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.