Research and analysis

SARS-CoV-2 risk to UK cervid populations

Published 9 March 2023

Summary

This document is part of a series of 3 risk assessments into the likelihood and consequence of SARS-CoV-2 infection of the cervid population in the UK through various pathways and the potential spread to humans. The risk associated with food consumption and exposure to infected cervids will be the second and third documents as part of this Human Animal Infections and Risk Surveillance (HAIRS) group product.

Since 2021, the US and Canada have reported infection of white-tailed deer (WTD; Odocoileus virginianus) populations with SARS-CoV-2, which constitute the first confirmed cases of ruminant infection and transmission within livestock, globally. Concerns were raised about the possibility of these populations to form a reservoir for infection to pass back to humans, for viral evolution to be driven by infecting these animals and for any new variants to be capable of evading the immune response.

Between January to March 2021, SARS-CoV-2 was detected using real-time reverse transcription polymerase chain reaction (rRT-PCR) in 129 out of 360 (35.8%) free-ranging WTD from northeast Ohio. Experimental infections of WTD demonstrated animal-to-animal transmission and the high prevalence in the herds suggests this is occurring in the environment. More recently (April 2022) there was a report of related mule deer (Odocoileus hemionus) in the US also testing positive (5% seropositivity in a herd). Multiple human-to-deer incursions appear to have occurred over several months across the US (1). One small cluster of viral sequences detected in WTD was highly divergent, indicating adaption of the virus to new host species, and there is one reference human sequence in this cluster which indicates limited spill-back to the human population for this variant (2).

Previous research​ led by the US Department of Agriculture had shown evidence of antibodies in wild deer​. Deeper research into the Ohio cases showed infection was caused by at least 3 variants of SARS-CoV-2 in 6 northeast Ohio locations (3). The viruses were isolated and sequenced and based on this genomic sequencing, variants infecting wild deer matched strains of the SARS-CoV-2 virus that had been prevalent in Ohio coronavirus (COVID-19) patients at the time. Sample collection occurred before the Delta variant was widespread, and that variant was not detected in these deer. The fact that wild deer can become infected “leads toward the idea that we might actually have established a new maintenance host outside humans”.

Twenty-eight states have now reported SARS-CoV-2 in wildlife, where wildlife includes mule deer and wild mink. The period during which the virus can be detected in experimentally infected deer is 1 to 7 days post inoculation (4), but field data is not available. Nevertheless, the evidence strongly suggests SARS-CoV-2 has circulated widely in the North American WTD population and resulted in divergent viral strains.

This assessment considers the potential routes of entry for SARS-CoV-2 into the UK deer populations.

The main conclusions from this assessment were:

1. Immunohistochemistry of binding sites in tissue samples from UK deer species indicates they could be susceptible to infection with SARS-CoV-2, based on the presence of the ACE-2 receptor in the digestive tract, nasal passages and upper respiratory tract. However, further work to determine the other proteins necessary for viral cleavage and cell entry (for example the furin protein) may also be important and has not been done.

2. The likelihood of cases occurring as a result of imports is negligible as cervid imports are not allowed from the US or Canada due to the presence there of chronic wasting disease (CWD).

3. The likelihood of cases being detected in the UK deer population is dependent on the level of contact with humans. Roe deer, which are the most related to WTD, are generally solitary animals, so the risk of introduction will depend on the level of wider environmental contamination, rather than direct contact with other infected cervids. Other species of deer are farmed in the UK, but the level of human contact is expected to be lower than for WTD in the US, where herds are managed and culled for CWD controls and hunted using baits and lures, increasing the potential for contamination. No systematic testing of UK deer populations for evidence of SARS-CoV-2 infection, wild or captive, has been undertaken yet but there are research programmes looking into this.

