Susceptibility of ferrets, cats, dogs, and other domesticated animals to SARS-coronavirus 2

Jianzhong Shi, Zhiyuan Wen, Gongxun Zhong, Huanliang Yang, Chong Wang, Baoying Huang, Renqiang Liu, Xijun He, Lei Shuai, Ziruo Sun, Yubo Zhao, Peipei Liu, Libin Liang, Pengfei Cui, Jinliang Wang, Xianfeng Zhang, Yuntao Guan, Wenjie Tan, Guizhen Wu, Hualan Chen, Zhigao Bu, Jianzhong Shi, Zhiyuan Wen, Gongxun Zhong, Huanliang Yang, Chong Wang, Baoying Huang, Renqiang Liu, Xijun He, Lei Shuai, Ziruo Sun, Yubo Zhao, Peipei Liu, Libin Liang, Pengfei Cui, Jinliang Wang, Xianfeng Zhang, Yuntao Guan, Wenjie Tan, Guizhen Wu, Hualan Chen, Zhigao Bu

Abstract

Severe acute respiratory syndrome-coronavirus 2 (SARS-CoV-2) causes the infectious disease COVID-19 (coronavirus disease 2019), which was first reported in Wuhan, China, in December 2019. Despite extensive efforts to control the disease, COVID-19 has now spread to more than 100 countries and caused a global pandemic. SARS-CoV-2 is thought to have originated in bats; however, the intermediate animal sources of the virus are unknown. In this study, we investigated the susceptibility of ferrets and animals in close contact with humans to SARS-CoV-2. We found that SARS-CoV-2 replicates poorly in dogs, pigs, chickens, and ducks, but ferrets and cats are permissive to infection. Additionally, cats are susceptible to airborne transmission. Our study provides insights into the animal models for SARS-CoV-2 and animal management for COVID-19 control.

Copyright © 2020 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.

Figures

Fig. 1. Replication of SARS-CoV-2 in ferrets.
Fig. 1. Replication of SARS-CoV-2 in ferrets.
Viral RNA in organs or tissues of ferrets inoculated with (A) F13-E virus strain or (B) CTan-H strain. Viral titers in organs or tissues of ferrets inoculated with F13-E (C) and CTan-H (D). The viral RNA–negative organs indicted in (A) and (B) were also negative for virus titration [indicated as “Others” in (C) and (D)]. Viral RNA (E and F) and viral titer (G and H) in nasal washes of ferrets inoculated with F13-E [(E) and (G)] and CTan-H [(F) and (H)]. Antibodies against SARS-CoV-2 tested by ELISA (I and J) and neutralization assay (K and L) with sera derived from ferrets inoculated with F13-E [(I) and (K)] and CTan-H [(J) and (L)]. Each color bar represents the value from an individual animal. The gray bars in (I) to (L) indicate the antibody values of sera collected from each animal before inoculation. Asterisks denote animals that were euthanized on day 13 p.i.; the other four animals were euthanized on day 20 p.i. The dashed lines in (I) and (L) show the cutoff value for seroconversion, and the dashed lines in the other panels indicate the lower limit of detection. OD450, optical density measured at 450 nm; NT antibody, neutralizing antibody.
Fig. 2. Replication of SARS-CoV-2 in cats.
Fig. 2. Replication of SARS-CoV-2 in cats.
Subadult cats and juvenile cats inoculated with CTan-H virus were euthanized on days 3 and 6 p.i., and their organs were collected for viral RNA detection and virus titration. (A) Viral RNA and (B) viral titers of subadult cats on day 3 p.i. (C) Viral RNA and (D) viral titers of subadult cats on day 6 p.i. (E) Viral RNA and (F) viral titers of juvenile cats on day 3 p.i. The values of red bars in (E) and (F) are from the cat that died on this day. (G) Viral RNA and (H) viral titers of juvenile cats on day 6 p.i. “Others” represents viral-negative organs, including the brain, heart, submaxillary lymph nodes, kidneys, spleen, liver, and pancreas. Each color bar represents the value from an individual animal. The dashed lines indicate the lower limit of detection.
Fig. 3. Transmission of SARS-CoV-2 in cats.
Fig. 3. Transmission of SARS-CoV-2 in cats.
Transmission of the CTan-H virus strain was evaluated in subadult cats (A to D) and juvenile cats (E to G). (A) Viral RNA in the feces of virus-inoculated or virus-exposed subadult cats. (B) Viral RNA in tissues or organs of inoculated or exposed subadult cats euthanized on day 11 p.i. (pair 1, red bars) or day 12 p.i. (pairs 2 and 3). Antibodies against SARS-CoV-2 in these euthanized subadult cats were detected by ELISA (C) and neutralization assay (D). (E) Viral RNA in nasal washes of juvenile cats. Sera from juvenile cats were collected on day 20 p.i., except for sera from one virus-inoculated animal that died on day 13 p.i. Antibody values for this cat (indicated by asterisks) were detected from sera collected on day 10 p.i.; antibodies against SARS-CoV-2 were detected by ELISA (F) and neutralization assay (G). Each color bar represents the value from an individual animal. The horizontal dashed lines in (C) and (F) show the cutoff value for seroconversion, and the horizontal dashed lines in the other panels indicate the lower limit of detection.

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