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A review of chronic wasting disease in North America with implications for Europe

DOI:10.1007/s10344-019-1260-z
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Atle Mysterud at University of Oslo
Atle Mysterud
David Edmunds at United States Geological Survey
David Edmunds
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Abstract

Cervids are keystone species in ecosystems and are associated with enormous cultural and economic value. Chronic wasting disease (CWD) is a fatal prion disease spreading in North American cervid populations. The 2016 emergence of CWD in Europe makes it urgent to understand the basics of CWD and to assess the extent to which current CWD knowledge is transferable to Europe. CWD is difficult to detect in the early stages due to very low prevalence and slow growth rates. The negative population effect of CWD is mainly due to increased female adult mortality, as infected individuals continue to reproduce. It may take decades before CWD leads to population declines. The population dynamics of mule deer are affected more by CWD than those of white-tailed deer, which in turn are more affected than those of elk, and depending on other factors limiting the populations. Species- and population-specific differences in dynamical consequences are linked to the balance among the rates of transmission, incubation period (linked to the prion protein gene, PRNP), and reproductive rates. This make it difficult to predict effects of CWD in Europe with other cervids, but the dynamic impact may be marked to cervid populations over the long term. The process of spillover across the species barrier is not well understood. Occasional spillover to moose without an apparent epizootic suggests specific conditions can limit CWD. Frequency-dependent transmission or weak density–dependent transmission makes it difficult to control CWD using density reductions through harvest and/or culling. CWD is difficult to eradicate once it becomes endemic, and it calls for immediate management actions. These actions involve extensive culling, fencing, and ceasing of wildlife feeding and are likely to cause significant controversy.
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REVIEW
A review of chronic wasting disease in North America
with implications for Europe
Atle Mysterud
1
&David R. Edmunds
2
Received: 29 January 2018 /Revised: 28 January 2019 /Accepted: 10 February 2019 /Published online: 21 February 2019
#Springer-Verlag GmbH Germany, part of Springer Nature 2019
Abstract
Cervids are keystone species in ecosystems and are associated with enormous cultural and economic value. Chronic wasting
disease (CWD) is a fatal prion disease spreading in North American cervid populations. The 2016 emergence of CWD in Europe
makes it urgent to understand the basics of CWD and to assess the extent to which current CWD knowledge is transferable to
Europe. CWD is difficult to detect in the early stages due to very low prevalence and slow growth rates. The negative population
effect of CWD is mainly due to increased female adult mortality, as infected individuals continue to reproduce. It may take
decades before CWD leads to population declines. The population dynamics of mule deer are affected more by CWD than those
of white-tailed deer, which in turn are more affected than those of elk, and depending on other factors limiting the populations.
Species- and population-specific differences in dynamical consequences are linked to the balance among the rates of transmis-
sion, incubation period (linked to the prion protein gene, PRNP), and reproductive rates. This make it difficult to predict effects of
CWD in Europe with other cervids, but the dynamic impact may be marked to cervid populations over the long term. The process
of spillover across the species barrier is not well understood. Occasional spillover to moose without an apparent epizootic
suggests specific conditions can limit CWD. Frequency-dependent transmission or weak density–dependent transmission makes
it difficult to control CWD using density reductions through harvest and/or culling. CWD is difficult to eradicate once it becomes
endemic, and it calls for immediate management actions. These actions involve extensive culling, fencing, and ceasing of wildlife
feeding and are likely to cause significant controversy.
Keywords Frequency-d ependent ver sus density -dependent transmissi on .Directand environmentaltransmissionroutes .Spatially
targeted harvesting .Extermination and fallowing .Salt licks and supplemental feeding .Genetics and pathology .Epizootiology
and population dynamics
Introduction
The first case of chronic wasting disease (CWD) in Europe
was diagnosed in March 2016 in a female reindeer (Rangifer
tarandus) in the Nordfjella mountains, Norway (Benestad
et al. 2016). Since then, several more CWD-infected reindeer
from the same population were detected by testing during the
2016 and 2017 hunting seasons (Viljugrein et al. 2019).
