An update on COVID-19 and animals: ones which have been shown to be susceptible and related welfare issues
John T. Hancock, Ros Rouse and Emma Stone
Animal Welfare and Ethics Sub-Committee
University of the West of England, Bristol
Since our article of 20/07/2020 on “Predicting the susceptibility of animals to Covid-19”  it seems appropriate to review the situation with regards to animals reported as having the disease. Covid-19 continues to be a major issue in the human population, with regional and local lockdowns continuing in many countries. Therefore, a question which needs to be addressed is whether this has spread across animal populations, a possibility predicted from earlier work?
In our article the interactions between the SARS-CoV-2 spike proteins and a protein on human cells, i.e. angiotensin-converting-enzyme-2 (ACE2)  were discussed. Based on the homology of ACE2 in animals with that of the known human amino acid sequence, we estimated whether the spike proteins could recognise the ACE2 in different species. Damas et al.  predicted the susceptibility of over four hundred vertebrates, including mammals, birds, fish and reptiles based on whether spike proteins can recognise the ACE2 receptors. Although they suggested that all birds, fish, amphibians and reptiles could be classed as very low susceptibility, the situation with mammals was more complex. Primates seemed, perhaps with no great surprise, to be highly susceptible, while other mammals were less so. Of course concentrating on ACE2 is a narrow view of the pathogenesis of SARS-CoV-2 as other proteins may be involved . Having said that, now the virus has been circulating in the human population for several months, have other animals also suffered, as these ACE2-based predictions suggest they should?
There are several issues with the potential of animals’ susceptibility. Will the animals themselves get ill and potentially die? Will SARS-CoV-2 transmit across animal populations? Will the virus transmit to other species, and importantly, back to humans from animals? Will the human perception of the problem cause animal welfare issues? Concerns have been raised by the IUCN SSC Wildlife Health Specialist Group and the Primate Specialist Group who issued a joint statement on March 15 about Great Apes and guidance on how to protect them from Covid-19 . Nature reserves are being cordoned off and guidance given to local communities and those likely to be in contact with apes . Other organisations have developed similar guidance about working with wild mammals . Furthermore, recent evidence of the virus being present in human waste has led to concerns about the quality of sea water  and the potential danger to sea mammals , which are susceptible to coronaviruses . There are concerns about the transfer of Covid-19 from humans to bats . In addition, popular media are publishing articles with headlines such as “Owners warned not to kiss pets after first cat infected with coronavirus in UK”, which was in the Guardian on 27th July , although the same newspaper on 8th August published “We found the first cat in the UK with Covid-19 - but there's no need to panic” .
So what is the reality, and has there been disease in some animal species, as predicted? Primates can indeed suffer from Covid-19, e.g., SARS-CoV-2 has been reported to cause pneumonia in Rhesus macaques (Macaca mulatta)  and to affect the immune system in African green monkeys (Chlorocebus aethiops) , with severe effects seen in some animals. However, there are no reports of wild primates being infected. In a zoo in New York several lions and tigers fell ill and one tiger was confirmed to be positive for Covid-19 .
Domestic cats and dogs, because of their close proximity to humans, are of particular concern. A survey of cats and dogs in Italy in July 2020 suggested that Covid-19 was relatively widespread. Although no animals were positive using the polymerase chain reaction (PCR) test, when 817 companion animals were assessed for relevant antibody titres, 3.4% of dogs and 3.9% of cats were found to be positive. Some of these were from households thought to be Covid-19 negative for the human inhabitants . A domestic cat has tested positive in the UK  and dogs tested positive in Japan . Zhang et al. (2020) reported that cats in Wuhan China, where the Covid-19 outbreak is said to have originated, have tested positive for the virus . They concluded that a suitable distance should be maintained between Covid-19 patients and companion animals. On the 18th September 2020, a conference presentation by Dorothee Bienzle and her colleagues in Canada, for the ESCMID Conference on Coronavirus Disease, suggested that a substantial proportion of dogs and cats were infected by their owners . This was widely reported in the popular press at the time [22, 23]. In contrast, Temmam et al.  reviewed 21 domestic animals which were in close contact with Covid-19 positive humans, and although some animals appeared to show symptoms, none were positive when using the PCR-based test or were positive for relevant antibodies. In the USA there is a database of confirmed cases of SARS-Cov-2 in animals across all the States, using either the PCR or antibody tests, and at the time of writing this article (24th September 2020) there was one tiger, one lion, 21 cats, 17 dogs and five mink listed . Considering that up to the same day 6.96 million humans have been tested positive across the USA, with an estimated 202K deaths, even if there were to be significant under-reporting to the database of confirmed disease in animal subjects, the transmission to animals seems to be relatively very small, although more extensive testing could confirm that.
One of the most reported animal species to be infected by Covid-19 are mink. In the Netherlands and Spain this seems to be a significant problem, and it has led to the euthanasia of around a million animals . Mink farms in other countries have also reported Covid-19 positive animals, including the USA , and this has been a major blow for the fur industry. The concern about mustelids has led to the release of guidance for fieldwork, with particular consideration of potential impacts on black-footed ferrets (Mustela nigripes) which are listed as an endangered species in the USA [28, 29].