4. The likelihood of the spread of a SARS-CoV-2 infection through farmed or captive deer species is difficult to assess. However, given the speed of spread in the US, it must be considered plausible. The virus can be detected in the faeces and urine of infected people. Therefore, the presence of SARS-CoV-2 receptors in the cervid digestive tract leads to the expectation that the virus may be excreted in deer faeces and/or urine. Both are attractive to other deer, therefore transmission through this indirect route is likely.

5. In the US, new foci of CWD are often detected first in farmed herds, before detection in local wild cervids, so the contact between these 2 discrete populations is clearly sufficiently high to facilitate transmission in North America.

6. The possible sources of infection into a deer population would include contact with humans, contact with contaminated equipment or a contaminated environment or contact with an unknown reservoir species. In the US, there are farmed and wild mink, both of which have tested positive, and disease transmission from infected mink to other mink and to humans has been observed during the pandemic. The presence of other wild small mammal reservoir hosts cannot be ruled out.

7. Of the cervid species in Britain, red deer (Cervus elaphus elaphus), fallow deer (Dama dama), roe deer (Capreolus capreolus) and the non-native populations of Sika deer, Chinese Water deer and Muntjac deer are all likely to be susceptible.

8. There are multiple examples of contact between deer and livestock species in the UK (5) and therefore the potential for spread into these other species is plausible, but without understanding the routes of spread (oral faecal, respiratory and so on) or the infectious dose required, there is high uncertainty. The recent finding of antibodies to SARS-CoV-2 in cattle suggests spillover events can happen but there is no evidence of further virus spread between cattle.

Overall, the probability of importing SARS-CoV-2 into the UK’s deer herds through the imports of live cervids from the US and Canada is negligible, because imports are not allowed under current certification requirements. However, the likelihood of any single deer in the UK becoming infected with SARS-CoV-2 following contact with an infected human is considered to be high, given the in vitro studies of viral receptors and considering how frequently it has happened in North America.

The likelihood of spread among the deer population is greater (medium but with high uncertainty given the lack of surveillance) in herds of deer or large captive deer populations rather than the more solitary wild deer (very low likelihood during non-breeding seasons when animals remain solitary). Nevertheless, it will depend on whether deer can sustain infection independent of the prevalence in the human population or whether it will burn out quickly. The population size in North America is quite different to that of the UK (35 million WTD in the US compared to 100,000 fallow deer in the UK) and therefore the effective population size (the population required to maintain virus circulation) would be considerably higher.

The public health aspects of the likely spread from deer to humans through consumption or occupational exposure are considered separately by the Food Standards Agency and the UK Health Security Agency (UKHSA), but 3 assessments have been written as a joint project (to be published). The conclusions from the joint analysis are as follows.

1. The likelihood of a SARS-CoV-2 infected deer being imported to the UK is negligible (low uncertainty).
2. The likelihood of a reverse zoonosis event occurring, resulting in SARS-CoV-2 being introduced into a UK cervid population [Entry assessment] is considered to be medium likelihood and medium uncertainty.
3. The likelihood of a cervid variant of SARS-CoV2 causing infection in other livestock or wildlife species [Exposure assessment] is considered to be overall: high likelihood for cervids, very low for other livestock and non-negligible for wildlife.
4. The likelihood of infection in British deer leading to human infection through consumption is negligible and through occupational exposure is very low.
5. The likelihood of a cervid SARS-CoV-2 variant in the US or Canada posing a different or greater risk than the strains circulating in humans [Consequence assessment] is considered to be unlikely, but with high uncertainty.

Background

There have now been multiple reports of both natural and experimental infection of WTD with strains of SARS-CoV-2 in North America. There is no confirmed route for infection from humans or from the environment yet, but evidence of strain sequences suggests human to deer spillover has occurred multiple times at different sites.

