Introduction
First detected in late 2019, the COVID-19 pandemic caused by the novel
severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has since
been declared a public health emergency of international concern,
approaching eleven million human infections and causing over half a
million human deaths by early July 2020 (Dong, Du, & Gardner, 2020).
The zoonotic virus was first identified in Wuhan, China and the initial
cluster of cases was initially believed to be linked to a live ‘wet’
seafood and animal market, although results of back tracing activities
have now called this into question (Letzter, 2020; Woodward, 2020).
Phylogenetically related to SARS-CoV-1, which caused the disease SARS
that emerged from China in 2003, SARS-CoV-2 is also believed to have
emerged from a betacoronavirus circulating in rhinolophid (horseshoe)
bats (Lau et al., 2020; Zhou et al., 2020), which then made the species
jump to humans, potentially by way of an intermediate animal host.
Various animal species including snakes, turtles and pangolins have been
proposed as the intermediate host (Andersen, Rambaut, Lipkin, Holmes, &
Garry, 2020; Lam et al., 2020a; Lam et al., 2020b; Liu et al., 2020;
Xiao et al., 2020; S.-L. Zhai et al., 2020; Zhang, Wu, & Zhang, 2020),
with no consensus yet being reached.
From the initial zoonotic spill-over event in China, the virus quickly
demonstrated efficient human-to-human transmission, with virus in
respiratory droplets expelled by COVID-19 patients during coughing,
sneezing and talking reportedly remaining viable for multiple hours in
aerosols and up to days on some surfaces (Meselson, 2020; van Doremalen
et al., 2020). With billions of people around the world harbouring the
virus, and the known animal-origin and high recombination rates of
SARS-coronaviruses (Stavrinides & Guttman, 2004), reverse spill-over of
SARS-CoV-2 from humans to animals (anthroponotic transmission) was
surely inevitable.
Incalculable numbers of human-animal interactions occur each day in
domestic, agricultural, research, recreational, educational,
therapeutic, entertainment and wild settings. Over 470 million dogs and
370 million cats were kept as pets worldwide in 2018 (Bedford, 2020),
with the USA, China and Russia the top three dog and cat owning nations
(Walden, n.d.). Over half of 27,000 surveyed households owned at least
one pet in 2016, and increases in pet ownership are reportedly highest
in China, India and Latin America (GfK, 2016). Worldwide, an estimated
70 billion terrestrial animals were raised and slaughtered for human
consumption in 2018, with farm animal production the fastest growing
agricultural sub-sector and increases particularly expected to occur in
developing countries (Ilea, 2009). Flourishing legal and illegal
wildlife trades exist worldwide, with the global trafficking in illegal
wildlife commodities including pangolin scales, elephant ivory, tiger
bone and bear bile estimated at $7-23 billion USD in 2016 (TRAFFIC,
2020). Encroachment of humans into previously uninhabited areas for
logging, cropping and urbanisation can create diverse
wildlife-livestock-human interfaces that represent critical points for
cross-species transmission and emergence of pathogens (Hassell, Begon,
Ward, & Fèvre, 2017). Over 60% of recently identified emerging disease
events have been zoonotic – the majority of which have had a wildlife
origin – and such events have been increasing significantly in recent
times (Jones et al., 2008; Wang & Crameri, 2014).
As recent outbreaks of zoonotic diseases with pandemic and panzootic
potential – including highly pathogenic avian influenza, SARS and Ebola
virus – have demonstrated, an understanding of the human-animal
interface and its relevance to disease transmission remains a critical
control point. For the current pandemic, determination of the
susceptibility of various animal species to infection with SARS-CoV-2
and the role of animals in the epidemiology of the disease are critical
to informing appropriate human and veterinary public health responses.
Many simulation models have been developed to assess the likelihood of
SARS-CoV-2 susceptibility in animal hosts. These studies aim to classify
animal susceptibility or elucidate possible intermediate or reservoir
host species based on the implied affinity of the species’
angiotensin-converting enzyme 2 (ACE2) receptor binding domain sites for
the SARS-CoV-2 spike protein. Results have indicated that species at
highest risk of infection with SARS-CoV-2 include primates –
particularly of the catarrhine (Old world) order (Damas et al., 2020) –
and most of the carnivores, even- and odd-toed ungulates, pangolins and
scaly anteaters (Praharaj et al., 2020). Medium to high probability was
ascribed to pangolins, rabbits and cats; lower probability to chickens
and turkeys; and rats, mice and ducks were rated as low to very low
(Praharaj et al., 2020; X. Zhao et al., 2020). X. Zhai et al. (2020)
noted that pigs and dogs, and even cattle and sheep appear to have ACE2
proteins capable of acting as a receptor for viral entry, and the
apparent low susceptibility of infection in these species is likely
related to the relatively low levels of ACE2 expressed in the
respiratory tract. Notably, the Damas et al. (2020) model predicted
domestic cats, tigers and golden hamsters to be only medium risk, and
ferrets low risk. Contrary evidence of natural and experimental
infection in these animals (see below) suggests that the utility of
these models as predictive tools may be limited.
Given the conflicting results of predictive modelling studies and the
large numbers of journal articles, pre-prints, press releases and media
reports of varying quality that have flooded the literature in recent
months, definitive answers regarding the infectivity and clinical
picture of SARS-CoV-2 in animals have been difficult to find. To this
end, this study aimed to review the current literature to identify
animal species that have been conclusively shown to be permissive to
SARS-CoV-2 infection and transmission, and to collate the latest
information regarding natural and experimental infections of the virus
in animals, in order to assess the potential role of animals in
community transmission of COVID-19.