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4 January 2022 MOUNTAIN LIONS (PUMA CONCOLOR) RESIST LONG-TERM DIETARY EXPOSURE TO CHRONIC WASTING DISEASE
Lisa L. Wolfe, Karen A. Fox, Karen A. Griffin, Michael W. Miller
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Abstract

For nearly 18 yr, we evaluated susceptibility of captive mountain lions (Puma concolor) to chronic wasting disease (CWD) in the face of repeated exposure associated with consuming infected cervid carcasses. Three mountain lions with a monomorphic prion protein gene (PRNP) sequence identical to that described previously for the species had access to parts of ≥432 infected carcasses during ≥2,013 feeding occasions, conservatively representing >14,000 kg of infected feed material, during May 2002 to March 2020. The proportion of diet in infected carcass material averaged 43% overall but differed from year to year (minimally 11–74%). Most infected carcasses were mule deer (Odocoileus hemionus; ∼75%). We observed no clinical signs suggestive of progressive encephalopathy or other neurologic disease over the ∼14.5–17.9 yr between first known exposure and eventual death. Histopathology revealed no spongiform changes or immunostaining suggestive of prion infection in multiple sections of nervous and lymphoid tissue. Similarly, none of 133 free-ranging mountain lion carcasses sampled opportunistically during 2004–20 showed immunostaining consistent with prion infection in sections of brainstem or lymph node. These findings align with prior work suggesting that CWD-associated prions face strong barriers to natural transmission among species outside the family Cervidae.

INTRODUCTION

Chronic wasting disease (CWD; Williams and Young 1980)—an infectious prion disease—naturally infects deer (Odocoileus spp.), wapiti (Cervus canadensis), and several closely related species in the family Cervidae. Over the past five or more decades, this disease has become established in free-ranging cervid populations in foci scattered across North America (US Geological Survey 2020). Unchecked CWD epidemics have the potential to destabilize affected cervid herds (Edmunds et al. 2016; DeVivo et al. 2017), thereby raising concerns for managing and conserving affected species as well as questions about broader ecological, socioeconomic, and perhaps health implications (Miller and Fischer 2016; Mysterud and Edmunds 2019).

Although the natural host range of CWD appears to be limited to cervids, several predatory species (including humans) may be exposed to prions by consuming infected carcasses (Stewart et al. 2012; Hannaoui et al. 2017). Mountain lions (Puma concolor) are the main nonhuman predator of mule deer (Odocoileus hemionus) in the foothills of northcentral Colorado and southeastern Wyoming where CWD has been present in the wild since at least the 1970s (Williams and Young 1992; Miller et al. 2000). Infected deer are relatively vulnerable to predation (Miller et al. 2008; Krumm et al. 2010; DeVivo et al. 2017); consequently, mountain lions probably have some degree of CWD exposure in areas where their ranges overlap endemic foci.

Here, we describe the results of a long-term study (nearly 18 yr) to evaluate natural susceptibility of captive mountain lions to CWD under conditions of prolonged, repeated exposure by consumption of infected deer and wapiti carcasses. Spongiform encephalopathy is not known in free-ranging mountain lions. However, we regarded experimental assessment of exposure and susceptibility important in clarifying the role that mountain lions might play in helping suppress CWD in cervid populations and, conversely, the potential ecological ramifications of susceptibility in an apex predator. When we conceived this study in 2001, the susceptibility of mountain lions (Willoughby et al. 1992), other wild felids (Kirkwood and Cunningham 1999, 2007), domestic cats (Felis catus; Hewicker-Trautwein and Bradley 2007), and humans (Will et al. 1996; Bruce et al. 1997) to bovine spongiform encephalopathy (BSE) prions underscored a broader potential value in understanding mountain lion susceptibility to CWD.

MATERIALS AND METHODS

Three orphaned, 4–6-wk-old mountain lions originating from near Chugwater, Wyoming, were acquired opportunistically from the Wyoming Game and Fish Department in October 2001. The native prion protein (PRNP) gene sequence for each subject animal was determined from extracts of genomic DNA by primers and methods described by Stewart et al. (2012;  Supplementary Material (40_jwdi-58-01-14_s03.pdf)).

The three siblings (one female, two males) resided together at the Foothills Wildlife Research Facility of the Colorado Division of Parks and Wildlife (Table 1). We held them in a fully enclosed ∼224-m2 pen for the first year, then in a larger, dividable ∼275-m2 covered outdoor pen connected to a building with three ∼8-m2 indoor cages that could be opened or closed to comingle or separate individuals. All three animals generally had access to the entire outdoor and indoor housing complex.

Table 1

Individual dietary exposure and ultimate cause of demise for captive mountain lions (Puma concolor) receiving carcasses and meat from native cervids infected with chronic wasting disease, as summarized from available feeding records and assuming all three animals partook in each feeding opportunity. Longevity estimates based on an assumed birth date. See text and  Supplementary Material (40_jwdi-58-01-14_s03.pdf) for additional information.

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The two males were castrated and the female was spayed at about 5 mo of age to facilitate long-term tractability and to minimize potential for conspecific aggression. Routine veterinary care included regular use of vaccines against rabies (Imrab, Merial Inc., Duluth, Georgia, USA), feline leukemia (multiple products used), and a combination of feline panleukopenia, feline herpes, and feline calicivirus (multiple products used), as well as the anthelmintic praziquantel every 6–12 mo (Droncit Cestode Tabs, BayerDVM, Shawnee Mission, Kansas, USA).

