The zoonotic nature of SARS-CoV-2 has been evident since the onset of the pandemic, with origins rooted in wildlife. The broad host range accompanied by efficient transmission1,2, raised concerns about the possibility of reverse zoonosis, whereby humans would transmit the virus back into non-human animal populations.
Reverse zoonosis is a concern, since infecting novel animal host species with SARS-CoV-2 may lead to the virus evolving in new directions. Adaptive changes to a new host species might lead a virus to become less infectious to other species, including humans. On the other hand, viruses jumping into animals could also lead to mutations affecting host evasion while retaining infectivity, creating the conditions for transmission from non-human animals back into humans (sometimes called spillback). An example of mutated SARS-CoV-2 spilling back into the human population occurred when a lineage evolved in captive mink and infected mink farm workers in the Netherlands 3.
Given concerns about the possibility of reverse zoonotic transmission of SARS-CoV-2, we established a collaborative group in the Canadian provinces of Ontario and Quebec, beginning early in the summer 2020 to carry out wildlife disease surveillance. Our group included people with a range of backgrounds and expertise, including wildlife scientists, public health experts, animal health experts, and virologists. We took advantage of existing wildlife monitoring programs to obtain samples opportunistically, while ensuring precautions were implemented to avoid the spread of SARS-CoV-2 between humans and wildlife. During that first summer of 2020, and through the following autumn and winter, we detected no evidence of SARS-CoV-2 in wildlife 4.
In early 2021, data began to accumulate showing that the white-tailed deer (Fig. 1), a common North American ungulate, was susceptible to SARS-CoV-2 infection 5 and that free-ranging deer had been exposed to SARS-CoV-2 in several states in the USA 6. Indeed, transmission from deer to humans appeared to have occurred frequently 7,8. These findings led our collaborative group to expand surveillance efforts to include white-tailed deer. We accomplished this by partnering with ongoing Chronic Wasting Disease (CWD) surveillance programs that operated in Ontario and Quebec, working with deer hunters in both provinces to obtain samples from harvested deer. CWD is a prion disease afflicting deer, which has not been detected in Ontario, and only at one location in Quebec 9.
We sampled white-tailed deer during the CWD surveillance program in southwestern Ontario in autumn 2021 and discovered a highly divergent lineage of SARS-CoV-2 in deer 10. The lineage had 79 mutations compared to ancestral SARS-CoV-2, with the closest common ancestor being viruses derived from both mink and people in nearby Michigan, USA about a year earlier. This suggests that deer were infected with SARS-CoV-2 through interspecies transmission from either mink or people. The Ontario deer virus, now called B.1.641, shared some mutations with viruses derived from Michigan mink, but there were also some indications that it had been evolving in deer, given the observed mutations. While investigating the B.1.641 genomic sequences from virus that we recovered from deer, we also identified a human-derived virus from the same region of Ontario and sampling time frame, with a very similar genomic sequence, suggesting there has been spillback, or deer-to-human transmission of B.1.641. Subsequent investigations confirmed the human case had known contact with deer.
Figure 1. The white-tailed deer (Odocoileus virginianus) is a common ungulate in eastern North America that is susceptible to SARS-CoV-2 infection. Picture credit: Jacob Bowman.
Our SARS-CoV-2 wildlife surveillance collaboration included investigators from government and academic sectors, and across fields ranging from wildlife science to virology to public health. This is the kind of diverse collaboration that seems essential to implement a One Health surveillance program, which cuts across sectors by definition. One Health is defined by the One Health High Level Expert Panel (OHHLEP) as “an integrated, unifying approach that aims to sustainably balance and optimize the health of people, animals and ecosystems 11. The OHHLEP underscores the importance of unifying approaches, which has proven to be a great benefit for our surveillance work, especially given the findings of a novel virus in wildlife and an associated human case, where there are potential implications for all three legs of the One Health stool: animals, people, and environment.
One Health has the benefit of bringing together experts with a range of backgrounds to consider processes occurring across sectors (i.e., people, animals, and environment). However, there are also challenges that can arise. For example, formal One Health governance structures tend not to be in place, or are novel, and gaps in responsibility can emerge. Operational funding is also elusive, with many contributors, but no clear revenue stream(s) to support activities. We continue to learn how best to address the various opportunities and challenges that arise from One Health, but overall consider the approach to be essential.
