SPONGIFORM ENCEPHALOPATHY OF ROCKY MOUNTAIN ELK

Transcription

1 SPONGIFORM ENCEPHALOPATHY OF ROCKY MOUNTAIN ELK Author(s): ELIZABETH S. WILLIAMS nd STUART YOUNG Source: Journl of Wildlife Diseses, 18(4): Published By: Wildlife Disese Assocition URL: BioOne ( is nonprofit, online ggregtion of core reserch in the biologicl, ecologicl, nd environmentl sciences. BioOne provides sustinble online pltform for over 170 journls nd books published by nonprofit societies, ssocitions, museums, institutions, nd presses. Your use of this PDF, the BioOne Web site, nd ll posted nd ssocited content indictes your cceptnce of BioOne s Terms of Use, vilble t Usge of BioOne content is strictly limited to personl, eductionl, nd non-commercil use. Commercil inquiries or rights nd permissions requests should be directed to the individul publisher s copyright holder. BioOne sees sustinble scholrly publishing s n inherently collbortive enterprise connecting uthors, nonprofit publishers, cdemic institutions, reserch librries, nd reserch funders in the common gol of mximizing ccess to criticl reserch.

2 Journl of Wildlife Diseses Vol. 18, No. 4, October SPONGIFORM ENCEPHALOPATHY OF ROCKY MOUNTAIN ELK #{176} ELIZABETH S. WILLIAMS nd STUART YOUNG, Wild Animl Disese Center nd I)eprtment of Pthology, College of Veterinry Medicine nd Biomedicl Sciences, Colordo Stte University, FortCollins, Colordol4o52.3, USA. Abstrct: A disese with striking clinicl nd pthologic similrities to the spongiform encephlopthies is described in six Rocky Mountin elk (Cervus elphus nelsoni) mintined in wildlife fcilities in Colordo nd Wyoming. Clinicl signs included behviorl ltertions nd progressive weight loss over period of weeks or months. Consistent microscopic lesions were limited to the centrl nervous system nd chrcterized by widespred spongiform trnsformtion of the neuropil, intrcytop!smic vcuoles in neuronl perikryons, nd strocytic hypertrophy nd hyperplsi. INTRODUCTION The purpose of this report is to describe the clinicl nd pthologic fetures of spontneous spongiform encephlopthic disese in six Rocky Mountin elk. We hve recently reported such disese syndrome, identified s chronic wsting disese (CWD), in cptive mule deer (Odocoileus hemionus hemionus), blck-tiled deer (0. hemionus columbinus), nd mule deer x white-tiled deer (0. virgininus) hybrid in the wildlife fcilities in Colordo nd Wyoming (Willims nd Young, 1980). The disese in elk occurred in the sme fcilities. MATERIALS AND METHODS Elk hd spordic fence-line contct with ffected nd cliniclly norml deer nd were occsionlly mintined in pens tht hd previously held CWDffected deer. The elk lso hd occsionl contct with other cptive nd freernging mmmlin species01 nd, in one fcility, with domestic sheep nd gots tht were confined in seprte pens within the compound. Elk were mintined for nutritionl nd metbolic reserch purposes nd generlly occupied pens up to 1 h. Good qulity lflf or grss hy, commercilly mixed grins supplemented with minerls nd vitmins, nd fresh wter were fed to the nimls except during experimentl feeding trils. Two of the elk were cptured s dults in Wyoming in the winter of nd trnsported to nd mintined t the Wyoming Gme nd Fish Deprtment Sybille Wildlife Reserch Unit. Four elk clves were hnd-rised in the Colordo Division of Wildlife fcilities or t the Wild Animl Disese Center, Fort Collins, Colordo, on cow s milk supplemented with vitmins nd wened onto lflf hy nd grin mixture This study ws supported in prt by Ntionl Institutes of Helth, Biomedicl Reserch Support Grnt 2-S117- RR05458-i9 nd by Burroughs Wellcome Fellowship dministered by the Americn College of Veterinry Pthologists. 01 White-tiled deer, pronghorns (Antelocpr mericn), bighorn sheep (Otis cnden.s isi, mouflon fot ts musimon). deer mice (Peromyscus mnicultus), house mice (Mus musculus), white-tiled jckrhhits Lepus townsendii), blck-tiled jckrbbits (L. clifornicus). desert cottontils (Sylt ilgu.s uduboniii, rccoons (Procyon lotor), striped skunks (Mephitis mephitis. Richrdson ground squirrels (Spermophilus richrdsoniii, 13-lined ground squirrels (S. tridecemlinetusi, domestic dogs nd cts.

