Granule cell type cerebellar hypoplasia in a beagle dog
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1 Laboratory Animals (1993) 27, Granule cell type cerebellar hypoplasia in a beagle dog Y. TAGO, O. KATSUTA & M. TSUCHITANI Mitsubishi Kasei Institute oj Toxicological and Environmental Sciences, 14 Sunayama, Hasaki machi, Kashima, lbaraki , Japan Summary Cerebellar hypoplasia characterized by severe depletion of granule cells and almost intact Purkinje cells was found in a male 19-month-old beagle dog used in a toxicity study. Microscopically, there was a narrow space lacking granule cells between the row of Purkinje cells and the medulla. Gliosis was not seen in any portion of the cerebellum including this space. No significant changes were seen in the Purkinje cells except for occasional cytoplasmic vacuolation. In the molecular layer and medulla, no histopathological abnormalities were observed. Keywords: Cerebellar hypoplasia; Granule cell; Pathology; Beagle dog Cerebellar hypoplasia is one of the most common congenital nervous system anomalies seen in domestic animals (Sullivan, 1985). Virus infections and trichlorfon toxicity during the developing stage are known to cause this malformation (Sullivan, 1985; Jones & Hunt, 1983; Knox et al., 1978). The typical microscopic features of cerebellar hypoplasia are decrease of both Purkinje cells and granule cells (Sullivan, 1985; Jones & Hunt, 1983). On the other hand, selective inhibition of granule cell development in the cerebellum of neonatal animals can be induced by X-irradiation (Altman & Anderson, 1972) or cycasin poisoning (Hirano et al., 1972). This report describes the spontaneous cerebellar hypoplasia characterized by diffuse Correspondence to: Dr Y Tago. Received 12 March 1992; accepted 9 July 1992 disappearance of granule cells and almost intact Purkinje cells in a 19-month-old male beagle dog. Case report This animal was one of the dogs imported from a commercial breeder in the USA (5 months old at arrival) for use in a 52-week chronic toxicity study. Vaccinations for brucellosis, leptospirosis, rabies, distemper, infectious hepatitis and parvovirus infection had been carried out before shipment. Rare and slight tottering had been observed from quarantine and acclimatization periods. Because of insignificant clinical sign, this case was allowed to be used in the study. As the result of random sampling, this case was placed in the highest dose group of four dogs. Throughout the study period, tottering was the only clinical sign found, and its intervals and degree were not progressive. At the end of the study period, this dog was killed by exsanguination from the carotid artery under sodium pentobarbital anaesthesia. Clinical and pathological examinations revealed no toxic effects on the nervous system in this study. The cerebellum and other organs and tissues of this dog were fixed in 100/0 neutral buffered formalin, embedded in paraffin wax, made into 5 I!m-thick sections and stained with haematoxylin and eosin (HE). Sections of the cerebellum were also stained with luxol fast blue (LFB), Bodian's method and Cajal's silverpyridine method. An ultrastructural examination was also performed. The cortico-medullary junction of the formalin-fixed cerebellum was cut into 10 pieces (approximately O 5 x 0,5 x O 5 mm in size), post-fixed with osmium tetroxide, embedded in epoxy resin, ultrathin-sectioned,
2 152 Tago, Katsuta & Tsuchitani Fig. 1. Median cut surface of the brain. Upper: normal case; lower: present case of cerebellar hypoplasia. Note apparently small cerebellum and its widened medulla. stained with uranyl acetate and lead citrate and examined with a transmission electron microscope (JEMIOO CXn, JEOL) operated at 80 kv. At necropsy, the cerebellum of this dog was obviously small (Fig. 1); thin folia consisting of Fig. 3. Adjacent section of Fig. 2. Note the narrow gap between the row of Purkinje cells and the medulla. No demyelinization is observed (LFB, bar: 10 /lm). narrow cerebellar cortex and relatively widened medulla were observed on the cut surface. No other macroscopic abnormalities were seen in any organs or tissues of this dog. Microscopically, severe depletion of granule cells was the most noticeable change in all areas of the cerebellum (Fig. 2). Due to thinning of folia, the space between them was widened. In the J<"ig.2. Hypoplastic cerebellum. Note thin cerebellar cortex and complete disappearance of granule cells(hemisphere, HE, bar: 10flm). Fig. 4. Cytoplasmic vacuolation in Purkinje cell. (LFB, bar: 5/lm).