Throughout their lives, all three mountain lions received a diet primarily composed of deer (Odocoileus spp., mainly mule deer) and wapiti carcasses or carcass parts, infrequently supplemented with moose (Alces alces), bighorn sheep (Ovis canadensis), or pronghorn antelope (Antilocapra americana). All three also probably caught and consumed small mammals and birds that on rare occasion strayed into their enclosure. Carcasses were prepared to retain the nervous system, lymphoid, and muscle tissues, and other organ tissues if available. Carcasses were whole, cut in half, or quartered. Initially the entire gastrointestinal tract was offered, but because gut tissue or offal generally were not consumed, we switched to offering mainly eviscerated carcasses with the heart, liver, and kidneys intact. We offered carcasses or parts daily when the study animals were young and growing, then every 3 or 4 d as they matured, to simulate natural feeding patterns, facilitate training, and combat obesity (Fig. 1).

Figure1

Temporal distribution of dietary exposure of three captive mountain lions (Puma concolor) to carcass materials from native cervids infected with chronic wasting disease (CWD). Bar segments show the cumulative number of CWD-positive (solid) and negative (open) feeding opportunities within successive 12-mo periods, as summarized from available feeding records and observed behavior assuming all three animals partook in each feeding opportunity. Study years defined as May–April (e.g., year 1 May 2002–April 2003). Asterisk (*) indicates study years that had ≥1 mo of missing feed records (late June to early August 2004; early March 2014 to late July 2015).

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Plans for this investigation were approved by the Colorado Division of Parks and Wildlife animal care and use committee (file 04-2002) in April 2002. The cubs first fed on a confirmed positive mule deer carcass on 3 May 2002. We assessed repeated exposure that would mimic patterns expected through a lifetime of natural foraging in a CWD-endemic area, with a goal that about 20% of the collective annual diet included CWD-positive tissues. Note that the highest observed prevalence in a free-ranging mule deer herd in Colorado in 2002 was about 15% among hunter-harvested adult males (Miller et al. 2000). We obtained deer and wapiti carcasses opportunistically from captive and free-ranging sources in conjunction with ongoing research, surveillance, and management programs, as well as meat donated by hunters who harvested test-positive deer and wapiti. Infected cervids represented all disease stages from early preclinical to end-stage clinical CWD. The distribution of positive or negative meat among feedings was irregular within and across years (Fig. 1) because most carcasses were fed to the lions before laboratory results were available.

All carcasses were tested by immunohistochemistry (IHC; Spraker et al. 2002a, b) or enzyme-linked immunosorbent assay (Hibler et al. 2003) of brain, lymphoid tissues, or both, primarily by the Colorado State University Veterinary Diagnostic Laboratory (Fort Collins, Colorado, USA). Group housing precluded determining individual consumption. Positive donated meat consumed during training and adjunct working activities (∼0.5–5 kg/animal per session) augmented exposure. We estimated CWD exposure retrospectively and provide minimum estimates because we did not track the meat fed during training, and some records were missing or incomplete.

On the basis of our experience observing early signs of prion disease in cervids (Miller et al. 1998) and accounts of spongiform encephalopathy in nondomestic felids, including mountain lions (Willoughby et al. 1992; Kirkwood and Cunningham 1994, 1999), we recognized the clinical value of tractable and readily observed subject animals. Conventional veterinary neurologic examinations assess mentation, posture and gait, cranial nerve function, and postural reactions that may reveal deficits in coordination and strength. However, many of the necessary manipulations (e.g., “hopping,” “wheel barrowing,” “hemiwalking”) to assess postural reactions are neither feasible nor advisable in captive mountain lions and other nondomestic animals. Consequently, we regularly conducted clinical assessments of subject animals to provide a sensitive indicator of infection, which is important from a scientific as well as an ethical standpoint. To facilitate these behavioral and other neurologic assessments, we trained all three mountain lions by positive reward-based operant conditioning (Skinner 1938; Pryor 1999; Westlund 2014; see  Supplementary Materials (40_jwdi-58-01-14_s03.pdf) for details). We selected trained behaviors that served as proxies for the elements of a conventional neurologic examination, essentially capturing and reinforcing natural behaviors as on-demand assessment tools by marking and rewarding them in the course of training and other interactions ( Supplementary Material Table S1 (40_jwdi-58-01-14_s03.pdf)).

A veterinary pathologist (K.A.F.) examined each animal postmortem within 1–16 h of death and collected representative tissue samples ( Supplementary Material (40_jwdi-58-01-14_s03.pdf)). Distribution of spongiform lesions and disease-associated prion protein (PrPd) accumulation in mule deer (Sigurdson et al. 1999, 2001; Fox et al. 2006) and felids (Ryder et al. 2001; Seelig et al. 2015) guided sampling and microscopic examinations ( Supplementary Material (40_jwdi-58-01-14_s03.pdf)). Subsamples were stored in 10% neutral buffered formalin, with paired samples frozen at –20 C. Fixed tissues were embedded in paraffin and sectioned at 5–6 µm, and multiple sections were examined by light microscopy after H&E staining ( Supplementary Material (40_jwdi-58-01-14_s03.pdf)). We referenced established criteria (e.g., Fraser and Dickinson 1968; Wells and Wells 1989; Wyatt et al. 1991; Willoughby et al. 1992; Williams and Young 1993; Wohlsein et al. 2012) in interpreting spongiform changes consistent with prion disease.