3 466 Journl of Wildlife Diseses Vol. 18, No. 4, October, 1982 (Hobbs nd Bker, 1979). Three of these clves were obtined from either Sybille or the Denver Zoo in 1976 nd one ws collected from the wild in Blood smples in E1)TA nd for serum were obtined from two ffected elk for hemtologic evlution nd determi ntion of chemicl nd electrolyte levels; the elk were immobilized with xylzine hydrochloride E during smple collection. Erythroeyte nd leukocyte cell counts were performed on Coulter counter U nd hemoglobin content ws determined using Coulter hemoglobu!inometer.u A Hyce!-17 utonlyzer U ws used for nlysis of blood ure nitrogen (BUN), eretinine, cholesterol, biliruhin, sodium, inorgnic phosphorus, chloride, potssium, cretinine phosphokinse (CPK), serum glutmie oxlocetic trnsminse (SGOT), totl protein, globulin, nd lkline phosphtse. Cerebrospin! fluid ws collected (0.5 hr following euthnsi) from one elk; urinlysis ws performed on urine collected from the bldder of two elk t necropsy. Smples of liver from two elk were oven-dried overnight t 100 C, weighed, shed t 600 C, dissolved in HNO;i nd diluted in HO, nd nlyzed by tomic bsorption speetrometry for copper. Brin nd other tissues U of ffected elk were fixed by immersion in neutrl buffered 10% formlin solution within 1 hr of euthnsi. Brins from 15 ito 2-yrold cptive elk, two cptive dult bull elk, nd 22 2 to 9-yr-old free-rnging cow elk unffected with the clinicl syndrome were exmined s controls; these elk were euthnized nd tissues collected nd fixed s described for the ffected nimls. Tissue sections representing vrious regions of the brin were embedded in prffin, sectioned t 6-7 tim, nd stined with hemtoxy!in nd eosin. Selected tissues were post-fixed in formlin-mmonium bromide, sectioned t gm on freezing microtome, nd stined by the Cjl s gold sublimte method for strocytes (Lillie nd Fullmer, 1976). RESULTS Clinicl signs occurred in elk fter cptivity for period of 3 to 5 yr, whether hnd-rised or cptured in the wild s dults (Tble 1). Femles, mles nd cstrtes were ffected. The clinicl course of the disese lsted 1 to 6 mo nd ws chrcterized by nervousness or hyperexeitbility, ltertions in personlity, chnges in behvior towrd hndlers, nd progressive weight loss leding to emcition (Fig. 1). Most elk showed signs of excessive slivtion, teeth-grinding, lowering of the hed, nd drooping of the ers. Conspicuous polydipsi, polyuri or pruritis were not observed. Although behviorl chnges were consistently present, specific motor or sensory neurologic deficits were not identified. In ech instnce, the disese ws terminted by euthnsi. Hemtologic vlues, serum electrolytes nd serum chemistry (Tbles 2 nd 3) were considered to be in the norml rnge for elk (Kitchen, 1978) or to reflect their emcited condition. Cerebrospinl fluid ws colorless nd cler, the specific grvity ws 1.006, ph Rompun, Hver Lockhrt, Shwnee, Knss 6621)1, USA. UI Coulte-r Electriinics, Inc., Hile-h, Florid 13010, USA. U Hycel Inc., Houston. Texs 77ll5U, USA. L Vrin Techtriin 1251) tomic bsiirptiiin spe. ctriiphotiimeter, Vrinl echtron Pty. LTI)., Springvle, Victori, Austrli. U Hert, spleen, mesenteric lymph node, rumen. bomsum, jejunum, ileum, colon, spinl cord, lung, skeletl muscle, drenl glnd, pituitry glnd, thyriiicl glnd, pncres, liver, kidney, gonds nd eyes were collected from most nimls.

