Seroprevalence of anti-SARS-CoV-2 antibodies in household domestic ferrets ( <i>Mustela putorius furo</i>) in Spain, 2019–2023

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Abstract

SARS-CoV-2 is the causal agent of Coronavirus Disease 2019 (COVID-19) in humans that emerged in late 2019. This virus is able to infect humans and different animal species. Among pets, cats and ferrets are more susceptible to be infected by the SARS-CoV-2. Epidemiological studies are an important tool to provide information under natural conditions of exposure to SARS-CoV-2 virus. In comparison to cats, limited epidemiological studies have been performed in domestic ferrets ( Mustela putorius furo) reporting the presence of antibodies in this species. This study analysed the presence of anti-SARS-CoV-2 antibodies in 432 cliend-owned ferrets from different geographical areas of Spain during the different waves of COVID-19 outbreaks from December 2019 to May 2023 (42 months). For this purpose, anti-SARS-CoV-2 antibodies were detected by an enzyme-linked immunosorbent method (ELISA) using the receptor binding domain (RBD) of Spike antigen and confirmed by serum virus neutralization assay. Eighteen of the 432 ferrets included were seroreactive by the in-house ELISA (4.17%, 95% Confidence Interval (CI): 2.65–6.49). In this sense, the wave of COVID-19 with the higher number of seropositive ferrets occurred during the seventh wave when the different Omicron subvariants were the dominant virus variants. Our results suggest that the risk of SARS-CoV-2 transmission in domestic ferrets in natural conditions is low. Further research is need to evaluate the potential risk of transmission of SARS-CoV-2 from human to pets.

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The online version contains supplementary material available at 10.1007/s11259-023-10190-2.

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

Jianzhong Shi, Zhiyuan Wen, Gongxun Zhong … (2020)

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) causes the infectious disease COVID-19, which was first reported in Wuhan, China in December, 2019. Despite the tremendous efforts to control the disease, COVID-19 has now spread to over 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 completely unknown. Here, 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. We found experimentally that cats are susceptible to airborne infection. Our study provides important insights into the animal models for SARS-CoV-2 and animal management for COVID-19 control.

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Transmission of SARS-CoV-2 on mink farms between humans and mink and back to humans

Bas Oude Munnink, Reina S Sikkema, David Nieuwenhuijse … (2020)

Two-way transmission on mink farms Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is a zoonotic virus—one that spilled over from another species to infect and transmit among humans. We know that humans can infect other animals with SARS-CoV-2, such as domestic cats and even tigers in zoos. Oude Munnink et al. used whole-genome sequencing to show that SARS-CoV-2 infections were rife among mink farms in the southeastern Netherlands, all of which are destined to be closed by March 2021 (see the Perspective by Zhou and Shi). Toward the end of June 2020, 68% of mink farm workers tested positive for the virus or had antibodies to SARS-CoV-2. These large clusters of infection were initiated by human COVID-19 cases with viruses that bear the D614G mutation. Sequencing has subsequently shown that mink-to-human transmission also occurred. More work must be done to understand whether there is a risk that mustelids may become a reservoir for SARS-CoV-2. Science, this issue p. 172; see also p. 120

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SARS-CoV-2 in fruit bats, ferrets, pigs, and chickens: an experimental transmission study

Kore Schlottau, Melanie Rissmann, Annika Graaf … (2020)

Summary Background In December, 2019, a novel zoonotic severe acute respiratory syndrome-related coronavirus emerged in China. The novel severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) became pandemic within weeks and the number of human infections and severe cases is increasing. We aimed to investigate the susceptibilty of potential animal hosts and the risk of anthropozoonotic spill-over infections. Methods We intranasally inoculated nine fruit bats (Rousettus aegyptiacus), ferrets (Mustela putorius), pigs (Sus scrofa domesticus), and 17 chickens (Gallus gallus domesticus) with 105 TCID50 of a SARS-CoV-2 isolate per animal. Direct contact animals (n=3) were included 24 h after inoculation to test viral transmission. Animals were monitored for clinical signs and for virus shedding by nucleic acid extraction from nasal washes and rectal swabs (ferrets), oral swabs and pooled faeces samples (fruit bats), nasal and rectal swabs (pigs), or oropharyngeal and cloacal swabs (chickens) on days 2, 4, 8, 12, 16, and 21 after infection by quantitative RT-PCR (RT-qPCR). On days 4, 8, and 12, two inoculated animals (or three in the case of chickens) of each species were euthanised, and all remaining animals, including the contacts, were euthanised at day 21. All animals were subjected to autopsy and various tissues were collected for virus detection by RT-qPCR, histopathology immunohistochemistry, and in situ hybridisation. Presence of SARS-CoV-2 reactive antibodies was tested by indirect immunofluorescence assay and virus neutralisation test in samples collected before inoculation and at autopsy. Findings Pigs and chickens were not susceptible to SARS-CoV-2. All swabs, organ samples, and contact animals were negative for viral RNA, and none of the pigs or chickens seroconverted. Seven (78%) of nine fruit bats had a transient infection, with virus detectable by RT-qPCR, immunohistochemistry, and in situ hybridisation in the nasal cavity, associated with rhinitis. Viral RNA was also identified in the trachea, lung, and lung-associated lymphatic tissue in two animals euthanised at day 4. One of three contact bats became infected. More efficient virus replication but no clinical signs were observed in ferrets, with transmission to all three direct contact animals. Mild rhinitis was associated with viral antigen detection in the respiratory and olfactory epithelium. Prominent viral RNA loads of 0–104 viral genome copies per mL were detected in the upper respiratory tract of fruit bats and ferrets, and both species developed SARS-CoV-2-reactive antibodies reaching neutralising titres of up to 1/1024 after 21 days. Interpretation Pigs and chickens could not be infected intranasally by SARS-CoV-2, whereas fruit bats showed characteristics of a reservoir host. Virus replication in ferrets resembled a subclinical human infection with efficient spread. Ferrets might serve as a useful model for further studies—eg, testing vaccines or antivirals. Funding German Federal Ministry of Food and Agriculture.

