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. 2024 Aug;30(8):1609-1620.
doi: 10.3201/eid3008.231056.

SARS-CoV-2 Seropositivity in Urban Population of Wild Fallow Deer, Dublin, Ireland, 2020-2022

Kevin Purves, Hannah Brown, Ruth Haverty, Andrew Ryan, Laura L Griffin, Janet McCormack, Sophie O'Reilly, Patrick W Mallon, Virginie Gautier, Joseph P Cassidy, Aurelie Fabre, Michael J Carr, Gabriel Gonzalez, Simone Ciuti, Nicola F Fletcher

SARS-CoV-2 Seropositivity in Urban Population of Wild Fallow Deer, Dublin, Ireland, 2020-2022

Kevin Purves et al. Emerg Infect Dis. 2024 Aug.

Abstract

SARS-CoV-2 can infect wildlife, and SARS-CoV-2 variants of concern might expand into novel animal reservoirs, potentially by reverse zoonosis. White-tailed deer and mule deer of North America are the only deer species in which SARS-CoV-2 has been documented, raising the question of whether other reservoir species exist. We report cases of SARS-CoV-2 seropositivity in a fallow deer population located in Dublin, Ireland. Sampled deer were seronegative in 2020 when the Alpha variant was circulating in humans, 1 deer was seropositive for the Delta variant in 2021, and 12/21 (57%) sampled deer were seropositive for the Omicron variant in 2022, suggesting host tropism expansion as new variants emerged in humans. Omicron BA.1 was capable of infecting fallow deer lung type-2 pneumocytes and type-1-like pneumocytes or endothelial cells ex vivo. Ongoing surveillance to identify novel SARS-CoV-2 reservoirs is needed to prevent public health risks during human-animal interactions in periurban settings.

Keywords: COVID-19; Dublin; Ireland; SARS; SARS-CoV-2; cervid; coronavirus; coronavirus disease; deer; respiratory infections; severe acute respiratory syndrome coronavirus 2; viruses; wildlife reservoir; zoonoses.