4 Journl of Wildlife Diseses Vol. 18. No. 4, October C ; n,. -, - e.., - l_.e.et I.. ci e Z Z Z Z - - CI CI CI - ci..,.c c.i c1 - - Cli Cl) Ci) Cl) Ci) Ci) -- - ici -1 c Ci).CI -,..ri., ClD.f.,C...,f.f - t) CI Z Cl) Cl) Cl) Ci), = = = = C C C C - : L, C z CIC C-C Cl) I- ci ci 0 CI. I

5 - :. 468 Journl of Wildlife Diseses Vol 18. No 4 October F1(t.TR )t 1tte (1 ( i)\ elk. 4 yr of ge, showing ( Xce ssive slivtilin end depressed ttitude d hrctei isti( e)f the syndrome. TA.BLE 2. 1 Ie. mtiiliigic vlues of two Hocks Mountin elk with spongif orm encephlei pt hy. Prmeter Elk ol Elk #{176}. P( V ( UI 3:3 :38 hg (11) Serum protein (g dl) WB(. mm Neutrophils U Lymphocytes ( I 29 :39 Monocvte s ( 1) 1 hosinophils (1) 5 2 I3sophils, 0 (1 ws 7, nd te)tl protein ws 50 mg. Pndy test nd ( Ph. were negtive; few ervthrocvtes nd iine monocvte were present in the smple. 1.Ji ine specific grvity nd phi we re nd 7.5 nd nd 8.0, resl)e ctivelv, for two elk. The urine smple s were negtive for protein, glucose, ke teine s, nd bilirubin, but one smple hd trce e)f hemogleibi ii nd 1)0th contined few epithelil ( ( us. Liver copper levels (Tble ;o were ( ill) sidered to be within the nelrml rnge for elk nd red deer (Ce rcus clp Jius (Reid et l., 1980: McTggrt et l The primry gross lesions were emcition nd dr, rough pelge.

6 Journl of Wildlife Diseses Vol. 18, No. 4, October, TABLE 3. Serum electrolytes, serum chemistry, nd live Mountin elk with spongiform encephlopthy. r copper levels of two Rocky Prmeter Elk #4 Elk #5 BUN(g/dl) Globulin (g/dl) Cholesterol (mg/dl) Totl bilirubin (mg/dl) Cretinine Alk. phos. (U /l) SGOT(U/l) 102 :34 Inorgnic phosphorus (mg/dl) Clcium (mg/dl) Chloride (meg/dl) Sodium (meg/di) Potssium (meg/dl) 4.3 Liver copper (ppm) b 40 lntemtionl units. per million, dry weight Trumtic reticulitis nd pericrditis were ssocited with smll pieces of biling wire penetrting the forestomchs of two nimls. One elk ws pregnnt nd helthy full-term clf ws removed t the time of euthnsi. The clf remined cliniclly norml until killed when 2.5 yr of ge. Microscopiclly the brin ws norml. Consistent histopthologic chnge ws not identified in extrneurl tissues of ffected elk. Neurohistologic chnges, similr in ll ffected elk, were chrcterized by spongiform trnsformtion of the neuropil, predominntly of the gry mtter (Fig. 2) nd to lesser degree the white mtter, by single or multiple intrcytoplsmic vcuoles in neuronl perikryons (Fig. 2), nd by neuronl degenertion. Inflmmtion ws not observed. Spongiform chnge ws widespred, vrible in severity, nd spred only portions of cerebrl cortex nd bsl gngli. Astrocytic hypertrophy nd hyperplsi were demonstrble in gold sublimte stined sections (Fig. 3). Exmintion of brins from 39 cptive or free-rnging elk, cliniclly unffected with the syndrome, did not revel the presence of spongiform eneephlopthy. Only occsionl discrete single vcuoles were observed intrcytoplsmiclly nd in the neuropil of grey nd white mtter. Mny control elk showed vsculr nd neuropthologic evidence of eleophorosis. DISCUSSION CWD of mule deer ws first identified in 1967 t Fort Collins; the first two elk cses were in 1979 in the sme pens. Subsequently, cses in elk were dignosed t Sybille, 2 yr fter the first cse of CWD ws recognized in deer t tht fcility. Morbidity nd mortlity of elk since recognition of this syndrome vried between the two fcilities. Four of eight elk hnd-rised nd mintined for longer thn 3 yr in the Fort Collins fcility died of this disese, while in the Sybille fcility only two of 60 hve been ffected. Mngement of the elk ws somewht different t these fcilities. At Fort Collins, ll elk were hnd-rised nd hd close contct with humns nd with other cptive wild species, including mule deer. In contrst, elk t Sybille were cptured s dults from the wild nd hd only spordic direct contct with