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Author and article information

Contributors

Sergio Villanueva-Saz: svs@unizar.es

Journal

Journal ID (nlm-ta): Vet Res Commun

Journal ID (iso-abbrev): Vet Res Commun

Title: Veterinary Research Communications

Publisher: Springer Netherlands (Dordrecht )

ISSN (Print): 0165-7380

ISSN (Electronic): 1573-7446

Publication date (Electronic): 7 August 2023

Publication date PMC-release: 7 August 2023

Publication date (Print): 2024

Volume: 48

Issue: 1

Pages: 533-540

Affiliations

[1 ]Clinical Immunology Laboratory, Veterinary Faculty, University of Zaragoza, ( https://ror.org/012a91z28) 50013 Zaragoza, Spain

[2 ]Department of Animal Pathology, Veterinary Faculty, University of Zaragoza, ( https://ror.org/012a91z28) Zaragoza, Spain

[3 ]GRID grid.11205.37, ISNI 0000 0001 2152 8769, Instituto Agroalimentario de Aragón-IA2 (Universidad de Zaragoza-CITA), ; Zaragoza, Spain

[4 ]Hospital Veterinari Canis, Girona, Spain

[5 ]GRID grid.11205.37, ISNI 0000 0001 2152 8769, Institute for Biocomputation and Physics of Complex Systems (BIFI), , University of Zaragoza, ; Edificio I+D, Campus Rio Ebro, Zaragoza, Spain

[6 ]GRID grid.450869.6, ISNI 0000 0004 1762 9673, Aragon I+D Foundation (ARAID), ; Zaragoza, Spain

[7 ]GRID grid.488737.7, ISNI 0000000463436020, Aragon Health Research Institute (IIS Aragón), ; Zaragoza, Spain

[8 ]Department of Microbiology, Pediatrics, Radiology and Public Health, University of Zaragoza, ( https://ror.org/012a91z28) Zaragoza, Spain

[9 ]CIBER de Enfermedades Infecciosas, Instituto de Salud Carlos III, ( https://ror.org/00ca2c886) Madrid, Spain

[10 ]Department of Animal Medicine and Surgery, Veterinary Faculty, Univerisdad Complutense Madrid, ( https://ror.org/02p0gd045) Madrid, Spain

[11 ]Hospital Veterinario de Animales Exoticos Los Suaces, Madrid, Spain

[12 ]Department of Animal Production and Sciences of the Food, Veterinary Faculty, University of Zaragoza, ( https://ror.org/012a91z28) Zaragoza, Spain

Article

Publisher ID: 10190

DOI: 10.1007/s11259-023-10190-2

PMC ID: 10811151

PubMed ID: 37548874

SO-VID: 31055407-2781-4fe9-81a2-ea4905da499a

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Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 8 June 2023

Date accepted : 26 July 2023

Funding

Funded by: Universidad de Zaragoza

Open Access :

Open Access funding provided thanks to the CRUE-CSIC agreement with Springer Nature.

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ScienceOpen disciplines: Veterinary medicine

Keywords: elisa,ferret,sars-cov-2,serology,spain,vnt

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ScienceOpen disciplines: Veterinary medicine

Keywords: elisa, ferret, sars-cov-2, serology, spain, vnt

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Seroprevalence of anti-SARS-CoV-2 antibodies in household domestic ferrets ( Mustela putorius furo) in Spain, 2019–2023

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Novel Coronavirus Disease COVID-19

Most cited references 21

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

Transmission of SARS-CoV-2 on mink farms between humans and mink and back to humans

SARS-CoV-2 in fruit bats, ferrets, pigs, and chickens: an experimental transmission study

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