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Figures

Figure 1
Figure 1
SARS-CoV-2 neutralizing antibodies found in serum samples from fallow deer in an urban deer population located in Dublin, Ireland, 2020–2022. A) Serum samples collected in November 2020 (n = 28); B) samples from November 2021 (n = 25); C) samples from February 2022 (n = 21). Serum samples were collected from wild fallow deer and screened in duplicate for SARS-CoV-2 neutralizing antibodies by using the Genscript cPass SARS-CoV-2 surrogate virus neutralization test (Genescript, https://www.genscript.com). Deer identification numbers are shown on the x axes for each year. Dotted lines indicate a cutoff of 30% neutralization. Red dots indicate serum samples that had >30% neutralization and were considered seropositive for SARS-CoV-2. Data are presented as mean percent neutralization calculated from duplicate wells from 2 independent assays.
Figure 2
Figure 2
Infectivity of SARS-CoV-2 pseudoviruses after incubation with SARS-CoV-2–positive serum samples from wild fallow deer, Dublin, Ireland, 2020–2022. Spike proteins were from Alpha (A), Delta (B), Omicron BA.1 (C), and Omicron BA.2 (D) variants of concern. SARS-CoV-2 pseudoviruses bearing spike proteins from different variants of concern were incubated with 5 deer serum samples at a 1:1 ratio in triplicate and then used to infect Vero E6/TMPRSS2 cells. Identification numbers of deer are indicated. Controls were virus incubated in triplicate at a 1:1 ratio with culture medium. Relative light units from a luciferase reporter were used to calculate percentage infectivity relative to the untreated control virus. Data are from 2 independent experiments with 3 biologic replicates per experiment. Error bars indicate SDs. NE, no envelope naked pseudovirus control; NS, not significant; UF, uninfected cells.
Figure 3
Figure 3
Infectivity of SARS-CoV-2 infectious viruses after incubation with SARS-CoV-2–positive serum samples from wild fallow deer, Dublin, Ireland, 2020–2022. Deer serum samples were incubated with infectious SARS-CoV-2 ancestral strain Italy_INMI1 (A) or Omicron BA.1 (B) and then used to infect Vero E6/TMPRSS2 cells. Identification numbers of deer are indicated. Cytopathic effect was calculated as TCID50, as previously described (19). Data are from 2 independent experiments with 8 biologic replicates per experiment. p values were calculated by using 1-way analysis of variance (Appendix 2 Tables 2, 3). Error bars indicate SDs. NS, not significant; TCID50, 50% tissue culture infectious dose.
Figure 4
Figure 4
Begging behavior of deer sampled to detect SARS-CoV-2 neutralizing antibodies in study of SARS-CoV-2 seropositivity in urban population of wild fallow deer, Dublin, Ireland, 2020–2022. A) November 2020; B) November 2021; C) February 2022. Dotted lines indicate a cutoff of 30% neutralization of SARS-CoV-2 by serum antibodies; >30% neutralization was considered SARS-CoV-2 seropositive. Red dots indicate occasional beggars; most deer were either consistent or occasional beggars.
Figure 5
Figure 5
Example of fallow deer–human interaction in study of SARS-CoV-2 seropositivity in urban population of wild fallow deer, Dublin, Ireland, 2020–2022. Photograph by Bawan Amin, University College Dublin, July 2018.
Figure 6
Figure 6
Deer begging rank distributions in study of SARS-CoV-2 seropositivity in urban population of wild fallow deer, Dublin, Ireland, 2020–2022. Mirror density plot was generated to compare begging rank distributions (Appendix 1) for the whole deer population (black shading) and sampled deer (gray shading).
Figure 7
Figure 7
Begging category proportions in study of SARS-CoV-2 seropositivity in urban population of wild fallow deer, Dublin, Ireland, 2020–2022. A) Total fallow deer population; B) fallow deer sampled for SARS-CoV-2 serum antibodies.
Figure 8
Figure 8
Deer age and sex structure in study of SARS-CoV-2 seropositivity in urban population of wild fallow deer, Dublin, Ireland, 2020–2022. A) Female deer; B) male deer.
Figure 9
Figure 9
Phylogenetic analysis of SARS-CoV-2 superlineages circulating in humans during deer sampling months in study of SARS-CoV-2 seropositivity in wild fallow deer, Dublin, Ireland, 2020–2022. We analyzed SARS-CoV-2 whole-genome sequences from human clinical samples collected in Ireland covering months corresponding to the deer culling dates (November 2020, November 2021, and February 2022). Branch lengths in the phylogenetic tree (left panel) show the number of base substitutions per site. Colors indicate different SARS-CoV-2 variants. Pangolin lineages are shown with corresponding major circulating variants for each cull month. Location of dots shown for each cull month (right 3 panels) corresponds to the sampling date in each month (horizontal axis) and the phylogenetic position within the tree panel (vertical axis).
Figure 10
Figure 10
SARS-CoV-2 infection of tracheal explant in study of SARS-CoV-2 seropositivity in urban population of wild fallow deer, Dublin, Ireland, 2020–2022. Tracheal explants from 2 SARS-CoV-2–seronegative deer were inoculated with SARS-CoV-2 Italy-INMI1 and stained by using immunohistochemistry. Control sections were stained with IgG only or mock infected. A) Arrows indicate SARS-CoV-2 Italy-INMI1 antigen immunoreactivity in tracheal epithelium; B) no immunoreactivity was observed after staining with the IgG control. Scale bars indicate 60 μm.
Figure 11
Figure 11
SARS-CoV-2 Omicron BA.1 infection of ex vivo lung tissue in study of SARS-CoV-2 seropositivity in urban population of wild fallow deer, Dublin, Ireland, 2020–2022. Precision cut lung slices were collected from 2 SARS-CoV-2–seronegative deer and inoculated with SARS-CoV-2 Omicron BA.1; sections were stained by using immunohistochemistry. Control sections were stained with IgG only or mock infected. A) Deer 1; B) deer 2. Arrows in first and middle panels indicate Omicron BA.1 immunoreactivity in cells morphologically consistent with type 2 pneumocytes. Third panel indicates no immunoreactivity after staining with the IgG control. No immunoreactivity was observed in the mock-infected tissues for either animal. Scale bars indicate 60 μm.
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