7 470 Journl ofwildlife Diseses Vol 18. No 4, October 1982 I d. 4 S (-4 C. - r. p.,,, b. 4.., I q.,,..-,, p. -, e-.. :1 #{149},1. (_) S.. S.,...4.,;.-. t... 5,,. F!( ;URE 2. 1)if f use speingi f e)rm chnge in the neure)pil nd intrcvliiplsmic vcuides in noun ins i if the med ull oble)ngt. h-1& E. 6:30., -. J.5. S #{149} - *t.,.... I S,. Fl( JRE :3. Asti eio vtlc hypertrophy nd hyperplsi in the thlmus. ( jl s gold ( hliinide impregnltiiin ON), humns nd fence line ( ont( t with o)the r species. Mny more cses of ( WI) in deer hve occurred in the l ort (.edlins fcility thn t Svhille. It is not known if these mngement differences sig- nificntly influenced development e)f the disese, Clinicl pthologic vlues e)f ffected elk were conside red to) he in the norml rnge for elk, with the exception of low

8 Journl of Wildlife Diseses Vol 18 No 4. October urine specific grvity, 1)egenertive chnges were consistently present in the hypothlmus nd, in some elk, specific lesions were identified in the supro)ptic nd prventrk-ulr nuclei. This dmge co)uld influence production e)f ntiduiretic hormone with resultnt com pre)mised bility to concentrte the urine. All nimls were in norml stte o)f hydrtion when killed. The clinicl signs nd neurohisto. pthology of this syndrome in elk closely resemble CWI) ef mule deer (Willims nd Young, 1980) nd re qulittively comprble te) other spongiform encephlopthies of nimls (scrpie. trnsmissible mink encephlopthy) nd mn (kuru, Creutzfeld-.Jkob (lisese) (Prusiner nd Hdlow, 1979). The ssocition 1)etween CWI) in mule (leer nd the spongiform encephle)pthy e)f elk held in the sme fcilities is uncler. The disese is pprently limited te) wildlife fcilities in ( olordo nd Wyoming. The indirect or fence-line contct e)f elk in 1)0th fcilities with ffected mule (leer provides only (ircu mst ntil evidence of trnsmission of the disese between these species. Similr -ir- -umstntil evidence indicting possil)l( horizontl trnsmission mong mule deer exists. 1)ut the primry source of the disese in mule deer nd elk hs not been identified. Estblished trnsmissible spongiform encephlopthies hve been trnsnlitteol to vriety o)f species nd re thought to) be cused l)y slow virus infection. Acknowledgements We wish to) thnk Mr. Pul Neil. Mr. I)n Bker, Mr. Huey I)wson, nd l)rs. Tom Thorne nd Bill Lnce fe)r ssistnce nd cse mteril. LITERATURE CITEI) HOBBS, NT. nd I).L. BAKER Rering nd trining elk clves for use in food hbits studies. J. Wildl. Mnge. 43: KITCHEN, H Hemtologicl vlues nd blood chemistries for vriety of rtiodctylids. In: 7..iio nd Wild Animl Medicine. ME. Fowler (ed). W.B. Sunders Co., Phildelphi, Pennsylvni. pp LILLIE, RI). nd H.M. FULLMER Histopthologic Technique nd Prcticl Histoc/ie,nistrv, 4th ed. McGrw-Hill Book Ce)., New York, New York. 942 pp. McTAGGART, H.S., V.P.N. LOWE, P.J. BARI)EN nd J.B.M. GELLATLY Copper sttus of red deer on the islnd of Rhum. Vet. Rec. 109: PRUSINER, SB. nd W.J. HA!)LOW Slow Trnsmissible Diseses of the ous S stem. Vol. 1.: ( lin icl, Epidem zologi cl, Gen ( tic rid Pthologic Aspects of the Spongiforin Lncephlopthzes. Acdemic Press, New york, New York. 472 pp. REII), T.C.. H.J.F. McALLUM nd P.1). JOHNSTONE Liver copper (-one-entrtions in red deer (C ro us elphus) nd wpiti ((.cndenszs) in New Zelnd. Res. Vet. Sci. 28: , WILLIAMS, ES. nd S. YOUNG Chronic wsting disese of cptive mule (leer: spongiform encephlopthy. J. Wildl. l)is. 16: Rece,t ed for publiction 26 April 1982