Hence, we have the first reported outbreak of CWD in
Europe. CWD was first documented in a captive mule deer
(Odocoileus hemionus) in 1967 in Colorado, USA (Williams
and Young 1980), and it appeared in wild mule deer in 1981
(Williams and Young 1992; Spraker et al. 1997;Milleretal.
2000). CWD in the wild has since spread to 25 states and,
through sales of farmed elk, has been introduced to two
Canadian provinces and to South Korea (Uehlinger et al.
2016); however, the origin of CWD in Norway remains un-
known (Benestad et al. 2016).
It is important to realize that although CWD was first iden-
tified among wild deer in 1981, it is still spreading to new
areas and continuing to increase in prevalence in most, if not
all, endemic areas. Evidence of declining populations in en-
demic areas is recently reported for white-tailed deer
(Odocoileus virginianus) (Edmunds et al. 2016) and mule deer
*Atle Mysterud
atle.mysterud@ibv.uio.no
1
Centre for Ecological and Evolutionary Synthesis (CEES),
Department of Biosciences, University of Oslo, P.O. Box 1066,
Blindern, NO-0316 Oslo, Norway
2
Natural Resource Ecology Laboratory, Colorado State University,
Fort Collins, CO 80523, USA
European Journal of Wildlife Research (2019) 65: 26
https://doi.org/10.1007/s10344-019-1260-z
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... T he contagious prion disease "chronic wasting disease" (CWD) infects mule deer (Odocoileus hemionus) and at least six other species of the deer (cervid) family [1][2][3] . Chronic wasting disease has been recognized for only a few decades, yet has become widely regarded as one of the most worrisome diseases affecting wildlife in the Northern Hemisphere [2][3][4] . Unchecked epidemics raise ecological, socioeconomic, and public health concerns [2][3][4] . ...
... Chronic wasting disease has been recognized for only a few decades, yet has become widely regarded as one of the most worrisome diseases affecting wildlife in the Northern Hemisphere [2][3][4] . Unchecked epidemics raise ecological, socioeconomic, and public health concerns [2][3][4] . Prion infection shortens the host's lifespan, applying novel selective pressure and affecting herd dynamics when prevalence (proportion of adults infected) becomes sufficiently high [5][6][7][8][9] . ...
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The contagious prion disease “chronic wasting disease” (CWD) infects mule deer ( Odocoileus hemionus ) and related species. Unchecked epidemics raise ecological, socioeconomic, and public health concerns. Prion infection shortens a deer’s lifespan, and when prevalence (proportion of adults infected) becomes sufficiently high CWD can affect herd dynamics. Understanding population responses over time is key to forecasting long-term impacts. Here we describe unexpected stability in prevalence and abundance in a mule deer herd where CWD has been left unmanaged. High apparent prevalence (~30%) since at least 2005 likely drove observed changes in the proportion and age distribution of wild-type native prion protein ( PRNP ) gene homozygotes among deer sampled. Predation by mountain lions ( Puma concolor ) may be helping keep CWD in check. Despite stable appearances, prion disease nonetheless impairs adult survival and likely resilience in this deer herd, limiting its potential for growth despite refuge from hunter harvest and favorable habitat and winter conditions.
View
... Chronic wasting disease (CWD), a fatal prion disease, has been associated with population declines in mule deer and elk (DeVivo et al., 2017;Edmunds et al., 2016;Monello et al., 2014), threatening cervid populations in western North America (Mysterud & Edmunds, 2019). As a chronic infection, young to prime-aged adults are most likely to test positive (Miller & Conner, 2005;Monello et al., 2014). ...
