COVID-19 pandemic, eighteen months on:
Animals which have been reported to be SARS-CoV-2 positive and impact on animal welfare
Katherine Heath1, Ros Rouse 2, John T. Hancock 1*,
- Department of Applied Sciences, University of the West of England, Bristol, BS16 1QY, UK
- Research, Business and Innovation, University of the West of England, Bristol, BS16 1QY, UK
* Correspondence: firstname.lastname@example.org Tel.: +44(0)1173282475
On the 2nd October 2020 we wrote an article for the AWRN on the state-of-play on the COVID-19 pandemic , as it pertains to animals and animal welfare. A year on, it seems timely to revisit the topic, especially as lockdowns are easing in several countries, including the UK, although some caution is probably needed as this happens . There have been other reviews published recently on the topic of animals during the pandemic [3,4], and the consensus of opinion appears to be that although animals can become infected, there is no need for panic about the spread of the disease back to humans.
The COVID-19 pandemic continues to be a major issue across the globe. At the time of writing (25/08/21) there have been 214,209,856 recorded cases of COVD-19 around the world with 4,469,469 deaths . How many animals have been infected remains unknown, but there are several interesting reports from a range of species.
The human disease, COVID-19, is caused by the coronavirus SARS-CoV-2, which was thought to have originated in a bat, and then passed to humans through an intermediate animal species, perhaps a pangolin, but this has been disputed and never confirmed . However, having a likely animal origin makes it likely that it can also infect other animals. Alternatively, the virus may have originated in a laboratory, but again, this has never been confirmed . Regardless of its origin, its impact on animals, whether they are companion animals or in the wild, is important to ascertain.
Several bioinformatic studies [8,9], including our own , have tried to predict which animals are likely to be susceptible to the SARS-CoV-2 virus, but this has not been very successful. The virus gains entry to cells using the angiotensin-converting-enzyme-2 (ACE2) receptor , but it is known that there are several other proteins involved. Even looking at the homology of several of these proteins, including Transmembrane Protease Serine Type2 (TMPRSS2), furin and neuropilin-1 , there still seems little evidence as to why certain animal species are being found to be positive for the virus, whilst others have not.
Sequence homology analysis has, as might be predicted, shown that the non-human primates are likely to be susceptible. This has been borne out in reality, with captive gorillas being found to be virus positive . This has raised issues about tourism and gorillas  so that the wild populations are not infected, as it would not be known how well such animal communities would transmit the disease. Experimentally, Green monkeys, old world monkeys such as Macaca mulatta and Macaca fascicularis, and rhesus macaques could be infected with SARS-CoV-2. Symptoms similar to those seen with COVID-19 were reported, including decreased appetite, laboured breathing and temperature spikes. There were also similar pathological changes in the pulmonary tissues and similar time periods of viral shedding [14-16].
On the other end of the spectrum of vertebrates for which bioinformatics has been used to predict disease susceptibility, several animal groups were predicted to be safe from infection. These include fish, amphibians, reptiles and birds [8-10]. To date, this seems to be the case, as no reports of disease in these species being published, either from captive (including companion), or wild populations.
There are, however, many animal species for which predictions and reality do not relate. One of the animal groups of most concern are the mustelids. Predictions from protein sequences [8-10] suggest that such animals should be of low SARS-CoV-2 susceptibility, and yet mink in farms  and in the wild  have been found to be virus positive. In Denmark alone, 17 million mink were culled as there was concern over the risk to human health , as it is known that animal-human transmission is possible .
Other species of possible concern are the felines and the canines. Many cat species have been found to test positive, including domestic , lions and tigers , and cougars . This can be serious for these species, with death of lions being reported following SARS-CoV-2 infection . Transmission of the virus amongst the cat population is possible , and therefore there is a risk for viral spread, especially considering the nature of cats roaming their neighbourhoods. However, there seems no cat-to-human transmission and it does not seem to be causing a major health population in domestic cats. Dogs too can become SARS-Cov-2 infected . However, they seem to be less severely affected and they have less viral shedding , suggesting that they pose less risk of either transmission or to human health.
There are reports of other companion animals being able to be infected with SARS-CoV-2, but there is little evidence that this causes an issue to either viral spread or human health. For example, in hamsters, some transmission was possible, but the animals recovered from symptoms similar to those seen in humans .
One group of animals which were predicted to be susceptible were some of the marine mammals [8-10]. This included the beluga whale (Delphinapterus leucas), dolphin (Tursiops truncates) and killer whale (Orcinus orca). However, even though the COVID-19 causing virus could potentially exist in wastewater and sea water [29,30], so exposing such animals to infection, there have not been reports of such animals testing positive for SARS-CoV-2. This could, of course, be that such animals have not been tested. If they had non-severe symptoms, they might simply recover, and the disease go un-noticed in such species.
What is clear from the data so far is that animals can become SARS-CoV-2 infected, but that this is hard to predict, although it also does not seem to be major issue, at least so far. There is a risk that virus variants may arise in animals and get transmitted back to the human population, and this concern has been raised in relation to mink farms . Therefore, as the pandemic continues this does remain a risk.
