Discussion

While the initial SARS-CoV-2 spill-over event is believed to have been a zoonotic transfer from bats to humans, possibly by way of an unidentified intermediate animal host, the driving force behind the pandemic has undeniably been human-to-human transmission (WHO, 2020). The vast number of human COVID-19 patients worldwide and the incalculable numbers of human-animal interactions occurring each day make ongoing, unreported zoonotic and anthroponotic transmission of SARS-CoV-2 likely. The sheer number of human cases and the global shortages of adequately equipped and resourced diagnostic laboratories in recent months have prevented many countries from reaching testing targets in people; unsurprisingly, widespread testing or structured surveillance in animals has not been prioritised.
Nevertheless, there have been several cases of natural SARS-CoV-2 infections in animals confirmed globally. Cats are the most commonly reported domesticated animal to be infected, including both pet cats, and captive lions and tigers in a New York zoo. Pet dogs appear to be less susceptible to infection than cats, based on evidence from both the smaller number of reported cases and the results of experimental data. Most animal cases have had known or suspected exposure to human COVID-19 patients, indicating that human-to-animal infection is the primary cause of spread in domestic settings. Nearly all infected animals have recovered naturally or following supportive treatments, except for those cases that died or were euthanised due to other underlying conditions. To prevent further anthroponotic transmission, animal owners have been advised to implement basic hygiene measures such as washing hands before and after contact with animals, their food or bedding, and to avoid cuddling, kissing or being licked by animals or sharing food with them. People who are suspected or confirmed to be infected with SARS-CoV-2 have been advised to limit contact with animals altogether (OIE, 2020f).
There is no evidence that people are at risk of contracting infection from their pets, and the OIE has advised that there is no justification in taking measures directed at companion animals that may compromise their welfare (OIE, 2020f). During the early stages of the pandemic there were reports of stray dogs and cats rounded up in Russia (Balmforth, 2020), companion animals owned by confirmed COVID-19 patients routinely euthanised by authorities in China, of large-scale abandonment of pet dogs and cats and even of pets being thrown to their deaths from high-rise buildings by fearful owners following early reports of pets testing positive for SARS-CoV-2 (Campbell, 2020). This occurred despite no evidence of animal-to-human transmission of the virus in domestic settings. In fact, the results of one modelling study predicted that abandoning cats could actually increase incidence of COVID-19 in urban settings (Gao, Pan, & Pan, 2020).
While SARS-CoV-2 infections in humans and animals within domestic settings are unlikely to contribute to community transmission, in high-density animal environments, such as on farms with susceptible species, the risk of anthroponotic and zoonotic transmission must increase substantially. The lack of susceptibility of poultry and pigs to SARS-CoV-2 infection is reassuring, particularly given the heavy losses to these highly intensive commercial industries following recent and ongoing outbreaks of avian influenza and African swine fever, respectively (FAO, 2020; Tian & von Cramon-Taubadel, 2020). Commercial farming of mink, ferrets and other small mammals including rabbits that are known or presumed to be susceptible to SARS-CoV-2 infection and replication (Kim et al., 2020; Richard et al., 2020; Schlottau et al., 2020; Shi et al., 2020), however, provides ideal conditions for viral transmission and spill-over. The outbreaks of SARS-CoV-2 in Dutch and Danish mink farms are presumed to have been introduced by infected employees, followed by extensive mink-to-mink spread and ultimately, mink-to-human transmission in at least two instances (de Jonge & Schouten, 2020e; Larsen & Zuferov, 2020). Implementation of precautionary measures for all mink farms in these countries, including visitor bans and PPE for farm employees (MoF, 2020a; Schouten, 2020d), and the subsequent depopulation of all infected premises and the proper disposal of mink carcasses (de Jonge & Schouten, 2020a; Larsen & Zuferov, 2020), will go some way to alleviating the occupational and public health risk posed by these farms.
