Severe Acute Respiratory Syndrome Coronavirus 2-Specific Antibodies in Pets in Wuhan, China
Authors: Jianjun Chen, Chaolin Huang, Yanan Zhang, Sai Zhang, Meilin Jin
Journal: Journal of Infection (2020)

In this Journal, Hogan et al. have reported the household pet dogs and cats play important role in colonization of methicillin-resistant Staphylococcus aureus (MRSA).1Hogan P.G. Mork R.L. Boyle M.G. Muenks C.E. Morelli J.J. Thompson R.M. et al.Interplay of personal, pet, and environmental colonization in households affected by community-associated methicillin-resistant Staphylococcus aureus.J Infect. Mar 2019; 78: 200-207Abstract Full Text Full Text PDF PubMed Scopus (27) Google Scholar We would like to share our findings for infection of SARS-CoV-2 in household pet cats and dogs. In December 2019, cases of coronavirus disease 2019 (COVID-19), caused by the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), were first reported in Wuhan, China.2Zhou P. Yang X.L. Wang X.G. Hu B. Zhang L. Zhang W. et al.A pneumonia outbreak associated with a new coronavirus of probable bat origin.Nature. Mar 2020; 579: 270-273Crossref PubMed Scopus (14258) Google Scholar, 3Huang C. Wang Y. Li X. Ren L. Zhao J. Hu Y. et al.Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China.Lancet. 2020 Feb 15; 395: 497-506Abstract Full Text Full Text PDF PubMed Scopus (32448) Google Scholar, 4Lu R. Zhao X. Li J. Niu P. Yang B. Wu H. et al.Genomic characterisation and epidemiology of 2019 novel coronavirus: implications for virus origins and receptor binding.Lancet. 2020 Feb 22; 395: 565-574Abstract Full Text Full Text PDF PubMed Scopus (8116) Google Scholar Since then, a large number of human COVID-19 cases have been reported around the world, becoming a global pandemic as declared by the World Health Organization (WHO). Experimental data has confirmed that the SARS-CoV-2 virus can use angiotensin-converting enzyme II (ACE2) as a receptor.2Zhou P. Yang X.L. Wang X.G. Hu B. Zhang L. Zhang W. et al.A pneumonia outbreak associated with a new coronavirus of probable bat origin.Nature. Mar 2020; 579: 270-273Crossref PubMed Scopus (14258) Google Scholar Furthermore, animal models of SARS-CoV-2 infection have shown that ferrets and cats are susceptible to infection,5Shi J. Wen Z. Zhong G. Yang H. Wang C. Huang B. et al.Susceptibility of ferrets, cats, dogs, and other domesticated animals to SARS-coronavirus 2.Science. 2020 Apr 8; 368: 1016-1020Crossref PubMed Scopus (1250) Google Scholar implying that companion animals might be infected after contact with individuals carrying COVID-19. In this study, we collected swab and blood samples from pet cats and dogs in Wuhan whose owners were confirmed to have COVID-19. Our results provide serological evidence for SARS-CoV-2 infection in pets. Pet cats and dogs were recruited from COVID-19 patients admitted to Wuhan Jinyintan Hospital, one of the designated hospitals for COVID-19. Participation of each pet was granted by the verbal informed consent of the respective owner. Sampling was conducted on 30 and 31 March 2020. Whole blood, oral, and rectal swabs were collected, and the sex and age of the pets were recorded. Swab samples were collected using sterile swabs and placed in a vial containing 2 ml of viral transport medium, stored at 2–8 °C, and shipped to the laboratory within 12 h for further analysis. Whole blood samples (0.5–1 ml) were drawn into evacuated tubes containing EDTA. Plasma was separated, aliquoted, and stored at −40 °C prior to processing. Swab and whole blood samples were collected from 10 cats (four female, six male) and 9 dogs (four female, five male) (Supplementary Table 1) from 15 owners infected with COVID-19, from 15 communities located in six districts in Wuhan (Supplementary Figure 1). The mean ages of enroled cats and dogs were 1.83 years (range: 0.4 to 4.6 years, median 1.7 years) and 3.07 years (range: 0.9 to 7.4 years, median 2.3 years), respectively. All cats and dogs were physically normal when sampled. Swab samples were tested for SARS-CoV-2 RNA using real-time reverse