Multiple sections of brain, spinal cord, and tonsil; multiple lymph nodes; and other tissues were examined after IHC staining ( Supplementary Material (40_jwdi-58-01-14_s03.pdf)) for evidence of PrPd accumulation, as per the Colorado State University Veterinary Diagnostic Laboratory protocol optimized for detecting PrPd in cervids (Spraker et al. 2002a) with monoclonal antibody (mAb) F99/97.6.1 (O'Rourke et al. 2000). Additionally, we examined a subset of tissue sections by a second IHC protocol (Seelig et al. 2015) optimized for detecting PrPd in cats experimentally infected with CWD (Mathiason et al. 2013). This subset included caudal brainstem (dorsal motor nucleus of the vagus nerve and solitary tract nucleus) and sites consistently reported as showing PrPd accumulations in prion-infected felids and cervids (Spraker et al. 2002b; Hilbe et al. 2009; Seelig et al. 2015). The Seelig et al. (2015) optimized protocol with mAb L42 (Vorberg et al. 1999) was run by CSU's Prion Research Center (Fort Collins, Colorado, USA); caudal brainstem sections from experimentally infected and uninfected cats (Mathiason et al. 2013) were used as IHC controls. We referenced multiple publications in establishing criteria for interpreting IHC staining patterns, including work by Bell et al. (1997), Ryder et al. (2001), Gill et al. (2013, 2020), Seelig et al. (2015), and Williams et al. (2018). See  Supplementary Material (40_jwdi-58-01-14_s03.pdf) for further details and additional references.

To complement experimental findings, we summarized IHC results for brainstem (medulla oblongata sectioned at the obex) and retropharyngeal lymph node tissues collected opportunistically from 133 free-ranging mountain lion carcasses originating from various locations in Colorado and screened for evidence of prion infection during 2004–20 according to the Colorado State University Veterinary Diagnostic Laboratory protocol.

RESULTS

Weekly neurologic assessments by operant conditioning revealed no clinical signs suggestive of progressive encephalopathy or other neurologic disease in the mountain lions. All three study animals maintained their unique individual personality and behavioral traits throughout their respective lifetimes and showed continued tractability and willingness to train and work (Fig. 2). Because of chronic osteoarthritis, we euthanatized one male at ∼15.2 yr and the female at ∼18.5 yr (5,290 and 6,531 d) after first known exposure; the other male unexpectedly died (metastatic cholangiocarcinoma) at ∼18.5 yr (6,528 d) after first known exposure (Table 1 and  Supplementary Material (40_jwdi-58-01-14_s03.pdf)).

Figure2

Antemortem and postmortem evaluations revealed no evidence of prion infection in three captive mountain lions (Puma concolor) consuming chronic wasting disease–infected carcasses for ≥14.5 yr. (A) Neurologic assessments by operant conditioning ( Supplementary Material Table S1 (40_jwdi-58-01-14_s03.pdf)) revealed no clinical signs suggestive of progressive encephalopathy or other neurologic disease. (See

of representative assessments.) (B) Intense immunohistochemistry (IHC) stain in cecal contents but not in gut-associated lymphoid tissue. Bar=200 µm; IHC with monoclonal antibody (mAb) F99/97.6.1 (slide 12, report WHL 16 949 in Supplementary Material). (C–E) A few areas of mild vacuolation (C) were observed (pictured: external cuneate nucleus of the brainstem; H&E stain), but no immunostained PrPd accumulations after IHC staining with either mAb F99/97.6.1 (D) or L42 (E). Bar=50 µm in panels C–E, all from the same section of external cuneate nucleus (slide 7, WHL 16 949).

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All three of the captive mountain lions matched the monomorphic PRNP sequence for this species reported by Stewart et al. (2012). Thus, despite being related and limited in number, we regarded these subject animals as broadly representative of mountain lions as a species with respect to their PRNP sequences.

Histopathology results indicated an absence of spongiform changes (neuronal vacuolation or neuropil spongiosis) typical of the central nervous system lesions seen in prion diseases (Fig. 2). Moreover, no immunostaining suggestive of prion infection was observed under either IHC protocol (Fig. 2). The full reports are included as Supplementary Material. In a few instances nonspecific staining was noted, including staining of atypical structures (e.g., staining of parasitic sarcocysts with mAb F99/ 97.6.1; inconsistent staining of vessel walls with mAb L42), as well as background staining (e.g., diffuse, wispy, or globular deposits of stain not specific in color or shape for PrPd deposits). None of the 133 free-ranging mountain lions, including at least 86 adults (≥2 yr old) and 31 subadults (1–2 yr old), showed immunostaining consistent with prion infection.