3 Cerebellar hypoplasia in beagle dog 153 Fig. S. No gliosis is seen in the space lacking granule cells. (Cajal's silver-pyridine method, bar: 5 ILm). HE stained section, because of lack of granule cells, the border between the granular layer and medulla was unclear, giving an impression of widened medulla. However, in the LFB stain section, a narrow gap corresponding to the granular layer was clearly observed between the row of Purkinje cells and the medulla which contained abundant myelinated fibres (Fig. 3). No demyelinization was found in the medulla. Purkinje cells were almost intact and the distance between them was almost normal. However, some of them had cytoplasmic vacuolation (Fig. 4). These cells had several vacuoles of various sizes mainly located in their periphery. Vacuolation was found only in the Purkinje cells and not in the neurons of any other nuclei including those in the cerebrum, brainstem and spinal cord. In Bodian's method section, no significant changes were seen in the axons or dendrites of Purkinje Fig. 6. Cytoplasmic vacuolation in Purkinje cell. Vacuole with monolayer limiting membrane (arrow) contains Oocculent material and membranous substance. Inset: high power view (uranyl acetate & lead citrate, each bar: IlLm).
4 154 Tago, Katsuta & Tsuchitani cells and other nerve fibres of the cerebellum. Cajal's silver-pyridine method section revealed a few glia cells and their fibres in the space corresponding to the granular layer (Fig. 5), but no gliosis was seen. Ultrastructural examination revealed cytoplasmic vacuoles of Purkinje cells which had electron lucent spaces with a monolayer limiting membrane, containing flocculent material and membranous substance, and sometimes connected by a smooth endoplasmic reticulum (Fig. 6). However, no other significant changes were seen. Discussion The granular layer (internal granular layer) is formed by cell-immigration from the external granular layer during the developing stage of the cerebellum (Fujita et al., 1966; Shimada, 1966). Normally, the axons of the granule cells form parallel fibres, and their terminals make synaptic contacts with the spines of spiny branchlets of the Purkinje dendrites in molecular layer (Oyanagi, 1991). Depletion of granule cells has been reported in cases of organic mercury poisoning (Hunter & Russell, 1954), granule cell type cerebellar atrophy (Norman, 1940) and ataxic form of Creutzfeldt- Jacob disease (Brownell & Oppenheimer, 1965). In these cases, stellate bodies were often simultaneously observed in the molecular layer under light microscopy. The stellate bodies have been suggested to be excessively-produced spines of Purkinje dendrites, and formed as the result of disappearance of granule cells and their parallel fibres (Oyanagi, 1991). However, we found no significant changes in the molecular layer. This suggests that the granule cells had disappeared before they could make synaptic contact with the Purkinje cells. The absence of gliosis in the space corresponding to the granular layer and the lack of progressive clinical symptoms may support this view. The density of the Purkinje cells was normal. Because of the small mass of cerebellum, absolute number of Purkinje cells may be small, but there were no lesions suggesting their degeneration or necrosis, such as axonal torpedo or empty basket (Yasuba et al., 1988). The only abnormality seen in the Purkinje cells was cytoplasmic vacuolation. This change was not considered to be an artefact because it was observed only in the Purkinje cells. The pathological meaning of this change is not clear. However, the relationship between this lesion and defect of granule cells is doubtful, because this lesion seems to be relatively young, and it is suspected that the disappearance of granule cells occurred in the cerebellar developing stage as mentioned above. It is interesting that such dramatic depletion of granule cells had caused only minor clinical signs. Generally, in