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. 2022 Sep;69(5):e3060-e3075.
doi: 10.1111/tbed.14662. Epub 2022 Jul 26.

Multi-species outbreak of SARS-CoV-2 Delta variant in a zoological institution, with the detection in two new families of carnivores

Matthew C Allender  1   2 , Michael J Adkesson  1 , Jennifer N Langan  1   3 , Katie W Delk  1 , Thomas Meehan  1 , Copper Aitken-Palmer  1 , Michael M McEntire  4 , Mary L Killian  5 , Mia Torchetti  5 , Shirley A Morales  6 , Connie Austin  7 , Richard Fredrickson  8 , Colleen Olmstead  8 , Ruian Ke  9 , Rebecca Smith  10 , Eric T Hostnik  1   11 , Karen Terio  12 , Leyi Wang  8
Affiliations

Multi-species outbreak of SARS-CoV-2 Delta variant in a zoological institution, with the detection in two new families of carnivores

Matthew C Allender et al. Transbound Emerg Dis. 2022 Sep.

Abstract

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has a worldwide distribution in humans and many other mammalian species. In late September 2021, 12 animals maintained by the Chicago Zoological Society's Brookfield Zoo were observed with variable clinical signs. The Delta variant of SARS-CoV-2 was detected in faeces and nasal swabs by qRT-PCR, including the first detection in animals from the families Procyonidae and Viverridae. Test positivity rate was 12.5% for 35 animals tested. All animals had been vaccinated with at least one dose of a recombinant vaccine designed for animals and all recovered with variable supportive treatment. Sequence analysis showed that six zoo animal strains were closely correlated with 18 human SARS-CoV-2 strains, suggestive of potential human-to-animal transmission events. This report documents the expanding host range of COVID-19 during the ongoing pandemic.

Keywords: Procyonidae; SARS-CoV-2; Viverridae; carnivore; severe acute respiratory syndrome coronavirus; zoo.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

FIGURE 1
FIGURE 1
SARS‐CoV‐2 case positivity rate zoological animals. Daily (vertical bars; left axis) and 7‐day test positivity rate (line, right axis) in 12 carnivores with SARS‐CoV‐2 detected at the Chicago Zoological Society's Brookfield Zoo in 2021
FIGURE 2
FIGURE 2
SARS‐CoV‐2 viral copies between species at a zoological institution. Viral copy number in 12 carnivores detected with SARS‐CoV‐2 with and without clinical signs at Chicago Zoological Society's Brookfield Zoo in 2021
FIGURE 3
FIGURE 3
Clinical signs in SARS‐CoV‐2 positive and negative zoological animals. Number of days positive in 12 carnivores detected with SARS‐CoV‐2 at the Chicago Zoological Society's Brookfield Zoo in 2021
FIGURE 4
FIGURE 4
Imaging of a binturong prior to and after SARS‐CoV‐2 infection. Computed tomography of a female binturong (Arctictis binturong) 1 year before (a, b) and 2 months post (c, d) SARS‐CoV‐2 infection at the Chicago Zoological Society's Brookfield Zoo in 2021. Comparison images at similar locations at two time points; the white chevrons highlight areas of peripheral linear unstructured interstitial pattern.
FIGURE 5
FIGURE 5
Complete genome comparison of six zoo SARS‐CoV‐2 strains from this study using the closest human strain (hCoV/human/USA/IN‐CDC‐STM‐000721646/2021, GenBank accession number: OL526659) as a reference. Two to four nucleotide differences observed in them.
FIGURE 6
FIGURE 6
Phylogenetic tree analysis of complete genome of SARS‐CoV‐2 Delta variants including six zoo animal strains, 18 human strains from the United States, and the original Wuhan human strain (Wuhan‐Hu‐1)
FIGURE 7
FIGURE 7
Phylogenetic tree analysis of spike gene of SARS‐CoV‐2 Delta variants including six zoo animal strains, 18 human strains from the United States, and the original Wuhan human strain (Wuhan‐Hu‐1)
FIGURE 8
FIGURE 8
Individual host response in zoological animals with SARS‐CoV‐2. Fitting results of the viral dynamic model (lines) to data (dots) in 12 carnivores detected with SARS‐CoV‐2 at the Chicago Zoological Society's Brookfield Zoo in 2021. Open circles denote censored data (i.e. viral load below the limit of detection, black dashed lines)
FIGURE 9
FIGURE 9
Current taxonomic diversity of wildlife detected with SARS‐CoV‐2. The diagram shows 17 animal species tested positive for SARS‐CoV‐2 within three animal orders Carnivora, Artiodactyla, and Primates. Information on order, suborder, and family of these animal species is listed. In the present study, three new animal species tested positive for SARS‐CoV‐2 and they are highlighted with a red colour frame; the other three animal species that tested positive are highlighted with an aqua colour frame.
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