Failure of pyramidal tract decussation in the Dandy-Walker syndrome
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1 J Neurosurg 50: , 1979 Failure of pyramidal tract decussation in the Dandy-Walker syndrome Report of two eases RAYMOND L. LAGGER, M.D. Department of Pathology ( Neuropathology ), Stanford University School of Medicine, Stanford, California o,' The author describes non-decussation of the corticospinal tracts in two patients with the Dandy-Walker syndrome and multiple other congenital anomalies. KEY WORDS 9 pyramidal tract 9 Dandy-Walker syndrome 9 hydrocephalus 9 congenital malformation T HE occurrence of a variety of congenital anomalies in association with the Dandy-Walker syndrome is well known. Agenesis of the corpus callosum, glial heterotopias, syndactylism, and polycystic kidneys are frequently encountered in patients who have this syndrome, and are well documented in the literature. 3'8 Although there have been several reports of the Dandy-Walker anomaly occurring in association with absent medullary pyramids, TM the literature contains no description of a case in which it is accompanied by non-decussation of the corticospinal tracts. The following is a report of two such cases. Case 1 Case Reports This baby boy weighing 1300 gm was delivered at the Stanford University Hospital by caesarean section to a healthy, 34-year-old, primiparous mother. The 33-week pregnancy was complicated by late polyhydramnios and pre-eclampsia. After delivery, the child appeared to be deeply cyanotic and did not breathe spontaneously. Despite vigorous resuscitative efforts, he remained hypotonic and apneic. Examination. Physical examination disclosed multiple congenital anomalies, which included an abnormal skull with a prominent forehead and depressed temporal bones; a submucous cleft palate; small (2 cm), low-set ears; and a small thorax suggestive of hypoplastic lungs. Abdominal examination revealed large, mobile, polycystic kidneys. Duodenal atresia was suspected when a plain film of the abdomen, taken when the child was 5 hours old, failed to show bowel gas past the duodenum. Intra-abdominal calcific streaks were also noted on the film. The infant had a complex, right-to-left, congenital, cyanotic heart defect, and a chest x-ray film revealed mesocardia. Six hours after delivery, the child died of cardiorespiratory failure. Postmortem Examination. General autopsy confirmed the presence of these multiple congenital anomalies. The brain weighed 150 gm. External examination of the brain revealed a typical Dandy- Walker malformation, with a prominent cleft in the midline of the cerebellum and an apparent absence of the posterior vermis (Fig. 1). There was cystic dilatation of the fourth ventricle and evidence of fresh subarachnoid hemorrhage over the inferior aspect of the right temporal lobe. Serial coronal sections revealed moderate ventricular dilatation and a patent Sylvian aqueduct. The corpus callosum was intact. There was a small intratemporal hematoma contiguous with the subarachnoid hemorrhage over the surface of the right temporal lobe. Close inspection revealed patency of the foramen of Luschka. The patency of the foramen of Magendie could not be determined. Microscopic examination of the brain stem and cerebellum revealed that the Dandy-Walker cyst was lined by ependyma and was continuous with the fourth ventricle. The cyto-architecture of the cerebellar folia, dentate, and emboliform nuclei was normal. Serial sections taken at several levels of the brain stem and spinal cord revealed non-decussation of the cor- 382 J. Neurosurg. / Volume 50 / March, 1979
2 Uncrossed pyramidal tracts FIG. 1. Case 1. Caudal view of hind brain demonstrating absence of the posterior vermis (left) and cystic dilatation of the fourth ventricle (right). ticospinal tracts. The pyramidal tracts occupied their usual ventral location in the cerebral peduncles, migrating anteromedially at the level of the medullary pyramids and continuing uncrossed in the ventral funiculi throughout the course of the spinal axis (Fig. 2). Case 2 This 31/2-year-old girl, the product of a normal pregnancy and delivery, was first seen at the Stanford University Hospital at 3 weeks of age because of an expanding head circumference. A wide metopic suture, bulging anterior fontanel, and a capacious posterior fossa were noted. Ventriculography revealed hydrocephalus, absence of the septum pellucidum, and an extremely large, cystically dilated, fourth ventricle. The tentorium and torcula were displaced superiorly. A ventriculo-atrial shunt was placed initially, but required several revisions. Course. As the child developed, an increasingly spastic right hemiparesis became apparent. She kept her head and eyes deviated to the right, but would follow a target by moving her head. It was postulated that she had a right homonymous hemianopsia. She was unable to sit upright, had very poor head control, and her speech was not spontaneous. Her IQ was estimated at 27. During the last 18 months of her life, her ventriculo-atrial shunt did not function. She had no signs of