On the basis of 2,013 feeding records, we estimated that all three mountain lions had access to parts of at least 432 infected carcasses (Table 1); more than 500 CWD-positive cervids were offered to the two longer lived animals. The majority of infected carcasses (n=492) were mule deer (∼75%), with wapiti (∼18%) and white-tailed deer (Odocoileus virginianus; ∼7%) comprising the balance. Conservatively this represented >14,000 kg of infected carcass material offered, although only a portion was consumed. The proportion of infected carcass material averaged 43% over all 18 yr, but differed considerably from year to year (11–74%; Fig. 1). Exposure was underestimated—especially in years 11–18—because the supplemental positive meat fed in the course of training was not included in the annual total.

DISCUSSION

Our findings align with a prior assessment (Stewart et al. 2012) suggesting that mountain lions appear relatively unlikely to acquire CWD through natural dietary exposure. Despite hundreds of opportunities for prion exposure that simulated predation on infected cervids, and nearly two decades for potential incubation, neither clinical nor postmortem assessments indicated the mountain lions under study contracted prion disease. The amount of infected carcass material was designed to exceed exposure of mountain lions preying in endemic mule deer ranges in Colorado or Wyoming circa 2002 (Miller et al. 2000). Experimental exposure began at a relatively early age. Over the first decade, on average more than half of the carcasses fed were infected (mainly adult cervids including at least 200 carcasses in later stages of clinical CWD). By comparison, although prey killed by mountain lions studied along Colorado's northern Front Range included a high proportion of mule deer (∼64%; Blecha and Alldredge 2017), deer in the adult age classes most likely to be infected with CWD accounted for only ∼30% of the prey taken.

Because the animals under study were confined and fed regularly, their consumption of carcass material seemed less catholic than in free-ranging counterparts. Nonetheless, carcass offerings and feeding patterns approximated those associated with presumptive BSE cases in mountain lions and other felids in zoos (Willoughby et al. 1992; Kirkwood and Cunningham 1994, 2007).

Our study maximized the potential for dietary exposure in the captive mountain lions. Skeletal muscle tissues from CWD-infected mule deer harbor infectious prions (Angers et al. 2006), and PrPd occurs widely in lymph nodes and other organs (Sigurdson et al. 2001; Fox et al. 2006). Repeated exposure increases the probability of infection from low prion doses (Diringer et al. 1994, 1998) and probably drives transmission among natural host species (Miller et al. 2004; Tamgüney et al. 2009). Moreover, infectivity in lymphatic tissues can be high: Wolfe et al. (2012) precipitated rapid onset of clinical CWD in 17 mule deer exposed by oral inoculation with only ∼0.1 g of tonsil tissue.

Limited screening of free-ranging mountain lions from CWD enzootic areas revealed no evidence of prion infection, reinforcing our experimental findings. Mountain lions have become increasingly abundant in Colorado since the mid-1960s (Apker and Vieira 2017), even as CWD emerged throughout much of the state. Although the indirect effects of CWD on mountain lion abundance by the effects on abundance or vulnerability of their main prey remain a possibility, human intolerance presents a more proximate limit on mountain lion abundance and survival throughout most of their ranges overlapping CWD occurrence (Apker 2017; Apker and Vieira 2017). On the basis of field estimates of annual survival (Moss et al. 2016), our study animals lived well beyond the life expectancy of free-ranging mountain lions in northcentral Colorado (∼1.8–9.5 yr depending on sex and habitat). The advanced ages of our study animals also exceeded the reported lifespans of BSE-infected captive wild felids (Kirkwood and Cunningham 1999, 2007). Three mountain lions that contracted BSE in UK zoos developed clinical disease at ∼5–12 yr of age, although true ages and timing of exposure were uncertain for the two longer lived individuals (Kirkwood and Cunningham 1999).

Our investment in training and regular working interactions with the three exposed animals facilitated a sustained clinical assessment that was highly sensitive to detecting early signs consistent with prion disease (Miller et al. 1998). Ataxia, sometimes accompanied by tremors, was seen most often in mountain lions and other felids affected by BSE (Kirkwood and Cunningham 2007). Early signs, including apparent lameness and behavioral changes, were more variable and subtle and thus difficult to discern in fractious individuals. The index feline spongiform encephalopathy–affected mountain lion presented with ataxia, hypermetria, and falling accompanied by “unusual” behaviors reported by keepers (Willoughby et al. 1992). Behavioral changes (especially aggression or timidity), tactile and auditory hyperesthesia, polyphagia, and altered grooming habits have been noted more frequently than locomotor dysfunction among BSE cases in domestic cats (Leggett et al. 1990; Wyatt et al. 1990, 1991; Hewicker-Trautwein and Bradley 2007). Similarly, subtle clinical signs, including stilted gait, weight loss, anorexia, polydipsia, patterned motor behaviors, head and tail tremors, and ataxia, occurred in cats infected with CWD after intracerebral injection (Mathiason et al. 2013). Despite the use of a clinical approach designed to detect even subtle signs of encephalopathy, none of the three animals we studied showed altered personality or behavior or any of the more striking neurologic signs described in transmissible spongiform encephalopathy–affected felids. Beyond the immediate health monitoring and tangible animal welfare benefits (Westlund 2014), the extent of their training and willingness to work also allowed all three animals to be further trained and used in complementary studies over time, such as testing collars, trap designs, biomarkers, noninvasive sampling methods, and even metabolic physiology measures (Williams et al. 2014; see

).