However, despite the brief statement regarding negative testing results from Chinese fur farms (OIE, 2020b), there have been no reports of similar initiatives or surveillance activities being proactively implemented in other fur-farming nations. The global fur trade was reported to be worth $40 billion in 2014, and while many countries have banned fur farming in recent years, the major producers in China, parts of Europe and North America reportedly continue to produce over 101 million animal pelts every year (Lung & Lin, 2019). China produced 26.2 million mink pelts or nearly 40% of the global mink pelt harvest in 2016 (Lung & Lin, 2019), while other major mink producers include Denmark (17.8 million), Poland (8.5 million), the Netherlands (5.5 million), the USA (3.5 million) and Canada (2.1 million) (Bale, 2016; Ingman, 2015; Lung & Lin, 2019). The high numbers of confirmed human COVID-19 cases in these countries (Dong et al., 2020), coupled with particularly high densities of mink and other small mammals at this time of year due to seasonal breeding patterns (Amstislavsky, Lindeberg, Aalto, & Kennedy, 2008), means that the likelihood of unreported SARS-CoV-2 infections in commercial fur farms, and the potential for extensive virus transmission in these environments, must be considered high. PPE use by farm workers can mitigate viral transmission, but only if it is consistently implemented. While the direct risk to the general public from these entities is low, increased community transmission can arise if on-farm reservoirs of SARS-CoV-2 infections provide repeated spill-over opportunities to naïve employees and their direct contacts.
Colonies of ferrets, rabbits, non-human primates and other potentially susceptible animals kept for research purposes must similarly be at increased risk of introduction from infected humans, and could also provide reservoirs for ongoing viral replication, transmission and reverse spill-over. Introduction of PPE and strict hygiene protocols for in-contact researchers and animal support staff would be recommended to prevent occupational exposure to and transmission of the virus, and ongoing serological screening of both humans and animals could provide early warning of SARS-CoV-2 transmission within and between populations. Surveillance of commercial fur farms, colonies of research animals and other high-intensity animal enterprises should be encouraged to further investigate their role in community transmission of SARS-CoV-2.
Of additional concern is the potential for anthroponotic transmission of SARS-CoV-2 to vulnerable wild animal populations. While no natural or experimental cases of SARS-CoV-2 in great ape species have been reported to date, their known susceptiblity to common human respiratory viruses including rhinovirus C (the common cold) (Negrey et al., 2019), the similarity of their ACE2 receptors to the human form that SARS-CoV-2 uses to infect human cells (Melin et al., 2020), and the experimental studies that have demonstrated SARS-CoV-2 infections in other primate species (Lu et al., 2020; Rockx et al., 2020; Woolsey et al., 2020), suggest that SARS-CoV-2 is a tangible threat to great ape populations. Concern for highly vulnerable wild populations of great apes including chimpanzees and gorillas has already seen implementation of protective measures in wildlife preserves across Africa and Asia. Visitors have been banned from many such parks since early March 2020 to limit human contact with wild apes, and PPE, quarantine and social distancing measures for in-contact researchers have also been implemented (Gibbons, 2020). Research teams in Tanzania, Cote d’Ivoire and Uganda, among others, are reportedly conducting observational and faecal surveillance of wild apes, and working with local communities to develop strategies for the further protection of great apes and wildlife, including the provision of goats, cash crops or other incentives to prevent villagers from hunting wild meat (Gibbons, 2020).
Other wild animal populations may also be at similar risk from SARS-CoV-2, however it is too soon to know which populations are the most vulnerable. The virus has emerged so recently that few rigorous experimental studies about its infective potential in various animal species exist in the literature to date, and while numerous models have been developed to predict the susceptibility of animal species, large-scale testing of these predictions would not be feasible for numerous reasons. Gryseels et al. (2020) argue that unless or until such evidence is obtained, sanitary precautions such as physical distancing and the wearing of PPE should be implemented during all human interactions with wild mammal species. This would serve to both protect individual animals from disease, and to prevent the establishment of SARS-CoV-2 reservoirs in wild animal populations, among which viral transmission could occur unchecked and potentially seed repeated spillover events into humans. This proposal is further strengthened by the US Geological Survey’s risk assessment regarding north American bats, which indicated that implementation of PPE for researchers could reduce the risk of human-to-bat transmission of SARS-CoV-2 by approximately 95% (Runge et al., 2020). The authors of this risk assessment identified several critical uncertainties that could affect their estimates of SARS-CoV-2 entering bat populations and associated sequelae, including likelihoods of human-to-bat, bat-to-bat, bat-to-animal and bat-to-human viral transmission dynamics; pathogenesis and replication of the virus in bat tissues; and seasonal impacts including bat breeding and hibernation patterns on virus replication and transmission (Runge et al., 2020). Until further research results are available to fill these knowledge gaps, a precautionary use of PPE and a conservative approach to wildlife handling and interaction would be encouraged.