... Many authors have proposed predation as a potential biological control mechanism to reduce CWD prevalence in cervid populations and disease in general (DeVivo et al., 2017;Krumm et al., 2010;Miller et al., 2008;Monello et al., 2014;Mysterud & Edmunds, 2019). We developed a host-predator model that includes host age structure and age-specific disease and predation patterns to examine predator cleansing effects. ...
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1. Predators may create healthier prey populations by selectively removing diseased individuals. Predators typically prefer some ages of prey over others, which may, or may not, align with those prey ages that are most likely to be diseased. 2. The interaction of age-specific infection and predation has not been previously explored and likely has sizable effects on disease dynamics. We hypothesize that predator cleansing effects will be greater when the disease and predation occur in the same prey age groups. 3. We examine the predator cleansing effect using a model where both vulnerability to predators and pathogen prevalence vary with age. We tailor this model to chronic wasting disease (CWD) in mule deer and elk populations in the Greater Yellowstone Ecosystem, with empirical data from Yellowstone gray wolves and cougars. 4. Model results suggest that under moderate, yet realistic, predation pressure from cougars and wolves independently, predators may decrease CWD outbreak size substantially and delay the accumulation of symptomatic deer and elk. The magnitude of this effect is driven by the ability of predators to selectively remove late-stage CWD infections that are likely the most responsible for transmission, but this may not be the age class they typically select. Thus, predators that select for infected young adults over uninfected juveniles have a stronger cleansing effect, and these effects are strengthened when transmission rates increase with increasing prey morbidity. There are also trade-offs from a management perspective - i.e., increasing predator kill rates can result in opposing forces on prey abundance and CWD prevalence. 5. Our modeling exploration shows that predators have the potential to reduce prevalence in prey populations when prey age and disease severity are considered, yet the strength of this effect is influenced by predators' selection for demography or body condition. Current CWD management focuses on increasing cervid hunting as the primary management tool, and our results suggest predators may also be a useful tool under certain conditions, but not necessarily without additional impacts on host abundance and demography. Protected areas with predator populations will play a large role in informing the debate over predator impacts on disease.
View
... CWD is caused by the misfolding of prion protein (PrP CWD ) and the subsequent recruitment of native prion protein (PrP C ) into pathological amyloid fibrils, thus causing a contagious and unconditionally fatal disease [10,11]. The disease was first described in captive mule deer in Colorado in 1967 and has since been identified across the United States, Canada, Scandinavia, and South Korea [12][13][14]. Because of the severity and continued spread of the disease, diagnostic methods must evolve to meet the growing need for fast and accurate testing. ...
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View
... Understanding how hunters have and will respond to CWD management policies is particularly crucial to agencies because of the vital role hunters play in deer management. Hunters often directly assist in CWD management efforts such as general herd depopulation, spatially targeted harvesting in CWD-affected areas, and age and/or sex-specific targeted harvesting [6,7]. ...
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View
... There is uncertainty about how strongly CWD will affect the population dynamics in the Norwegian populations of cervids. The impact of CWD on the populations will rely on the relative balance between the basic reproduction ratio of the infection (also called basic reproduction number, R0), how long the course of infection lasts (among other factors related to variation in the PRNP-gene), the rate of reproduction and other mortality in the population(s) (Mysterud and Edmunds, 2019). White-tailed deer and roe deer are regarded as having a very high reproduction potential, mule deer and moose an intermediary and reindeer and red deer a low reproduction potential. ...
Mitigations options after detection of Chronic Wasting Disease in the Hardangervidda Wild Reindeer Area - a basis for future management strategies. Scientific Opinion from the Norwegian Scientific Committee for Food and Environment.
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View
... Disease can reduce animal populations substantially when it spreads unchecked, reaching epidemic proportions that can spread to adjacent populations or related species, including domesticated animals (Mysterud & Edmunds, 2019). Disease impairs physiological functioning and can render hosts more susceptible F I G U R E 1 Schematic contrast of the human environment and its influence on the nature of predator-prey systems. ...