The first reports came from Ohio State University scientists who had obtained nasal swab samples from 360 WTD at 9 sites from January through March 2021 in Ohio State. Of the 360 deer sampled, 129 (25.8%) tested positive for SARS-CoV-2 using rRT-PCR. The deer had been culled for population control. Deer in 6 of the locations were infected with 3 SARS-CoV-2 lineages (B.1.2, B.1.582, B.1.596 – none of which were variants of concern). The B.1.2 viruses, widely circulating in people in Ohio at the time of testing, infected deer at 4 sites. The researchers analysed the evolutionary relationships of the lineages and found evidence for 6 independent human-to-deer transmission events. The authors noted that “Probable deer-to-deer transmission of B.1.2, B.1.582, and B.1.596 viruses was observed”; they also noted mutations to the viral spike protein in some deer samples that are not commonly seen in human infections.

The investigators said the prevalence of infection varied from 13.5% to 70% across the 9 sites, with the highest prevalence observed in 4 sites that were surrounded by more densely populated human neighbourhoods. There was evidence for 6 different viral introductions into the deer populations. Sample collection occurred before the more transmissible Delta and Omicron variants were known to be infecting people, and the Ohio state team did not detect either variant in the deer.

WTD infected with SARS-CoV-2 have now been detected in multiple regions in the US at prevalence rates of neutralising antibody of around 40% (3, 6). Also, WTD were susceptible to experimental infection with SARS-CoV-2 and the virus was transmitted to uninfected deer that were caged with the infected animals (4). Sylvatic transmission among deer and multiple spillovers from humans to deer have also been confirmed (3, 7, 8). To date, SARS-CoV-2 viruses observed in deer have appeared similar to prevalent lineages circulating in nearby human populations, suggesting multiple, recent spillover events (7, 8).

In Canada, WTD have tested positive in Quebec and Ontario. Kotwa and others (2022) found 1.2% prevalence of positive PCR nasal swabs and 5.6% neutralising antibody positive from 258 animals in Quebec during November 2021 (7), while Pickering and others (2022) sampled WTD from Ontario in autumn 2021 and also found low prevalence of positive PCR detections from 5 out of 201 nasal swabs (2). Genome sequencing for the Ontario isolates showed a highly divergent B1 lineage with the closest clade being mink and human sequences found in Michigan, US in October 2020 and a human case in Ontario also found during 2021 who had had close contact with deer and tested positive at a time when the majority of human cases in the area were infected with the Omicron variant. Further information about this possible deer-to-human case is now published (2) which does indeed suggest deer-to-human transmission has occurred.

Efficient deer-to-deer transmission in WTD experimental infections was observed between day 3 and day 5 out of a 9-day contact experiment (9). The sequences derived from the infected animals showed no substantial viral variation between the index animals and the contact infected animals. However, work by Marques and others (2022) on deer in Pennsylvania demonstrated that 2 alpha sequences from animals in adjoining counties differed substantially and are likely to be the result of within deer transmission over time (10).

Hazard identification

The hazard is identified as SARS-CoV-2 viruses. No specific strain identified.

Risk question

This risk assessment considers the likelihood of introduction of SARS-CoV-2 into the UK deer herd and the risk posed by wider circulation if SARS-CoV-2 is detected in any of our wild or captive populations.

The specific risk question is:

What is the risk of SARS-CoV-2 being introduced into the deer populations of the UK and causing infection in farmed or other wild cervid populations?

To answer the above question, the risk assessment follows the OIE framework of release (or entry), exposure and consequence assessment.

Specifically, it is divided into 3 main areas:

1a. What is the likelihood of an infected deer being introduced from North America to the UK? [Entry assessment]

1b. What is the likelihood of a reverse zoonosis event occurring, resulting in SARS-CoV-2 being introduced into a UK cervid population? [Entry assessment]

2. What is the likelihood of a cervid-origin SARS-CoV-2 causing infection in other farmed or wild cervid species? [Exposure assessment]

3. Does the cervid variant in the US or Canada pose a different or greater risk than the strains circulating in humans? [Consequence assessment]

Risk assessment

Terminology related to the assessed level of risk

For the purpose of the risk assessment, the following terminology will apply.