In our experience, One Health has been facilitated through a combination of formal and informal structures. In Canada, there is a Federal/Provincial/Territorial One Health Working Group that emerged during the pandemic that served to connect workers within local regions, at a national level, and also to connect to global initiatives. The Federal One Health group has also co-ordinated a pan-Canadian surveillance initiative, to which our surveillance group contributes. We have also benefited from the informal network of our collaborative surveillance group. It has been important to maintain connections through these formal and informal structures. Ironically, this may have become easier during the pandemic due to the proliferation of video conferencing. Although some of our surveillance group have never actually met in person, we have had regular contact, facilitated by technology.
The COVID-19 pandemic has demonstrated the importance of zoonotic disease to society, and this has been underscored more recently by the appearance of other pathogens such as avian influenza and monkeypox. Long-term environmental trends suggest that zoonotic diseases will likely continue to be important. For example, increasing human-wildlife contact will likely result in the emergence or discovery of new zoonotic diseases. Consequently, carrying out wildlife surveillance for zoonotic diseases will continue to be a vital part of an effective One Health strategy 12,13.
- Shi, J., et al. Susceptibility of ferrets, cats, dogs, and other domesticated animals to SARS–coronavirus 2. Science 368, 1016–1020 (2020)
- Damas, G. M., et al. Broad host range of SARS-CoV-2 predicted by comparative and structural analysis of ACE2 in vertebrates. Proc. Natl. Acad. Sci. 117, 22311–22322 (2020).
- Oude Munnink, B. B., et al. Transmission of SARS-CoV-2 on mink farms between humans and mink and back to humans. Science 371, 172–177 (2021).
- Greenhorn, J.E., et al. SARS-CoV-2 wildlife surveillance in Ontario and Québec. Can. Communicable Dis. Rep. 48, 243–251 (2022).
- Palmer, M. V, et al. Susceptibility of white-tailed deer (Odocoileus virginianus) to SARS-CoV-2. J. Virol. 95, e00083-21 (2021).
- Chandler, J. C., et al. SARS-CoV-2 exposure in wild white-tailed deer (Odocoileus virginianus). Proc. Natl. Acad. Sci. 118, e2114828118 (2021).
- Hale, V. L., et al. SARS-CoV-2 infection in free-ranging white-tailed deer. Nature, 602, 481–486 (2022).
- Kuchipudi, S. V., et al. Multiple spillovers and onward transmission of SARS-CoV-2 in free-living and captive white-tailed deer. Proc. Nat. Acad. Sci. 119, e2121644119 (2022).
- Gagnier, M., Laurion, I. & DeNicola, A. J. Control and surveillance operations to prevent Chronic Wasting Disease establishment in free-ranging white-tailed deer in Québec, Canada. Animals, 10, 283 (2020).
- Pickering et al. Divergent SARS-CoV-2 variant emerges in white-tailed deer with deer-to-human transmission. Nat. Microbiol. doi: 10.1038/s41564-022-01268-9 (2022).
- Joint Tripartite (FAO, OIE, WHO) and UNEP Statement. Tripartite and UNEP support OHHLEP's definition of "One Health" (2021). https://www.who.int/news/item/01-12-2021-tripartite-and-unep-support-ohhlep-s-definition-of-one-health
- Food and Agriculture Organization (FAO), World Organisation for Animal Health (OIE) and World Health Organization (WHO). Joint statement on the prioritization of monitoring SARS-CoV-2 infection in wildlife and preventing the formation of animal reservoirs (2022). https://www.who.int/news/item/07-03-2022-joint-statement-on-the-prioritization-of-monitoring-sars-cov-2-infection-in-wildlife-and-preventing-the-formation-of-animal-reservoirs.
- Lefrançois, T., et al. After 2 years of the COVID-19 pandemic, translating One Health into action is urgent. The Lancet doi:10.1016/S0140-6736(22)01840-2 (2022).