Other adverse effects of SARS-CoV-2 on animals may include the ‘panic slaughter’ of species that are mistakenly blamed for transmitting disease. The reputation of bats as the probable source of COVID-19 has reportedly led to instances of fearful citizens setting fire to roosting bats (Fenton, Mubareka, Tsang, Simmons, & Becker, 2020), and prompted calls for their mass slaughter to protect public health (H. Zhao, 2020). Even less extreme requests for the removal of hibernating bats from human residential areas could disturb their delicate physiological balances, lead to high bat mortality and potentially increase the spread of other viruses (H. Zhao, 2020). In addition, many bat species are endangered, and those that have become habituated to urban life may not survive in the wild, placing already fragile populations at further risk (H. Zhao, 2020). Masked palm civets (Paguma larvata ) are widely accepted to have been the intermediate host species for SARS-CoV-1 (Gong & Bao, 2018), which led to the slaughter of thousands of wild civets in southern China using a variety of inhumane methods, including clubbing and drowning in disinfectant, following outbreaks in the region (Parry, 2004). Pangolins have been put forward as potential intermediate hosts for the current COVID-19 pandemic (Andersen et al., 2020; Liu et al., 2020; T. Zhang et al., 2020), leading to concern from conservationists that pangolins, already endangered and reportedly the world’s most trafficked mammal, may be placed at further risk by ‘ecological killing’ as part of disease control efforts (Standaert, 2020). On the other hand, the zoonotic origins of the COVID-19 pandemic has increased global calls to end the trading of wildlife for all purposes, including ‘wet’ animal markets and wild game hunting for human consumption, and the traditional medicine, tourism, wild pet and fur farming sectors still existing across the globe. In March 2020, China introduced a ban on hunting, trading, transporting and eating the meat of wild animals (NPC, 2020) and in early June upgraded the protection of all pangolin species to the highest level, banning all trade in pangolins and their products and removing pangolin scales from their approved list of traditional medicines (Yueming, 2020). While this is to be applauded, China’s reported proposal to reclassify mink, raccoon dogs, and silver and blue foxes from wild animals to domestic livestock (Dalton, 2020) may cause additional concerns, both for animal activists, and public health advisors concerned about extended SARS-CoV-2 transmission and the potential for future zoonotic pandemics.
Direct impacts of the COVID-19 pandemic on animals have been mostly limited to date, with mild to moderate transient clinical disease reported in less than half of the 14 pets and 8 zoo animals confirmed to be infected. Nevertheless, the pandemic has negatively impacted animal welfare directly in several reported instances – including the fatalities and depopulation of tens of thousands of farmed European mink, and the dogs and cats that have been abandoned and thrown out of high-rise buildings – and most likely indirectly, in many more unreported instances, such as via decreased activities of veterinary services during global lockdown (Gortázar & de la Fuente, 2020). While animals are not implicated in community transmission of SARS-CoV-2 at present, until more data from natural cases, surveillance and experimental infection studies become available, the level of uncertainty surrounding the role of animals in SARS-CoV-2 transmission remains high. Should SARS-CoV-2 become established in domestic or wild animal populations, the potential impacts of the resulting panzootic could be severe: morbidity and mortality in susceptible animals of high emotional, economic and/or agricultural value; threats to the health and survival of vulnerable wildlife species; and establishment of viral reservoirs that could seed repeated spill-over events into humans and thwart global disease control or eradication efforts. Continuing research and surveillance activities are needed, to further determine the role of animals in community transmission of SARS-CoV-2; to advise the public to prevent fear, ignorance and misinformation that may cause adverse animal welfare events; and to identify the reservoir and intermediate (if applicable) hosts of SARS-CoV-2 so that future spill-over events can be prevented.