increased intracranial pressure and her hydrocephalus was apparently arrested. She developed a febrile respiratory illness and died of respiratory failure at the Porterville, California, State Hospital. Postmortem Examination. Autopsy revealed that the skull had a prominent dolichocephalic shape; upon removal of the calvaria, multiple anomalies were seen. The brain weighed 1225 gm. There was absence of the anterior falx, crista galli, and the olfactory bulbs and tracts. The cerebral hemispheres were enlarged with conspicuous absence of the interhemispheric fissure anteriorly, producing a single frontal lobe (holo- prosencephaly). The tentorium, torcula, and lateral sinuses were displaced superiorly and the superior sagittal sinus was foreshortened. The cerebellar hemispheres appeared to be displaced laterally and superiorly by a large midline cyst of the fourth ventricle (Fig. 3). The patency of the outflow foramina could not be adequately ascertained. The Dandy- Walker cyst appeared to displace the normal anterior vermis superiorly over the quadrigeminal plate, and to displace a remnant of the posterior vermis laterally over the medial aspect of each cerebellar hemisphere. Serial coronal sections of the brain confirmed arrhinencephaly and prosencephaly. In addition, agenesis of the corpus callosum and absence of the septum pellucidum were noted. The right cerebral hemisphere, with the exception of the single frontal lobe, appeared normal, with a well developed cortical mantle, basal ganglia, and thalamus. The left temporal, parietal, and occipital lobes were rudimentary, with poorly defined subcortical architecture and multiple glial heterotopias. Microscopic sections of the left cerebral hemisphere demonstrated a marked disturbance in the cortical lamination. There was much heterotopia and micropolygyria. Sections of the cerebellum showed that the ependyma-lined cyst was continuous with the fourth ventricle. The architecture of the cerebellar hemispheres was normal. Sections of the brain stem showed a conspicuous absence of the left cerebral peduncle and pyramid, and apparent hypertrophy of the right pyramidal tract, which remained uncrossed and running in the right ventral funiculus throughout the entire length of the spinal cord (Fig. 4). In addition, there was a striking absence of the lateral funiculi; the posterior columns and central gray matter of the spinal cord were present. Discussion Congenital hydrocephalus associated with cystic dilatation of the fourth ventricle and absence of the J. Neurosurg. / Volume 50 / March,
3 R. L. Lagger FIG. 2. Case 1. Serial sections of hind brain and spinal cord demonstrating failure of pyramidal decussation and persistently uncrossed, poorly myelinated corticospinal tracts running in the ventral funiculi of the cord. Upper Left." Medulla. Upper Right." High cervical cord. Lower Left." Low cervical cord. Lower Right." Lower thoracic cord. H & E, 6. posterior vermis of the cerebellum was originally described by Dandy and Blackfan in 1914, ~ and later was reviewed by Taggert and Walker in is Both papers postulated that the associated hydrocephalus and concomitant cystic dilatation of the fourth ventricle were a consequence of congenital atresia of the foramina of Luschka and Magendie. Benda, in 1954,1 criticized this widely recognized theory of congenital hydrocephalus after reviewing a number of well documented cases of the anomaly in which hydrocephalus was minimal or absent, and in which the outlet foramina of the fourth ventricle appeared to be patent; these features were apparent in our first case. Benda thought that the anomaly was, indeed, a dysraphic disorder of the cerebellum in which the posterior vermis failed to fuse during embryological development, resulting in the posterior cystic dilatation of the fourth ventricle. Taggert and Walker 15 cited the observations of Hess, 7 Retzios, 13 and Koelliker, 1~ who found that the foramina of Luschka and Magendie appeared patent in the fourth to fifth months of intrauterine life. Since the vermis fuses in an anterior-to-posterior direction during the fifth month of development, Taggert and Walker concluded that fusion of the vermis would be arrested if the foramina failed to open. They suggested that this would be most evident in cystic dilatation of the posterior vermis. Later authors have taken exception to this hypothesis. Gardner, et al., 5 have pointed out that the roof of the fourth ventricle differentiates into rostral and caudal membranous areas early in fetal development. The rostral portion forms the choroid plexus of the fourth ventricle and the vermis overlying it during the sixth week of embryonic life. The caudal membranous area differentiates into the caudal sac (of Blake), which becomes permeable at the eighth week of development and ultimately becomes the foramen of Magendie. Brodal and Hauglie-Hanssen, 2 in their description of two cases of the Dandy-Walker syndrome, suggested that the rostral membranous area was directly involved in the pathogenesis of the 384 J. Neurosurg. / Volume 50 / March, 1979
