The ecology of chronic wasting disease in wildlife

Abstract

Prions are misfolded infectious proteins responsible for a group of fatal neurodegenerative diseases termed transmissible spongiform encephalopathy or prion diseases. Chronic Wasting Disease (CWD) is the prion disease with the highest spillover potential, affecting at least seven Cervidae (deer) species. The zoonotic potential of CWD is inconclusive and cannot be ruled out. A risk of infection for other domestic and wildlife species is also plausible. Here, we review the current status of the knowledge with respect to CWD ecology in wildlife. Our current understanding of the geographic distribution of CWD lacks spatial and temporal detail, does not consider the biogeography of infectious diseases, and is largely biased by sampling based on hunters' cooperation and funding available for each region. Limitations of the methods used for data collection suggest that the extent and prevalence of CWD in wildlife is underestimated. If the zoonotic potential of CWD is confirmed in the short term, as suggested by recent results obtained in experimental animal models, there will be limited accurate epidemiological data to inform public health. Research gaps in CWD prion ecology include the need to identify specific biological characteristics of potential CWD reservoir species that better explain susceptibility to spillover, landscape and climate configurations that are suitable for CWD transmission, and the magnitude of sampling bias in our current understanding of CWD distribution and risk. Addressing these research gaps will help anticipate novel areas and species where CWD spillover is expected, which will inform control strategies. From an ecological perspective, control strategies could include assessing restoration of natural predators of CWD reservoirs, ultrasensitive CWD detection in biotic and abiotic reservoirs, and deer density and landscape modification to reduce CWD spread and prevalence.

Keywords: CWD; Cervidae; Chronic Wasting Disease; prions; reservoirs; spread; wildlife; zoonotic.

Fig. 1.

Geographic distribution of Chronic Wasting Disease (CWD) reports. (A) The region with the most cases and areas infected with CWD is North America; (B) Europe has reported CWD in Norway, Sweden, and Finland; (C) Asia reported CWD in South Korea. Red: counties (in USA) and wildlife management areas (in Canada) with reports of CWD in wild cervids; dark grey: states/provinces reporting CWD in captive cervids; light grey: states with CWD detection in wild cervids; white: areas with no reports of CWD; (D) Timeline denoting the first detections of CWD in specified regions for each country. Data derived from CDC (2019) and CWD Alliance (2019).

Fig. 2.

Role for intermediate species and environmental reservoirs in the spread of Chronic Wasting Disease (CWD). Wild cervid populations serve as the reservoirs of CWD (Carlson et al., 2018), acting as source for spillover to other species and the environment. Natural spread: spread in natural areas associated with high CWD prevalence and dispersal observed in male white-tailed deer (Clements et al., 2011; Carlson et al., 2018). Unknown susceptible: species that have shown successful PrP^Sc infection under experimental settings, but for which no evidence is available under natural conditions; potentially susceptible predators (e.g. coyotes) and scavengers (e.g. crows and raccoons) exist that could act as vectors of the infectious prion (Bunk, 2004; Hamir et al., 2007; Fischer et al., 2013; Moore et al., 2019). Similarly, while fawns are known to be susceptible, little is known of their role in the shedding and spread of CWD. Known susceptible: species known to be susceptible to CWD infection, including mule deer, black-tailed deer, elk, white-tailed deer, red deer, moose, and reindeer (caribou) (Williams & Young, 1980; Spraker et al., 1997; Baeten et al., 2007; Benestad et al., 2016; Evira, 2018). Species susceptible in laboratory experiments include Reeve’s muntjac and fallow deer. Anthropogenic spread: spread of CWD facilitated by human intervention, including translocation of infected deer (e.g. deer farms, carcasses of infected deer). Environmental reservoirs: infected fluids or tissues (e.g. urine, saliva, faeces, blood) deposited in the environment (e.g. water, grass, soil, rocks) remaining infectious for months, years, or decades. Black arrows, observed in the wild or in laboratory conditions; red arrows, uncertain, requiring additional research.

Fig. 3.

Taxonomic breadth of Chronic Wasting Disease (CWD) infections in the Cervidae. Cladogram denotes cervid species found naturally susceptible (red), susceptible under experimental inoculation (blue), and of unknown susceptibility (black). Figure modified from Gilbert et al. (2006), based on species classification from the Integrated Taxonomic Information System (www.itis.gov) and sequences available from Genbank (https://www.ncbi.nlm.nih.gov/genbank/). Deer illustrations from Lydekker (1898).

Fig. 4.

Different dimensions and scales (micro to macro) to study Chronic Wasting Disease (CWD). Three dimensions could be used to study CWD: spatial, temporal, and organizational dimensions. The x axis denotes the spatial dimension (from millimetres to continents); the y axis denotes the temporal dimension (from seconds to centuries); the z axis denotes the organizational dimension (from molecules to biomes). Micro: (A) molecular-level studies focus on prion detection and characterization, e.g. in vitro measurements on prion conversion;(B) population-level studies explore transmission between individuals of a group, e.g. transmission experiments in captive deer; and (C) community-level studies explore potential CWD spillover among species, e.g. evaluating the role of other wild species in prion dissemination and maintenance. Medium: (D) landscape-level studies aim to identify biotic and abiotic factors associated with CWD maintenance and spread in endemic areas, e.g. assessing CWD distribution based on landscape configuration among seasons. Macro: (E) biogeographic-level studies aim to understand factors associated with CWD spread among large regions, periods, and communities, e.g. exploring climatic drivers of CWD occurrence at a continental level or long-distance spread from translocation of captive cervids. The different organizational levels can be studied across different geographic and temporal scales (e.g. from fine to coarse). Most CWD research has been restricted to studies at low organization level and fine temporal and spatial scales. Studies at the community, landscape, and biogeographic levels underlying CWD occurrence remain neglected and are critically needed.

Fig. 5.

Geomorphology and Chronic Wasting Disease (CWD). USA counties reported as CWD-positive in wildlife (black flags). Note the geomorphology of the country with areas of low (blue) and high elevation (white). The map suggests that CWD is broadly found in flat landscapes with plausible interruption or retardation of spread in the highlands of western (e.g. Utah, Idaho, western Colorado) and eastern regions (e.g. Appalachian Mountains).

Fig. 6.

Detection of Chronic Wasting Disease (CWD) in cervid tissues. Distribution of deer tissues used in CWD detection. (A) obex and brainstem (Haley et al., 2011); (B) cerebrospinal fluid (Haley et al., 2013); (C) spinal cord (Baeten et al., 2007); (D) fat (Race et al., 2009); (E) urine, kidneys, bladder (Haley & Hoover, 2015); (F) lymphoid tissue in the intestines including intestinal and rectoanal mucosa (Haley et al., 2011); (G) faeces (Tamgüney et al., 2009); (H) muscle (Angers et al., 2009); (I) spleen (Sigurdson et al., 2002); (J) peripheral nerves (Seelig et al., 2011); (K) blood (Mathiason et al., 2006); (L) medial retropharyngeal lymph nodes (Sigurdson et al., 2002); (M) tonsils (Sigurdson et al., 2002); (N) saliva (Mathiason et al., 2006); (O) nasal tissues (Haley et al., 2016); (P) antler velvet (Angers et al., 2009). Asterisks indicate whether sensitivity is >50% based on Haley & Richt (2017).