Domestic cats orally challenged with brain tissue from a CWD-infected mule deer also failed to contract prion disease over a 1.5–7-yr (19–85-mo) observation period (Mathiason et al. 2013) despite some susceptibility to intracerebral challenge. Regardless of the practical value in predicting the outcome of exposure to prions by natural routes, the lesion profiles described in cats successfully infected with intracerebral exposure on first passage provided reference data for the postmortem screening undertaken here. A comparative summary by Seelig et al. (2015; see their table 4) of PrPd distribution in CWD- and BSE-infected cats provided a framework for assuring that the examinations of central nervous system tissues from experimental and free-ranging mountain lions were sufficient to detect evidence of prion disease if present.

Nonspecific IHC staining observed in CWD-exposed mountain lions resembled descriptions of BSE in cats and humans (Bell et al. 1997; Hilbe et al. 2009; Gill et al. 2013, 2020). Some areas of mild vacuolation were noted in one male, but in the absence of clinical signs and immunostained PrPd accumulations in central nervous system sections, they were attributed to autolysis (longest postmortem interval), age, or euthanasia (Wells and Wells 1989; Gould et al. 2003; Wohlsein et al. 2012; Williams et al. 2018). Similar incidental lesions have been seen in aged cattle exposed to CWD (Gould et al. 2003; Williams et al. 2018). None of the mountain lion lymphoid tissues had PrPd accumulations. Lymphoid involvement is prominent in CWD cases among cervids (Williams 2005; Fox et al. 2006) and in humans infected with the BSE agent (Ironside et al. 2000). However, BSE-infected felids show inconsistent PrPd accumulation in lymphoid tissues (Ryder et al. 2001; Hilbe et al. 2009; Eiden et al. 2010), and lymphoid PrPd was not reported among CWD-infected cats.

An extensive genetic assessment of potential susceptibility to prion diseases in carnivore species revealed that mountain lion samples (n=100, all from Colorado) lacked PRNP gene sequence variation (Stewart et al. 2012), showing a monomorphic sequence also shared by our three subject animals. Moreover, mountain lions and feline spongiform encephalopathy–infected cheetah (Acinonyx jubatus) share a common PrP amino acid sequence (Stewart et al. 2012). Both species suffered disproportionately high numbers of BSE cases in zoo collections (Kirkwood and Cunningham 1994, 1999). Wild type mountain lions appear less susceptible to CWD-associated prions currently in Colorado than to BSE-associated prions, perhaps a further reflection of the strain differences between BSE and North American CWD prions (Bruce et al. 1997; Barria et al. 2014). Collectively, the findings described here and in similar long-term studies with various species (e.g., Rhyan et al. 2011; Williams et al. 2018; Fox et al. 2021) help to define the limits of the natural host range of CWD and identify apparent barriers to interspecies transmission.

ACKNOWLEDGMENTS

A prospective study spanning nearly 18 yr requires support and assistance from sources too numerous to track or to thank individually. We especially appreciate the extensive work done by T. Davis, K. Kearl, and I. LeVan in training and caretaking. A. Nalls kindly ran felid-optimized IHC on tissues from our study subjects, and C. Mathiason and E. Hoover graciously allowed access to that laboratory assistance and to reference control tissues from CWD-infected cats. T. Spraker examined IHC sections from free-ranging mountain lions and consulted on histopathology and IHC interpretation. A. Robinson shared the Roslin Institute's primer sequences and provided helpful advice for mountain lion PRNP gene sequencing. Numerous field officers, biologists, and staff from the City of Fort Collins and City of Boulder, as well as others, acquired carcasses. Numerous hunters donated meat from CWD-infected deer and elk harvested throughout Colorado. Our work was supported primarily by the Colorado Division of Parks and Wildlife Game Cash funds, supplemented by Federal Aid in Wildlife Restoration funding in some years. This study is dedicated to Mischief, Rascal, and Spunky, our friends, coinvestigators, and arguably the three most beloved mountain lions known to science.

SUPPLEMENTARY MATERIAL

Supplementary material for this article is online at  http://dx.doi.org/10.7589/JWD-D-21-00029.

LITERATURE CITED

1.

Angers RC, Browning SR, Seward TS, Sigurdson CJ, Miller MW, Hoover EA, Telling GC. 2006. Prions in skeletal muscles of deer with chronic wasting disease. Science 311:1117. Google Scholar

2.

Apker J. 2017. Managing lions: Fandom–irony–anachronism. In: Proceedings of the 12th mountain lion workshop, McLaughlin CR, Vieira M, editors. Estes Park, Colorado, 15–18 May, pp. 17–24. Google Scholar

3.

Apker JA, Vieira M. 2017. Colorado mountain lion status report. In: Proceedings of the 12th mountain lion workshop, McLaughlin CR, Vieira M, editors. Estes Park, Colorado, 15–18 May, pp. 74–84. Google Scholar

4.

Barria MA, Balachandran A, Morita M, Kitamoto T, Barron R, Manson J, Knight R, Ironside JW, Head MW. 2014. Molecular barriers to zoonotic transmission of prions. Emerg Infect Dis 20:88–97. Google Scholar

5.

Bell JE, Gentleman SM, Ironside JW, McCardle L, Lantos PL, Doey L, Lowe J, Fergusson J, Luthert P, McQuaid S, et al. 1997. Prion protein immunocytochemistry—UK five centre consensus report. Neuropath Appl Neurobiol 23:26–35. Google Scholar

6.