the cases of cerebellar hypoplasia with reduction of both Purkinje cells and granule cells, ataxia is the most common clinical sign (Knox et at., 1978; Jones &:; Hunt, 1983). In the present case, Purkinje cells were almost intact and no demyelinization was found. These facts may be associated with minor clinical signs. The cause of cerebellar hypoplasia in this dog could not be identified. Though this case belonged to the highest dose group, effect of treatment was excluded because no toxic effects on the nervous system were seen in the other animals used in this study and clinical signs had been observed from the quarantine period. The information provided by the breeder on litter mates, parents and their ancestors within several generations revealed no such familial tendency. During pregnancy, the mother of this dog had not received any drug treatment such as trichlorfon which is widely used as an antiparasitic and is known to induce cerebellar hypoplasia in piglets (Knox et al., 1978). The dog could not have been exposed to any of the conditions reported in experimental inhibition of granule cell development such as by X-irradiation (Altman & Anderson, 1972) or cycasin poisoning (Hirano et al., 1972). Several mechanisms are known in viral cerebellar hypoplasia, e.g. inhibition of cell division and maturation by the hog cholera virus and selective necrosis of external granular layer by the feline parvovirus and the viruses of bovine virus diarrhoea and border disease (Sullivan, 1985). There was no evidence of a viral infection in this dog, but the possibility could not be excluded.
5 Cerebellar hypoplasia in beagle dog 155 References Altman J & Anderson WJ (1972) Experimental reorganization of the cerebellar cortex. 1. Morphological effects of elimination of all microneurons with prolonged X- irradiation started at birth. Journal of Comparative Neurology 146, Brownell B & Oppenheimer DR (1965) An ataxic form of subacute presenile polioencephalopathy (Creutzfeldt-Jacob disease). Journal of Neurology, Neurosurgery and Psychiatry 28, Fujita S, Shimada M & Nakamura T (1966) lh-thymidine autoradiographic studies on the cell proliferation and differentiation in the external and internal granular layers of the mouse cerebellum. Journal of Comparative Neurology 128, Hirano A, Dembitzer HM & Jones M (1972) An electron microscopic study of cycasin-induced cerebellar alterations. Journal of Neuropathology and Experimental Neurology 31, Hunter D & Russell DS (1954) Focal cerebral and cerebellar atrophy in a human subject due to organic mercury compounds. Journal of Neurology, Neurosurgery and Psychiatry 17, Jones TC & Hunt RD (1983) The nervous system. In: Veterinary Pathology, 5th edn, pp Philadelphia: Lea & Febiger Knox B, Askaa J, Basse A, Bitsch V, Eskildsen M, Mandrup M, et al. (1978) Congenital ataxia and tremor with cerebellar hypoplasia in piglets borne by sows treated with Neguvon vet. (metrifonate, trichlorfon) during pregnancy. Nordisk Veterinaer Medicin 30, Norman RM (1940) Primary degeneration of the granular layer of the cerebellum: An unusual form of familial cerebellar atrophy occurring in early life. Brain 63, Oyanagi S (1991) The regenerative ability of the Purkinje cell as manifested in the degenerative human cerebellum. In Proceedings of the Xlth International Congress of Neuropathology, pp , 'Neuropathology' supplement 4. Japanese Society of Neuropathology Shimada M (1966) Cytokinetics and histogenesis of early postnatal mouse brain as studied by lh-thymidine autoradiography. Archivum Histologicum Japonicum 26, Sullivan ND (1985) The Nervous System. In: Pathology of Domestic Animals, vol. I, 3rd edn, pp (eds KVF Jubb, PC Kennedy & N Palmer). San Diego, New York, Berkeley, Boston, London, Sydney, Tokyo, Toronto: Academic Press Yasuba M, Okimoto K, Iida M & Itakura C (1988) Cerebellar cortical degeneration in beagle dogs. Veterinary Pathology 25,
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