transcription polymerase chain reaction (rRT-PCR), with primers and probes targeting the nucleocapsid protein (N) and RNA-dependant RNA polymerase (RdRp) genes of SARS-CoV-2. All pet samples were negative for SARS-CoV-2 RNA for both N and RdRp genes. The internal reference gene GADPH was amplified in all samples (data not shown). Titres of SARS-CoV-2 S1-specific IgG in plasma were determined with double antigen sandwich enzyme-linked immunosorbent assay (ELISA), as described previously.6Deng J. Jin Y. Liu Y. Sun J. Hao L. Bai J. et al.Serological survey of SARS-CoV-2 for experimental, domestic, companion and wild animals excludes intermediate hosts of 35 different species of animals.Transbound Emerg Dis. 2020 Apr 17; Crossref Scopus (93) Google Scholar Two cats (cat 8 and 18) and one dog (dog 4) were strongly positive and showed high ELISA optical density (OD) ratios for IgG (Fig. 1A). Positive plasma samples were further analysed with neutralising titres using the plaque reduction neutralisation test (PRNT) for SARS-CoV-2. Consistent with IgG titres, cat 8, cat 18, and dog 4 showed neutralising titres of 1:240, 1:240 and 1:120, respectively (Fig. 1B). Several other pet plasma samples were tested in parallel and showed titres of less than 1:20 (data not shown). The serological data indicates that some of the pets had been infected with SARS-CoV-2. We then conducted telephone questionnaires with the owners of the three pets. All owners and their spouses were diagnosed with COVID-19. All three pets were in close contact with the owners and their spouses when they developed COVID-19 symptoms. During the period when the owners were admitted to hospital, cat 8 left the house and wandered outside for more than 1 month; dog 4 was fostered by a pet hospital for more than 1 month until the owner was discharged and back home; and cat 18 was quarantined at home with cat 17 and dog 16, and cared for by other family members once every 3 days; cat 17 and dog 16 tested negative for SARS-CoV-2 antibodies. Questionnaire data suggests that pets acquired SARS-CoV-2 virus from their owners, while other source of infection could not be excluded. In this study, we conducted a survey for SARS-CoV-2 in pets whose owners were diagnosed with COVID-19, in 15 communities in Wuhan. Serological data suggests that three pets (two cats, one dog) had been exposed to the virus, although viral RNA detection was negative. Prior to our study, a preprint of a research article posted online at bioRxiv indicated that SARS-CoV-2-specific antibodies were detected in cats in Wuhan at the time of the COVID-19 epidemic.7Zhang Q. Zhang H. Huang K. Yang Y. Hui X. Gao J. et al.SARS-CoV-2 neutralizing serum antibodies in cats: a serological investigation.bioRxiv. 2020; 2020 (04.01.021196)Google Scholar In addition, pet dogs and cats in Hong Kong,8Sit T.H.C. Brackman C.J. Ip S.M. Tam K.W.S. Law P.Y.T. To E.M.W. et al.Infection of dogs with SARS-CoV-2.Nature. 2020 May 14; Crossref PubMed Scopus (481) Google Scholar whose owners had been diagnosed with COVID-19, tested positive for SARS-CoV-2 RNA. Collectively, these results indicate the SARS-CoV-2 can be transmitted to companion animals, possible through contact with owners carrying COVID-19. However, we were not able to determine whether, under natural conditions, pet cats and dogs can be readily infected with or transmit SARS-CoV-2. Further studies will be needed to establish the role of pets in the current COVID-19 epidemic. None This study was supported by the Emergency Scientific Research Project for COVID-19 from Hubei Province (2020FCA004). The funder had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. The authors of this study would like to acknowledge Professor Yaping Zhang, Bo Zhang, Fei Deng and Yi Shen for enlightening discussions; Changmin Hu, Jindong Gao, Juefu Hu, Xinglin He, Decheng Wang, Bei Li, Qiaoli Wu for excellent technical assistance; Lei Zhang at The Core Facility and Technical Support, Wuhan Institute of Virology, CAS for NGS sequencing. Download .docx (2.07 MB) Help with docx files