Negligible

So rare that it does not merit to be considered.

Very low

Very rare but cannot be excluded.

Low

Rare but does occur.

Medium

Occurs regularly.

High

Occurs often.

Very high

Event occurs almost certainly.

Entry assessment through imports

The routes by which any viral pathogen may be introduced into the UK from US or Canada and the likelihood based on trade rules are:

• importation of live deer (including reindeer, other cervids, other animals) – negligible: no trade allowed
• importation of deer urine lures – negligible: all urine must be processed, which includes heat treatment which would be sufficient to destroy heat labile viruses
• importation of meat and other products derived from cervid species (for example trophy items including antlers, semen) – negligible given the poor persistence of the virus on surfaces
• importation of animal feed – negligible as no trade is allowed
• hunters and other tourists (skiers and walkers) and British service personnel travelling from affected areas to the UK with contaminated equipment (such as boots, clothing, knives) – negligible given the poor environmental persistence of the virus

The assumption is that at present we are only concerned with the findings in the US and Canada and no other countries have detected SARS-CoV-2, but the only reports of surveillance in other countries are Austria and Germany (11). Nevertheless, it cannot be ruled out and the risk pathways would include live animals if the country were approved for consigning live cervids to the UK. Deer imports from the EU are very low numbers and if SARS-CoV-2 infection were present, it is possible they would arrive while infectious, but given the short period during which they are viraemic this is still considered a very low risk (9).

Entry assessment based on reverse zoonosis

The likelihood of spillover from humans to deer is a highly plausible pathway for animal populations which are handled frequently. The possibility of transmission resulting from contact with contaminated wastewater containing human faeces has not been shown and is thought to be unlikely given the dilution effect. It is possible wildlife reservoirs, such as small mammals, may be an intermediate host, although testing has been carried out in some areas, and the likelihood of finding infected wildlife has proven to be very low (12).

Given the results of sequencing of the North American isolates from deer and humans and the close similarity, the balance of probability lies with this being indirect contact with infected humans while managing the herds of deer, providing additional feed or undertaking testing for CWD and other disease controls.

Management of deer herds in the UK would still involve some contact, but wide-ranging herds of deer are less abundant than in the US. Some of our more common deer tend to be solitary or live as small family groups. The British Deer Society published guidance throughout the COVID-19 lockdown period to remind people to only undertake essential work and to use sanitary measures to avoid possible transmission to other workers or the animals.

Cervids are susceptible, as seen from the US and Canada situation. While no cases in deer have been detected in Europe yet, only Germany and Austria have done any systematic surveillance in red, roe and fallow deer (11). APHA Weybridge pathology department has shown conclusively that deer have available ACE-2 receptors, which bind SARS-CoV-2 in the respiratory tract, specifically the respiratory and olfactory epithelium and submucosa glands (13, and Personal Communication). While the presence is not definitive proof of likely infection, it is a strong indicator and the findings in the respiratory and olfactory glands also support this being a direct contact infection through respiratory or nose-to-nose contact.

Therefore, the likelihood of a reverse zoonosis event occurring from humans to animals is medium with high uncertainty, given the susceptibility of the cervid population and the high circulation of SARS-CoV-2 in the UK coupled with the lack of surveillance in deer, the widespread vaccination of the human population and the recent relaxation of lockdown rules. However, this will fluctuate with the prevalence in the human population going forward, the effective population size of the cervid population and the strains circulating. The high level of uncertainty also relates to the level of contact between humans working with cervids and the routes of indirect transmission.

Exposure assessment

Contact with other cervids

Should a farmed deer become infected, there is a high likelihood virus would spread to other in-contact conspecifics, but the level of contact with wild deer may not be as high as for other farmed deer. It is, nevertheless, difficult to prevent contact between wild and farmed deer and in the US, diseases such as CWD are often detected first in farmed deer where there are more regular inspections. Deer do carry out behaviour during the rut which brings stags into close contact with hinds’ perianal region and spraying urine to attract females is common. If virus is present in the urine of infected animals, as it is for humans, this would be a suitable transmission pathway.