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View
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Chronic wasting disease (CWD) is a fatal neurodegenerative disease of deer, elk, moose, and reindeer (cervids) caused by misfolded prion proteins. The disease has been reported across North America and recently discovered in northern Europe. Transmission of CWD in wild cervid populations can occur through environmental routes, but limited ability to detect prions in environmental samples has prevented the identification of potential transmission “hot spots”. We establish widespread CWD prion contamination of mineral licks used by free-ranging cervids in an enzootic area in Wisconsin, USA. We show mineral licks can serve as reservoirs of CWD prions and thus facilitate disease transmission. Furthermore, mineral licks attract livestock and other wildlife that also obtain mineral nutrients via soil and water consumption. Exposure to CWD prions at mineral licks provides potential for cross-species transmission to wildlife, domestic animals, and humans. Managing deer use of mineral licks warrants further consideration to help control outbreaks of CWD.
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Pathologic and biochemical characterization of PrPSc from elk with PRNP polymorphisms at codon 132 after experimental infection with the chronic wasting disease agent
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Scientific opinion on chronic wasting disease (II)
Article
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  • Jan 2018
Abstract The European Commission asked EFSA for a scientific opinion on chronic wasting disease in two parts. Part one, on surveillance, animal health risk‐based measures and public health risks, was published in January 2017. This opinion (part two) addresses the remaining Terms of Reference, namely, ‘are the conclusions and recommendations in the EFSA opinion of June 2004 on diagnostic methods for chronic wasting disease still valid? If not, an update should be provided’, and ‘update the conclusions of the 2010 EFSA opinion on the results of the European Union survey on chronic wasting disease in cervids, as regards its occurrence in the cervid population in the European Union’. Data on the performance of authorised rapid tests in North America are not comprehensive, and are more limited than those available for the tests approved for statutory transmissible spongiform encephalopathies surveillance applications in cattle and sheep. There are no data directly comparing available rapid test performances in cervids. The experience in Norway shows that the Bio‐Rad TeSeE™ SAP test, immunohistochemistry and western blotting have detected reindeer, moose and red deer cases. It was shown that testing both brainstem and lymphoid tissue from each animal increases the surveillance sensitivity. Shortcomings in the previous EU survey limited the reliability of inferences that could be made about the potential disease occurrence in Europe. Subsequently, testing activity in Europe was low, until the detection of the disease in Norway, triggering substantial testing efforts in that country. Available data neither support nor refute the conclusion that chronic wasting disease does not occur widely in the EU and do not preclude the possibility that the disease was present in Europe before the survey was conducted. It appears plausible that chronic wasting disease could have become established in Norway more than a decade ago.
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This article examined relationships between proximity to chronic wasting disease (CWD) and perceived risk and trust. The sample included 1,606 hunters in one of 10 northern Illinois counties with CWD, 1,958 hunters in a non-CWD county adjacent to these counties with CWD, and 2,099 hunters from the remaining non-CWD counties in Illinois. Compared to hunters in non-CWD counties, those in CWD counties were hypothesized to: (a) perceive more risk of CWD to humans, (b) perceive more risk of CWD to deer, (c) report less trust in the Illinois Department of Natural Resources (IDNR) CWD information, and (d) have less trust in the IDNR management of CWD. The first two hypotheses were not supported, as hunters in CWD counties perceived less risk to humans and deer than did respondents in non-CWD counties. Hunters in CWD counties, however, were less trusting of the IDNR information and management compared to the other hunters.
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Contact Tracing for the Control of Infectious Disease Epidemics: Chronic Wasting Disease in Deer Farms
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Contact tracing is a crucial component of the control of many infectious diseases, but is an arduous and time consuming process. Procedures that increase the efficiency of contact tracing increase the chance that effective controls can be implemented sooner and thus reduce the magnitude of the epidemic. We illustrate a procedure using Graph Theory in the context of infectious disease epidemics of farmed animals in which the epidemics are driven mainly by the shipment of animals between farms. Specifically, we created a directed graph of the recorded shipments of deer between deer farms in Pennsylvania over a timeframe and asked how the properties of the graph could be exploited to make contact tracing more efficient should Chronic Wasting Disease (a prion disease of deer) be discovered in one of the farms. We show that the presence of a large strongly connected component in the graph has a significant impact on the number of contacts that can arise.
