of SARS-CoV-2 RNA. The geographic distribution and nesting of clusters of deer and human lineages strongly suggest multiple human-to-deer transmission events followed by subsequent deer-to-deer spread.

Method
whole genome sequencing | phylogenetic clustering
Study design
phylogenetic surveillance and comparative lineage analysis in wild deer samples
Transmission direction
human-to-animal
Geographic raw
Iowa
Genomic Evolution
1 records · 1 evidence types
Evidence type
1 records
OVE5584
Key finding

Whole genome phylogenetic analysis of SARS-CoV-2 from white-tailed deer in Iowa revealed 12 viral lineages, predominantly B.1.2 and B.1.311.

Virus
Host
Location
Not specified
Supporting text

Whole genome sequencing of all 94 positive RPLN samples identified 12 SARS-CoV-2 lineages, with B.1.2 (n = 51; 54.5%) and B.1.311 (n = 19; 20%) accounting for ∼75% of all samples. The geographic distribution and nesting of clusters of deer and human lineages strongly suggest multiple human-to-deer transmission events followed by subsequent deer-to-deer spread.

Genes or proteins
whole genome
Analysis methods
whole genome sequencing | phylogenetic lineage identification