Deer-to-deer transmission has been shown in experimental work and has been inferred for field transmission based on sequence analysis of within herd viral isolates.

Contact with other livestock

Contact between wild deer and grazing livestock is possible, but close nose-to-nose contact is less likely. Experimental infections of livestock have given variable results, with ruminants demonstrating very low susceptibility while pigs and poultry appear to be refractory to infection (14, 15, 16, 17, 18), but cattle have tested positive by ELISA and weakly positive by virus neutralisation tests for antibodies on farms where the keepers were also testing positive (19). For deer to introduce infection to cattle or other ruminants, in the absence of nose-to-nose contact and given the poor environmental persistence of SARS-CoV-2 (several days maximum in various media and matrices), this pathway is considered a very low likelihood with low uncertainty.

Contact with wildlife

The term wildlife does not in this instance include wild deer (as we would include those in the section above). It is not possible to give a likelihood for this particular pathway as there is not enough evidence of wildlife becoming readily infected in the field, except those surrounding mink farms, where feral or escaped mink have tested positive. Therefore, while this is a plausible pathway, the uncertainty is high and the likelihood is non-negligible.

Consequence assessment

Considering the variants which have been detected in the US and Canada, there is some evidence that multiple incursions into the deer have occurred and only one possible instance of a deer-to-human transmission case. The variants detected in deer were not variants of concern (according to international terminology) and the mutations observed, compared to the Wuhan reference strain were not unexpected. Therefore, there is no evidence that the variants derived from cervid populations pose a greater problem to humans than the already circulating human strains, were zoonotic transmission to occur. However, it is not clear if continual circulation of SARS-CoV-2 in deer populations (in the absence of human to deer spillover) will eventually result in substantial evolution to variants of concern. The likelihood of high consequence is unlikely, but there is high uncertainty at this stage.

Conclusions

There is significant uncertainty associated with estimating the risk of SARS-CoV-2 entering the UK deer population as the mechanism for incursion in the US and Canada herds is not fully understood. Notwithstanding this uncertainty, the probability of a British deer becoming infected as a result of contact with an infected human is medium but with high uncertainty, given the susceptibility of deer species, the level of close contact with humans, widespread vaccination administration in humans and the guidance on working with animals during COVID-19 lockdowns. The risk from imports of any commodity is negligible.

In terms of exposure to other deer, the likelihood is high (medium uncertainty due to the solitary nature of some deer species), for livestock it is very low (low uncertainty) and for wildlife (not deer) it is non-negligible but as it was not possible to assign a risk level, uncertainty is high.

The consequences of SARS-CoV-2 infection mostly concerns whether new variants could arise which would jump back into humans and evade the immune protection conferred by vaccination. Evidence of the US and Canada cases suggests the genetic diversity of isolates is still largely aligned to the human population variants with no additional mutations leading to variants of concern. However, this cannot be ruled out given with wide prevalence in the deer populations in the US and Canada and whether this becomes widely established, driving emerging variants.

Current research indicates that of the 6 free-ranging deer species in the UK, red deer, and muntjac are susceptible to SARS-CoV-2, based on the ACE-2 receptor presence in respiratory and olfactory tissues. Roe deer are the closest related to WTD but farmed fallow deer are the most numerous and widespread in the UK. Wild roe deer are also ubiquitous but tend to live in smaller groups and do not herd to the same extent as WTD; therefore, establishment of SARS-CoV-2 may be less likely. However, surveillance needs to be undertaken to better understand the possible prevalence and spread pathways.

This assessment will be kept under review and updated as more information becomes available.

Acknowledgements

Dr Fabian Lean (Animal and Plant Health Agency (APHA)) for the information about histopathology and receptor distribution in deer populations, and Professor Richard (Dez) Delahay for information on serological surveillance in UK deer populations.

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