Blecha K, Alldredge M. 2017. Spatio-temporal and demographic drivers of cougar predation behaviors in an urban-rural gradient. In: Proceedings of the 12th mountain lion workshop, McLaughlin CR, Vieira M, editors. Estes Park, Colorado, 15–18 May, p. 211. Google Scholar

7.

Bruce ME, Will RG, Ironside JW, McConnell I, Drummond D, Suttie A, McCardle L, Chree A, Hope J, Birkett C, et al. 1997. Transmission to mice indicate that ‘new variant’ CJD is caused by the BSE agent. Nature 389:498–501. Google Scholar

8.

DeVivo MT, Edmunds DR, Kauffman MJ, Schumaker BA, Binfet J, Kreeger TJ, Richards BJ, Schätzl HM, Cornish TE. 2017. Endemic chronic wasting disease causes mule deer population decline in Wyoming. PLoS One 12:e0186512. Google Scholar

9.

Diringer H, Beekes M, Oberdieck U. 1994. The nature of the scrapie agent: The virus theory. Ann N Y Acad Sci 724:246–258. Google Scholar

10.

Diringer H, Roehmel J, Beekes M. 1998. Effect of repeated oral infection of hamsters with scrapie. J Gen Virol 79:609–612. Google Scholar

11.

Edmunds DR, Kauffman MJ, Schumaker BA, Lindzey FG, Cook WE, Kreeger TJ, Grogan RG, Cornish TE. 2016. Chronic wasting disease drives population decline of white-tailed deer. PLoS One 11:e0161127. Google Scholar

12.

Eiden M, Hoffmann C, Balkema-Buschmann A, Müller M, Baumgartner K, Groschup MH. 2010. Biochemical and immunohistochemical characterization of feline spongiform encephalopathy in a German captive cheetah. J Gen Virol 91:2874–2883. Google Scholar

13.

Fox KA, Jewell JE, Williams ES, Miller MW. 2006. Patterns of PrPCWD accumulation during the course of chronic wasting disease infection in orally inoculated mule deer (Odocoileus hemionus). J Gen Virol 87:3451–3461. Google Scholar

14.

Fox KA, Muller SM, Spraker TR, Wood ME, Miller MW. 2021. Opportunistic surveillance of captive and free-ranging bighorn sheep (Ovis canadensis) in Colorado, USA, for transmissible spongiform encephalopathies. J Wildl Dis 57:338–344. Google Scholar

15.

Fraser H, Dickinson AG. 1968. The sequential development of the brain lesions of scrapie in three strains of mice. J Comp Pathol 78:301–311. Google Scholar

16.

Gill ON, Spencer Y, Richard-Loendt A, Kelly C, Brown D, Sinka K, Andrews N, Dabaghian R, Simmons M, Edwards P, et al. 2020. Prevalence in Britain of abnormal prion protein in human appendices before and after exposure to the cattle BSE epizootic. Acta Neuropathol 139:965–976. Google Scholar

17.

Gill ON, Spencer Y, Richard-Loendt A, Kelly C, Dabaghian R, Boyes L, Linehan J, Simmons M, Webb P, Bellerby P, et al. 2013. Prevalent abnormal prion protein in human appendixes after bovine spongiform encephalopathy epizootic: Large scale survey. BMJ 347:f5675. Google Scholar

18.

Gould DH, Voss JL, Miller MW, Bachand AM, Cummings BA, Frank AA. 2003. Survey of cattle in northeast Colorado for evidence of chronic wasting disease: Geographical and high-risk targeted sample. J Vet Diagn Invest 15:274–277. Google Scholar

19.

Hannaoui S, Schatzl HM, Gilch S. 2017. Chronic wasting disease: Emerging prions and their potential risk. PLoS Pathog 13:e1006619. Google Scholar

20.

Hewicker-Trautwein M, Bradley R. 2007. Portrait of transmissible feline spongiform encephalopathy. In: Prions in humans and animals, Hörnlimann B, Riesner D, Kretzschmar HA, editors. Walter de Gruyter GmbH & Co., Berlin, Germany, pp. 271–274. Google Scholar

21.

Hibler CP, Wilson KL, Spraker TR, Miller MW, Zink RR, DeBuse LL, Andersen E, Schweitzer D, Kennedy JA, Baeten LA, et al. 2003. Field validation and assessment of an enzyme-linked immunosorbent assay for detecting chronic wasting disease in mule deer (Odocoileus hemionus), white-tailed deer (Odocoileus virginianus), and Rocky Mountain elk (Cervus elaphus nelsoni). J Vet Diagn Invest 15:311–319. Google Scholar

22.

Hilbe MM, Soldati GG, Kati K Zlinszky KK, Sabina S Wunderlin SS, Ehrensperger FF. 2009. Immunohistochemical study of PrPSc distribution in neural and extraneural tissues of two cats with feline spongiform encephalopathy. BMC Vet Res 5:11. Google Scholar

23.

Ironside JW, Head MW, Bell JE, McCardle L, Will RG. 2000. Laboratory diagnosis of variant Creutzfeldt-Jakob disease. Histopathology 37:1–9. Google Scholar

24.

