Neurological disorder in two calves ( Alces alces L.) naturally infected with Elaphostrongylus alces

Margareta Steen1 and Lars Roepstorff2

'National Veterinary Institute, S-750 07 Uppsala, Sweden 2Faculty of Veterinary Medicine, Swedish University of Agricultural Science, S-750 07 Uppsala, Sweden

Abstract: Two months old moose calves exhibiting neurological signs were videotaped, killed and necropsi- ed. The parasite Elaphostrongylus alces (Steen et al 1989) was found epidurally along the meninges of the spinal cord, and in the muscle faciae of the thoracic and lumbar regions. Progressive inflammatory pro• cesses were present in the epineurium, perineurium and endoneurium. Accumulations of inflammatory cells, eosinophils, lymfocytes and macrophages, were found around eggs and larvae and frequently, around regional blood wessels. The neurological disturbances in the moose calves were pronounced, with loco• motive abnormalities and ataxia. They showed weakness in the hindquarters, with uncoordinated and sway• ing movements of the hind legs. In addition, one of the calves was lame on the left forelimb. The muscles of the leg were visibly atrophic. The lesions produced by E. alces at the lumbar nerve roots and in the cauda equina are suggested to be the cause of the clinical signs observed.

Rangifer, Special Issue No. 3, 1990: 399-406

Introduction cus) (Vsevolodov and Pryadko 1964) and rein• Elaphostrongylus spp. are parasitic (Rangifer tarandus tarandus L.). (Roneus and associated with the central nervous system and Nordkvist 1962, Kummeneje 1974). muscle fasciae of a variety of cervids (Cameron Experimental infections have been perfor• 1931, Lyubimov 1945, Mitskevich 1958, med in different cervids, as caribou (Rangifer Roneus and Nordkvist 1962, Kummeneje tarandus caribou) (Lankester 1977), 1974, Krutzer and Prosl 1975, Mason et al (Mitskevich 1964), red deer (Watson 1982) 1976, Sugar 1978, Steen and Rehbinder 1986, and moose (Alces alces L.) (Lankester 1977, Stuve, 1987). Stuve and Skorping 1987.) Watson (1982) re• Elaphostrongylus spp. have been knovn to cau• ported that E. cervi infection in red deer calves, se neurologic disorders in wild and domesti• produced exercise intolerance, blindness, hind cated cervidae, as red deer (Cervus elaphus L.) limb incoordination and nervous disorders. A (Borg 1979), maral deer (Cervus elaphus sibiri- moose calf infected with L3-larvae obtained