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Fencing for wildlife disease control
Article
  • Nov 2018
1.Fencing is a contentious issue due to its impact on conservation. The Danish government aim to establish a 70 km fence towards the border of Germany and the agricultural ministry of Bulgaria erected 133 km fences along border with Romania to prevent spread of African swine fever by wild boar. The Norwegian government recently erected 24 km of fencing as part of combating chronic wasting disease among reindeer. Europe therefore faces a new situation: fencing to limit emerging wildlife diseases. There is, however, surprisingly little scientific literature available on the efficacy of fencing for controlling wildlife disease. 2.Fencing to combat disease include (1) ‘perimeter fencing’ aiming for containment and reducing likelihood of geographic spread, and (2) ‘hot spot fencing’ aiming to lower transmission rates within endemic disease areas. Critical limitations of perimeter fencing include: numerous practical and construction details, differences in animal behavior relative to fences, animal contact along fences, placement relative to natural barriers, human infrastructure that disrupt continuous fencing, and mode of disease transmission including human aided disease spread. 3.Hot spot fencing is a potentially important way of reducing transmission of diseases once endemic but materials and construction of fences need to be well thought through. A single fence breach does not have the same consequences as for perimeter fencing. 4.Synthesis and applications. Fencing as a tactic to mitigate disease appears appealing to politicians, but implementation uncertainty is considerable. We fear efforts may be futile unless more attention is paid to both practical and biological detail, and it seems urgent to build a more evidence based approach using experience from other sectors. This article is protected by copyright. All rights reserved.
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A method that accounts for differential detectability in mixed samples of long-term infections with applications to the case of Chronic Wasting Disease in cervids
Article
Surveillance of wildlife diseases is logistically difficult, and imperfect detection is a recurrent challenge for disease estimation. Using citizen science can increase sample sizes, but it is associated with a cost in terms of the anatomical type and quality of the sample. Additionally, biological tissue samples from remote areas lose quality due to autolysis. These challenges are faced in the case of emerging chronic wasting disease (CWD) in cervids. Here, we develop a stochastic scenario tree model of diagnostic sensitivity, allowing for a mixture of tissue sample types (lymph nodes and brain) and qualities while accounting for different detection probabilities during the CWD infection, lasting 2–3 years. We apply the diagnostic sensitivity in a Bayesian framework, enabling estimation of age-class-specific true prevalence, including the prevalence in latent, recently infected stages. We provide a simulation framework to estimate the sensitivity of the surveillance system (i.e., the probability of detecting the infection in a given population), when detectability varies among individuals due to different disease progression. We demonstrate the utility of our framework by applying it to the recent emergence of CWD in a European population of reindeer. We estimated apparent CWD prevalence at 1.2% of adults in the infected population of wild reindeer, while the true prevalence was 1.6%. The sensitivity estimation of the CWD surveillance was performed in an adjacent small (c. 500) and a large (c. 10,000) reindeer population, demonstrating low certainty of CWD absence. Our method has immediate application to the mandatory testing for CWD in EU countries commencing in 2018. Similar approaches that account for latent stages and a serial disease progression in various tissues with a temporal pattern of diagnostic sensitivity may enhance the estimation of the prevalence of wildlife diseases more generally. © 2018 The Authors. Methods in Ecology and Evolution
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A reindeer cull to prevent chronic wasting disease in Europe
Article
The emergence of chronic wasting disease among wild reindeer in Norway triggered the decision to eradicate an entire population of more than 2,000 animals. The cull, now complete, was a tremendously difficult process both politically and practically.
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