Kirkwood JK, Cunningham AA. 1994. Epidemiological observations on spongiform encephalopathies in captive wild animals in the British Isles. Vet Rec 135:296–303. Google Scholar

25.

Kirkwood JK, Cunningham AA. 1999. Scrapie-like spongiform encephalopathies (prion diseases) in non-domesticated species. In: Zoo and wild animal medicine: current therapy, 4th Ed., Fowler ME, Miller RE, editors. W. B. Saunders, Philadelphia, Pennsylvania, pp. 662–668. Google Scholar

26.

Kirkwood JK, Cunningham AA. 2007. Portrait of prion diseases in zoo animals. In: Prions in humans and animals, Hörnlimann B, Riesner D, Kretzschmar HA, editors. Walter de Gruyter GmbH & Co., Berlin, Germany, pp. 250–256. Google Scholar

27.

Krumm CE, Conner MM, Hobbs NT, Hunter DO, Miller MW. 2010. Mountain lions prey selectively on prion-infected mule deer. Biol Lett 6:209–211. Google Scholar

28.

Leggett MM, Dukes J, Pirie HM. 1990. A spongiform encephalopathy in a cat. Vet Rec 127:586–588. Google Scholar

29.

Mathiason CK, Nalls AV, Seelig DM, Kraft SL, Carnes K, Anderson KR, Hayes-Klug J, Hoover EA. 2013. Susceptibility of domestic cats to chronic wasting disease. J Virol 87:1947–1956. Google Scholar

30.

Miller MW, Fischer JR. 2016. The first five (or more) decades of chronic wasting disease: Lessons for the five decades to come. Trans N Am Wildl Nat Res Conf 81:110–120. Google Scholar

31.

Miller MW, Swanson HM, Wolfe LL, Quartarone FG, Huwer SL, Southwick CH, Lukacs PM. 2008. Lions and prions and deer demise. PLoS One 3:e4019. Google Scholar

32.

Miller MW, Wild MA, Williams ES. 1998. Epidemiology of chronic wasting disease in captive Rocky Mountain elk. J Wildl Dis 34:532–538. Google Scholar

33.

Miller MW, Williams ES, Hobbs NT, Wolfe LL. 2004. Environmental sources of prion transmission in mule deer. Emerg Infect Dis 10:1003–1006. Google Scholar

34.

Miller MW, Williams ES, McCarty CW, Spraker TR, Kreeger TJ, Larsen CT, Thorne ET. 2000. Epizootiology of chronic wasting disease in free-ranging cervids in Colorado and Wyoming. J Wildl Dis 38: 676–690. Google Scholar

35.

Moss WE, Alldredge MW, Pauli JN. 2016. Quantifying risk and resource use for a large carnivore in an expanding urban-wildland interface. J Appl Ecol 53: 371–378. Google Scholar

36.

Mysterud A, Edmunds DR. 2019. A review of chronic wasting disease in North America with implications for Europe. Eur J Wildl Res 65:26. Google Scholar

37.

O'Rourke KI, Baszler TV, Besser TE, Miller JM, Cutlip RC, Wells GAH, Ryder SJ, Parish SM, Hamir AN, Cockett NE, et al. 2000. Preclinical diagnosis of scrapie by immunohistochemistry of third eyelid lymphoid tissue. J Clin Microbiol 38:3254–3259. Google Scholar

38.

Pryor K. 1999. Don't shoot the dog! The new art of teaching and training. Bantam Books Inc., New York, New York, 224 pp. Google Scholar

39.

Rhyan JC, Miller MW, Spraker TR, McCollum M, Nol P, Wolfe LL, Davis T, Creekmore L, O'Rourke KI. 2011. Failure of fallow deer (Dama dama) to develop chronic wasting disease when exposed to a contaminated environment and infected mule deer (Odocoileus hemionus). J Wildl Dis 47:739–744. Google Scholar

40.

Ryder SJ, Wells GAH, Bradshaw JM, Pearson GR. 2001. Inconsistent detection of PrP in extraneural tissues of cats with feline spongiform encephalopathy. Vet Rec 148:437–441. Google Scholar

41.

Seelig DM, Nalls AV, Flasik M, Frank V, Eaton S, Mathiason CK, Hoover EA. 2015. Lesion profiling and subcellular prion localization of cervid chronic wasting disease in domestic cats. Vet Pathol 52:107–119. Google Scholar

42.

Sigurdson CJ, Spraker TR, Miller MW, Oesch B, Hoover EA. 2001. PrPCWD in the myenteric plexus, vagosympathetic trunk and endocrine glands of deer with chronic wasting disease. J Gen Virol 82:2327–2334. Google Scholar

43.

Sigurdson CJ, Williams ES, Miller MW, Spraker TR, O'Rourke KI, Hoover EA. 1999. Oral transmission and early lymphoid trophism of chronic wasting disease PrPres in mule deer fawns. J Gen Virol 80:2757–2764. Google Scholar

44.

Skinner BF. 1938. The behavior of organisms; an experimental analysis. Appleton-Century-Crofts, New York, New York, 457 pp. Google Scholar

45.