Rangifer, Special Issue No. 3, 1990. 399 from caribou showed pronounced weakness joints, she had difficulties to lift the hind part of primarily affecting the hindlimbs. The process her body with the hind legs. She was able to rise progressed rapidly until the calf after four to a standing position only by supporting her• months was unable to stand up (Lankester self against a tree. When standing the hind legs 1977). Stuve and Skorping (1987) experiment• were notably weaker than the front legs, and ally infected a moose calf with ELpbostrongylus the left hind leg was often abducted. The calf larvae obtained from moose. The moose calf put most of her weight upon her front legs showed neurological disorders, but recovered when walking with unsteady swaying move• The present study is the first to report on a ments of the hind quarters and a broad gait (Fig natural infection with E. dices in two wild moose 4). Forced to move, she lifted the forelimbs ab• calves with clinical manifestation of neurologi• normally high and brought them down in a cal disorders. stamping fashion. She easily stumbled over when handled or even when walking on slightly Material and methods uneven ground. The calf did not seem to be In May 1987 two approximately 11 months old mentally affected and was alert. moose calves, one male and one female, exhibi• Cdse 2. ting neurological signs, were found in the co• The male calf was observed in an area of approxi• unty of Lapland in the northern part of Sweden. mately 50 m2 that was totally browsed. Like the They were studied and videotaped before being female calf he appeared weak, uncoordinated and killed and necropsied. indifferent to disturbance. In attempts to rise he The brain and the whole spinal cord with often remained in a position of a "sitting dog". nerve roots were removed and examined for E.. He was lame in his left forelimb, which had alces and pathological lesions. Skeletal muscles atrophic muscles (Fig 5). When standing the were examined for the occurence of the pa• body weight was mainly supported by the right rasite. Visceral organs were inspected macro- forelimb and the left hind limb. The left front scopically and microscopically. The brain, spi• leg was frequently adduated (Fig 6). When nal cord, nerve roots, fasciae from skeletal forced to turn, the 's hind quarters sway• muscles and visceral organs were fixed in 10% ed even while standing on both hindlegs (Fig 7, formaline and prepared for histology. Nema• 8, 9). He frequently stumbled over when mov• todes found were fixed in heated 70% ethanol ing (Fig 10, 11, 12, 13). The hind leg gait was and identified. Bone marrow fat content was abnormally broad (Fig 6). The calf seemed to examined according to the method of the Nor• be aware and alert. dic Committee on Food analysis (1955). Gross pathological findings In both calves several adult E. dices were found Results epidurally in the lumbar region of the spinal ca• Neurological signs nal and in the cauda equina. In the male calf, Cdse 1. parasites were also located epidurally in the The female calf appeared week, uncoordinated thoracic region. The presence of E. dices was and indifferent to human proximity. She rose caracterized by hemorrhage and oedema in the with difficulty, leaning her cheek against the surrounding tissues. ground in order to gain and support balance Parasites were also found in the fasciae of the (Fig 1,2). When standing, her hind limbs were thoracic and lumbar muscles without surround• shivering, unsteady and weak, and the lumbar ing reactions. The bone marrow fat content region was lowered (Fig 3). was low (0.01%; 3.5% respectively), and both When rising and standing on her carpal calves were emaciated. 400 Raitgifer, Special Issue No. 3, 1990. Histopathological findings The epidural location of the nematodes and In the connective tissue surrounding the spinal the inflammatory changes, as seen in moose, cord, close to the nerve roots, aggregates of differs from that in other cervidae, where the mainly mononuclear leucocytes around blood parasites and the histopathological changes are vessels were a common finding. The inflamma• found in the subdural and the subarachnoidal tory reaction was generally characterized by spaces (Roneus and Nordkvist 1962, Polyan- oedema, hemorrhages and infiltrations by lym- skya 1963, Pryadko et al 1963, Mitskevich focytes, plasma cells, eosinophiles and macro• 1964, Barus and Blazek 1973, Prosl and Kutzer phages. Signs of intensive phagocytosis were 1980). Whether the locomotive disturbances seen as macrophages were partly or completely described in these two cases are solely due to filled by detritus masses. the nervous tissue lesions, or partly caused by The inflammatory changes in the meninges inanition and exhaustion, is difficult to evaluate. often extended to the spinal nerve roots. It is thus necessary to perform experimental Granulomas were observed around eggs and studies in order to obtain more conclusive data larvae. They were surrounded by a thin capsule on the neurological effects of infestations by of connective tissue. Infiltrates by mainly E. dices in moose. lymfocytes, were frequently found to extend in• Acknowledgements to the nerve tissue, invading the epineurium, This study was financially supported by the Swedish perineurium and endoneurium. National Environmental Protection Board. We thank Professor B. Funqvist for essential help and Discussion guidance, photographer B. Ekberg for skilful tech• nical assistance and game-keeper K-I From, Mr J. The locomotive abnormalities with symptoms Jonsson and Mr M. Jonsson for locating the moose of ataxia, as incoordination, swaying of the calves and videotaping them. hindquarters, broad and stamping gait and a certain amount of hypermetria suggest para• References lysis of ascending proprioceptive nerve fibers. Borg, K. 1979. Symntome der Kreuzlahme Schlen¬ It is known that the long proprioceptive kerkrankheiten bei Elaphostrongylus befalls des nerve fibers in the spinal cord and in the dorsal Kleinhirs bei einem Rotwildkalb /Symtoms of a ganglia are those to be injured first by com• lumbar paralysis (Kreuzlahme) in a red deer calf pression, (de Lahunta 1977). on the occasion of Elaphostrongylus infestation of The extent of the inflammatory reactions the cerebellum. - Z- Jegerwiss. 25: 237-238. strongly indicates the possibility of a compress• Cameron, TW.N. 1931. On two new species of ion of the nerve fibers by hemorrhages, oede- nematodes from the Scottish red deer. - J. Hel- mas, granulomas and perivascular cuffings, minthol. 9: 213-216. causing the described functional nervous di• de Lahunta, A. 1977. Vet. neuro -anatomy and clin• ical neurology. Wb. Saunders 6C Co. Philadelphia sturbances. Due to the circumstances during 205-211. the examination of the , paralysis due to Kummeneje, K. 1974. Encephalomyelitits and compression of efferent nervfibres can not be neuritis in acute cerebrospinal nematodiasis in re• excluded as the spinal nerves, carry both aff• indeer calves. - Nord. Vet. Med. 26: 456-458. erent and efferent nervfibres. The locomotive Kutzer, E. and Prozl, H. 1975. Zur Kenntnis von disturbances described, might also be explai• Elaphostrongylus cervi, Cameron, 1931. Morpholo• ned by the lesions shown in the epineurium, gic und diagnosse. (Contribution to the know• perinerium and endonerium, of the spinal ledge of Elaphostrongylus cervi, Cameron 1931. nerves. Morphology and diagnose - Wien, Tierarztl. M. Schr. 62:258-266.