The virus was first detected in Wuhan, China , but since then there are numerous variants . Some of these may have better transmission and cause more severe disease in humans, and there are some concerns that vaccinations will need to be altered to combat such viral variants. What is not widely known is how such viruses will infect animals. The B.1.1.7 variant has been found to infect cats and dogs in the USA . The B.1.1.7 variant contains 23 mutations which leads to 17 amino acid differences in the primary sequence , and this will no doubt lead to changes in the secondary and tertiary structures of proteins. Hence, such variants will cause the interaction of viral proteins with host proteins (such as ACE2) to be different. In our paper  we looked at polymorphisms in the host proteins which may make a significant difference to protein/protein interactions, but of course changes in either viral or host proteins will be important to understand. This is especially important because animal populations may be a reservoir for the virus and be where new variants may arise . If these were more harmful to humans, and were to transmit to human populations, there could be a potential problem.
There are still indirect effects of the COVID-19 pandemic on animal welfare. The increased use of personal protective equipment (PPE), especially by the public, has led to severe damage to the environment. Fish have been caught in gloves and PPE found in canals, for example . COVID-19-associated PPE has been found on beaches  and river outlets , suggesting that there is danger to marine wildlife. Plastics have been a concern for the environment for some time and the plastic use in PPE and the increased use during the pandemic has brought this to the fore . Clearly, future PPE use needs to consider animal welfare and the environment, not just human health.
The way out of the pandemic is thought to be through the extensive use of vaccines . Of course, the emergence of viral variants will affect the efficacy of any vaccine . Having said that, vaccines for use in animals are being developed. One of the first to be developed was in Russia : the Carnivac-Cov vaccine. In the USA, bears, tigers, gibbons, hyenas, chimpanzees, mountain lions and baboons are amongst zoo animals which are being vaccinated against the SARS-Cov-2 virus. This is being supplied by Zoetis . Clearly, there is a concern that certain zoo animals will be able to become infected from the staff working there or from the public when they visit. Certainly, the alternative is to close the zoo from visitors as has happened in Indian tiger reserves .
The above discussion, although not a comprehensive coverage of all the literature, shows that there are indeed impacts of the COVD-19 pandemic on animals, both in the case of health and welfare. Coronavirus outbreaks have been predicted in the past , so the present pandemic is unlikely to be the last. Therefore, lessons need to be learnt from our present situation, and with regards to animals and their welfare there are many issues which need to be addressed:
- Can better prediction tools of animal susceptibility to coronaviruses be developed? This would require more genome sequencing and the use of structural protein analysis, not just the sequence alignment used by some . However, this is time consuming and expensive, so may need to be targeted to specific species.
- Will SARS-CoV-2 variants or other coronaviruses affect animals more?
- Are there animals which are at risk, but of which we are not yet aware? Many animals are used in work environments (e.g. horses, elephants), whilst others may be in care and conservation areas (e.g. sloths). Should there be more systematic and widespread animal testing and monitoring, so that the true impact on animal communities, and on interspecies transmission, is known?
- Do animals pose a real threat as a viral pool from which new variants may arise?
- Should animal confinement in farms such as those containing mink be reconsidered, so that viral transmission is reduced, and animal welfare increased?
- Should PPE be produced which is more environmentally friendly? Can their plastic content be reduced/removed without reducing effectiveness, and can they be more biodegradable?
- Is there a justification for vaccinating animals when there are areas of the world where humans are still not able to get access to vaccines , and what are the factors influencing such decisions?
- Should waste from human activity be more controlled, so that water [29,30] is not contaminated with virus or PPE ?
In conclusion, whilst some animals seem to be safe from the SARS-CoV-2 virus, such as fish, reptiles and birds, others have been found to be infected, including gorillas, cats, dogs, otters, deer and especially mink. A full list of animals which have tested positive for the virus in the USA is available , as well as for the world . Transmission between individuals of a species have been reported, for example with cats and mink, and transmission back to humans has been reported for mink. However, there does not seem to be a widespread problem of viral transmission in animals. Some individual animals have received COVID-19 vaccinations [43,44], but this has not been widely adopted. At the present time, except for the protection of certain animals, such as gorillas in zoos, there is no need for widespread concern for animals being directly affected by the virus. There are, however, concerns about poor animal welfare leading to increased transmission in some farming practices and the use of PPE is having a significant environmental impact [37-39]. The COVID-19 pandemic will not be the last epidemic/pandemic which is caused by a coronavirus  and lessons need to be learnt. Animals, and their welfare, have not been at the forefront of discussions during the last eighteen months, with human health, perhaps predictably, being at the fore of most discussions. But moving into the future, the OneHealth strategy , in its broadest sense to include animal as well as human welfare, should be considered more, and then perhaps a future pandemic can be avoided.
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Acknowledgements: KH was sponsored by the Department of Applied Sciences, UWE, as a UG summer intern.
Conflicts of interest: the authors declare there are none.
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