Spraker TR, O'Rourke KI, Balachandran A, Zink RR, Cummings BA, Miller MW, Powers BE. 2002a. Validation of monoclonal antibody F99/97.6.1 for immunohistochemical staining of brain and tonsil in mule deer (Odocoileus hemionus) with chronic wasting disease. J Vet Diagn Invest 14:3–7. Google Scholar

46.

Spraker TR, Zink RR, Cummings BA, Sigurdson CJ, Miller MW, O'Rourke KI. 2002b. Distribution of protease-resistant prion protein and spongiform encephalopathy in free-ranging mule deer (Odocoileus hemionus) with chronic wasting disease. Vet Pathol 39:546–556. Google Scholar

47.

Stewart P, Campbell L, Skogtvedt S, Griffin KA, Arnemo JM, Tryland M, Girling S, Miller MW, Tranulis MA, Goldmann W. 2012. Genetic predictions of prion disease susceptibility in carnivore species based on variability of the prion gene coding region. PLoS One 7:e50623. Google Scholar

48.

Tamgüney G, Miller MW, Wolfe LL, Sirochman TM, Glidden DV, Palmer C, Lemus A, DeArmond SJ, Prusiner SB. 2009. Asymptomatic deer excrete infectious prions in faeces. Nature 461:529–532. Google Scholar

49.

US Geological Survey. 2020. Distribution of chronic wasting disease in North America.  https://www.usgs.gov/media/images/distribution-chronic-wastingdisease-north-america-0. Accessed September 2020. Google Scholar

50.

Vorberg I, Buschmann A, Harmeyer S, Saalmüller A, Pfaff E, Groschup M. 1999. A novel epitope for the specific detection of exogenous prion proteins in transgenic mice and transfected murine cell lines. Virology 255:26–31. Google Scholar

51.

Wells GAH, Wells M. 1989. Neuropil vacuolation in brain: A reproducible histological processing artefact. J Comp Pathol 101:355–362. Google Scholar

52.

Westlund K. 2014. Training is enrichment—And beyond. Appl Anim Behav Sci 152:1–6. Google Scholar

53.

Will RG, Ironside JW, Zeidler M, Cousens SN, Estibeiro K, Alperovitch A, Poser S, Pocchiari M, Hoffman A, Smith PG. 1996. A new variant of Creutzfeldt-Jakob disease in the UK. Lancet 347:921–925. Google Scholar

54.

Williams ES. 2005. Chronic wasting disease. Vet Pathol 42:530–549. Google Scholar

55.

Williams ES, O'Toole D, Miller MW, Kreeger TJ, Jewell JE. 2018. Cattle (Bos taurus) resist chronic wasting disease following oral inoculation challenge or ten years' natural exposure in contaminated environments. J Wildl Dis 54:460–470. Google Scholar

56.

Williams ES, Young S. 1980. Chronic wasting disease of captive mule deer: A spongiform encephalopathy. J Wildl Dis 16:89–98. Google Scholar

57.

Williams ES, Young S. 1992. Spongiform encephalopathies of Cervidae. In: Transmissible spongiform encephalopathies of animals. Rev Sci Tech OIE 11: 551–567. Google Scholar

58.

Williams ES, Young S. 1993. Neuropathology of chronic wasting disease of mule deer (Odocoileus hemionus) and elk (Cervus elaphus nelson). Vet Pathol 30:36–45. Google Scholar

59.

Williams TM, Wolfe L, Davis T, Kendall T, Richter B, Wang Y, Bryce C, Elkaim GH, Wilmers CC. 2014. Instantaneous energetics of puma kills reveal advantage of felid sneak attacks. Science 346:83–85. Google Scholar

60.

Willoughby K, Kelly DF, Lyon DG, Wells GAH. 1992. Spongiform encephalopathy in a captive puma (Felis concolor). Vet Rec 131:431–434. Google Scholar

61.

Wohlsein P, Deschl U, Baumgärtner W. 2012. Non-lesions, unusual cell types, and postmortem artifacts in the central nervous system of domestic animals. Vet Pathol 50:122–143. Google Scholar

62.

Wolfe LL, Kocisko DA, Caughey B, Miller MW. 2012. Assessment of prospective preventive therapies for chronic wasting disease in mule deer. J Wildl Dis 48: 530–533. Google Scholar

63.

Wyatt JM, Pearson GR, Smerdon T, Gruffydd-Jones TJ, Wells GAH. 1990. Spongiform encephalopathy in a cat. Vet Rec 126:513. Google Scholar

64.

Wyatt JM, Pearson GR, Smerdon TN, Gruffydd-Jones TJ, Wells GAH, Wilesmith JW. 1991. Naturally occurring scrapie-like spongiform encephalopathy in five domestic cats. Vet Rec 129:233–236. Google Scholar
© Wildlife Disease Association 2022
Lisa L. Wolfe, Karen A. Fox, Karen A. Griffin, and Michael W. Miller "MOUNTAIN LIONS (PUMA CONCOLOR) RESIST LONG-TERM DIETARY EXPOSURE TO CHRONIC WASTING DISEASE," Journal of Wildlife Diseases 58(1), 40-49, (4 January 2022). https://doi.org/10.7589/JWD-D-21-00029
Received: 3 March 2021; Accepted: 5 August 2021; Published: 4 January 2022
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KEYWORDS
chronic wasting disease
Mountain Lion
mule deer
Odocoileus hemionus
prion
puma
Puma concolor
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