Rangifer, Special Issue No. 3, 1990. 401 Lankester, M.W 1977. Neurologic disease in Roneus, O. and Nordkvist, M. 1962. Cerebro• moose caused by Elapbostrongylus cervi, Cameron spinal and muscular nematodiasis (Elapbostrongy• 1931, from caribou. - In: Proceedings of the 13th lus rangiferi) in Swedish reindeer. - Acta Vet Scand. annual North American moose conference and work• 3: 201-225. shop. Jasper, Alberta: 177-190. Steen, M. and Rehbinder, C. 1986. Nervous Lyubimov, M.P 1945. Novye glistneye Zabole- tissue lesions caused by elaphostrongylosis in wild vaniya mozga pantovykh olenei (New helminth di• Swedish moose. - Acta Vet Scand. 27 :326-346. seases of the brain of reindeer). - Sbornik N.-I. Ra¬ Steen, M., Chabaud, A. and Rehbinder, C. bot (Lab. Pantovogo olenovodstva Nkskh SSSR): 1989. Species of the genus Elapbostrongylus. Para• 225-232. site of Swedish Cervidae. A description of E.alces Mason, P.C., Kiddey, N.R., Sutherland, R.J., n.sp. - Anm. Parasitol. Hum. Comp. 64: 134-142. Rutherford, D.M. and Green, A.G. 1976. Stuve, G. 1987. Elapbostrongylus cervi infection in Elapbostrongylus cervi in red deer. - N.Z- Vet. I, 24: moose (Alces alces). Prevalence and pathological 22-23. changes in relation to age and season. - Acta Vet Mitskevich, VYu. 1958. Krashifrovke tsikla raz- Scand. 28: 157-164. vitia Elapbostrongylus rangifer nov. sp. otsevernogo Stuve, G. and Skorping, A. 1987. Experimental denya (Unraveling the cycle of development of Elapbostrongylus cervi infection in moose (Alces al• Elaspbostrongylus rangifer nor. sp from reindeer). - ces). - Acta Vet Scand. 28: 165-171. Dobl. AN SSSR, 3: 621-624. Sugar, L. 1978. On the infestation of Mitskevich, VYu. 1964. Tsikl razvitia Elapbo• wild ruminants in in Hungary (In Hungarian). - strongylus rangiferi Miz., 1958 (Cycle of develop• Parasitol. Hung. 11: 146-148. ment of Elapbostrongylus rangiferi Miz., 1958 ).- Vsevolodov, B.P. and Pryadko, E.I. 1964. Ma- Parazity Sel'skokhozyaistvennykb Zbivotnykb Ka- terialy po patomorfologii mozgovogo elafostron• zdkhstana, 3. Gel'minty. - Izd-vo AN KazSSR. gileza maralov (Data on the patology and morp• Alma-Ata: 49-60. hology of cerebral elaphostrongylosis of Sibirian Pryadko, E.I., Vysokov, S.N. and Frolov, VS. maral). - Parazity S. -kh. Zbivotnykb Kazakhstana. - 1963. On the epizootology of elaphostrongylosis hd-vo AN KazSSR, Alma-Ata, vol 1: 71-78. in reindeer (K epizootologii, Elafostrongileza pan• Watson, T.G. 1982. Some clinical and parasito- tovykh oleni).- Parasity Sel'skokhozyaistvennykb Zbi• logical features of Elapbostrongylus cervi infections votnykb Kazakhstana, Jzd-vo AN KazSSR, Alma- in Cervus elaphus: Proceedings N.Z- Society of Para• Ata 2: 74-85. sitology, 129.

t.-

Fig. 1. Female moose calf rising with difficulty.

402 Rangifer, Special Issue No. 3, 1990. Fig. 2. Leaning her cheek against the ground to gain balance.

Rangifer, Special Issue No. 3, 1990. Fig. 5. Male moose calf with lame and atrophic left forelimb.

404 Rangifer, Special Issue No. 3, 1990. Fig. 7-9. Forced to turn, the hindquarter is swaying, weak and unsteady.

Rangifer, Special Issue No. 3, 1990. 405 Fig. 10-13. When moving, the male moose calf frequently stumbled over.

406 Rangifer, Special Issue No. 3, 1990.