Shi et al.  tested the susceptibility of several animals, using inoculation. Although ferrets showed infection of their upper respiratory tracts the disease did not spread well between individuals. However, transmission was seen between pairs of domestic cats, and the infection was worse, being deeper in the respiratory system. Dogs (beagles) were less susceptible than cats and viral replication was less in these animals. This may be explained by differences in the ACE2 receptors in these animals, as investigated by Mathavarajah and Dellaire . Other animals tested, including pigs and birds (chicken and ducks), were not found to be susceptible . The authors suggest that surveillance of cat populations may be useful for the control of the spread of the SARS-CoV-2 virus.
There seems to be little doubt that animals can be infected by SARS-CoV-2, with regular reports of animals testing positive, both in laboratory settings and in society. However, there has to be a word of caution here . There have been some doubts about some positive results. There are two main tenets to the tests used: reverse transcriptase PCR (known as the PCR test) will find the presence of the viral RNA, so it is assumed that the virus is present; antibody-based tests will look for the response of an animal’s immune system, and can been used to assess whether an animal has previously been exposed, and importantly, responded. However, the PCR test is extremely sensitive, and does not say whether infectious virus is present, rather it reports the RNA presence. If this RNA is from viral fragments, which are not virulent, a positive result still may ensue. Further, as many animals are testing positive from homes in which the occupants are positive, it could be that the animals are simply carrying viral particles from the human, rather than being infected themselves . In addition, it is important to remember that there are numerous Coronaviruses, some of which are species specific, but they are all part of a family of similar viruses. There is a feline coronavirus  as well as a canine coronavirus, the latter being suggested as a model for studying SARS-CoV-2 . Therefore, simply because an animal shows symptoms of Covid-19 does not mean that it is infected with the human virus. Lastly, it appears that even when animals are infected with SARS-CoV-2 the majority seem to present less severe symptoms than those in humans, and they are thought to produce less virus to infect future hosts. Therefore, animals may not be an efficient means of SARS-CoV-2 transmission as discussed by Parry .
Although SARS-CoV-2 originated in an animal, since the initial outbreak there appears to be little evidence of humans catching Covid-19 from animals, although the transmission of the virus from mink to humans has been reported in mink farms . Despite animal-to-human transmission not being reported widely, there is still a perception that this can happen. Therefore, the presence of Covid-19 may have a significant impact on the welfare of animals. Guidance for communication about bats and Covid-19 has been published. Bats were thought to be the origin of Covid-19 raising concerns that they may be persecuted . Pets have been reported to have been abandoned as people leave their residences, and some authorities have said that stray pets would be killed . In Singapore rabbits have been abandoned . With the positive benefits that pets can bring to individuals and families, the loss of companion animals is not only a welfare problem but also a wellbeing issue .
Covid-19 also has indirect effects on animal welfare. For example, because of employees becoming ill, chickens have had to be slaughtered as they could not be used by the food industry . Furthermore, many animals are kept in captivity, and with travel and tourism restricted, the incomes for many establishments which keep animals has been severely reduced, casting into doubt the future of both the businesses and the animals. Whale and Dolphin Conversation highlights that 3500 marine mammals may be at risk of euthanasia . They also raise concerns that the pandemic is delaying the creation of both protective legislation and protected areas at sea for marine animals . In Papua New Guinea there are concerns about the forced closure of an animal welfare sanctuary. The loss of the Port Moresby Nature Park may mean euthanasia of hundreds of animals .
Other indirect consequences of the pandemic are from the use of personal protective equipment (PPE). There are several reports of birds being entrapped by discarded face masks [44, 45]. Conversely, some birds seem to have a reduced fear response to people when they are wearing a face mask .
A recent observation is that dogs may be able to sniff the presence of the virus, and therefore be useful in the fight against the pandemic . It is unclear how the animals are doing this, but they seem to be able to sense something, even before people are showing symptoms. It also poses the question as to whether other animals can sense, and perhaps avoid, the virus.
With the concern that animals can catch and/or spread disease from humans it has been suggested that a “One Health” policy is adopted [48, 49]. This concept seeks to embrace the health of animals alongside that of humans for a more holistic approach to ecosystem health. Even plants have been suggested to be encompassed in this concept . However, such a policy would require integration of research disciplines, embracing more ethical considerations  and a major input from governments. The ‘One Health’ concept has also tended to focus on the health of animals only in relation to improving human health outcomes, and a paradigm shift is necessary to ensure that animal health and welfare is seen as a goal not just a means to improved human health. In practical terms, in relation to Covid-19, this has implications, for example, for the availability of vaccines and treatments being made available for animals, as well as for humans, and the value of the study of naturally occurring disease in animals, such as studying companion animals alongside their humans, rather than animals solely being seen as test subjects in laboratory experiments.
It is clear that some animals are susceptible to SARS-CoV-2 and have symptoms of Covid-19. However, to date, no evidence has emerged of a widespread distribution of the virus in wild animals. Companion animals may be more at risk, with many dogs and cats being reported to be infected, while some farmed animals, such as mink, have also been shown to be positive for the virus. It is most likely that infected animals obtained the virus from people positive for Covid-19. There is little evidence of animals transmitting the disease back to humans, and in fact a person is much more likely to catch Covid-19 from another person than from an animal. To combat and manage future epidemics it has been suggested that a “One Health” policy is adopted across the globe , so that the health of animals is considered alongside that of humans for a holistic and integrated response. In the meantime, although relatively few animals have tested positive, animal welfare has become an issue, with some farmed animals (mink) and companion animals (cats, dogs and rabbits), being abandoned or killed. Despite concerns, transmission through animal populations or from animals to humans are unlikely to be widespread problems [11, 32].
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