4 Uncrossed pyramidal tracts Fic. 3. Case 2. Hind brain in situ at autopsy with well developed cerebellar hemispheres separated by a midline fourth-ventricular Dandy-Walker cyst. Note cephalad displacement of the anterior vermis superiorly. anomaly. Based on their observation that the two cerebellar anlagen fused long before the development of the outlet foramina, they concluded that atresia of the outlet foramina of the fourth ventricle could not be a causative factor, thus refuting the opinion of Hess and Retzios. Despite the difficulty in postulating the sequence of embryological events that leads to the Dandy-Walker malformations found at autopsy, many authors have attempted to establish the time of intrauterine insult by linking the syndrome to the anomalies that are frequently associated with it. Hart, et al., e in their review of 28 cases, noted associated congenital defects in 68% of their patients. Principal among these was polydactylism, which suggested that the insult occurred before the eighth week of intrauterine life, since the digits of both hands and feet are clearly defined by this time. A cleft palate was found in two of their patients, as was seen in our first patient. In normal individuals, fusion of the palate is complete by the 12th week of life. Gardner, et al., 5 point out that myelomeningocele rarely occurs in conjunction with the Dandy-Walker complex. This finding suggests that the Dandy-Walker anomaly originates at a later time than does the Arnold-Chiari malformation, which is thought to arise during the fourth to fifth week of life if the neural tube fails to close. Probably the most frequent of all the anomalies associated with the Dandy-Walker syndrome is agenesis of the corpus callosum. Development of the corpus callosum begins at about 3 months of gestational age? The outlet foramina of the fourth ventricle, however, do not normally become completely patent until the fourth month of fetal life. Thus, it seems unlikely that hydrocephalus is a causative factor in preventing the early development of the corpus callosum. FIG. 4. Case 2. Left: Section of medulla at the level of the inferior olivary nucleus with conspicuous absence of the left corticospinal tract and hypertrophy on the right. Right." Lower thoracic cord with large right pyramidal tract running in the ventralfuniculi. H & E, 6. J. Neurosurg. / Volume 50 / March,
5 R. L. Lagger According to Humphrey/ corticospinal axons in humans decussate during the 16th and 17th weeks of gestation. On the basis of the finding in our second case that the pyramidal tract had not undergone decussation, we may roughly date the embryonic insult to a gestation time before the 16th week. Although midline anomalies frequently accompany the Dandy-Walker syndrome, abnormalities of the pyramidal tracts are distinctly uncommon. D'Agostino and colleagues 8 reported that only one of their 10 patients had no medullary pyramids, and no other reports appear in the literature. Indeed, failure of the corticospinal tract to decussate at the pyramids very rarely occurs in human beings. According to Nyberg-Hansen and Rinvik, TM Zenner 17 reported a poorly documented case of acute left hemiplegia in an adult. The subsequent autopsy on this patient revealed a complete absence of pyramidal decussation and a gliosarcoma in the left cerebral hemisphere extending over the central gyrus? 2a7 Verhaart and Kramer le mentioned four cases of total non-decussation, three of which zccurred in neonates with large encephaloceles that involved the motor areas of one hemisphere; in each case the corticospinal tracts were found in the anterior funiculi, and no lateral cortical spinal tracts were evident. Their fourth case was an adult Chinese man who died of a progressive and generalized motor system disease, but had evidenced no neurological signs that could be attributed to the pyramidal non-decussation found at autopsy. This patient, too, had large anterior funiculi and no lateral corticospinal tracts. The pyramids and anterior funiculi in all these cases were asymmetrical. The authors concluded that such differences in fiber content, as well as differences in the time of arrival of the corticospinal axons at the cervicomedullary junction, were essential factors in preventing pyramidal decussation? 6 Luhan ~1 reported a bizarre case of a stab wound in the right pontomedullary region of a 27-year-old man, who recovered from the injury but had severe neurological deficits, including a left spastic hemiplegia. When this patient died 6 years later, it was found that the wound had penetrated the right pyramid at the pontomedullary conjunction. At the level of the rostral medulla, there was complete demyelination and atrophy of the right pyramid. According to his report, "relatively few" corticospinal fibers crossed at the cervicomedullary junction. In the cervical cord, the right anterior funiculus showed demyelination and atrophy, whereas the opposite anterior funiculus showed "no discrete area of demyelination;" in the thoracolumbar cord, this pattern of ipsilateral degeneration persisted. Silver stains demonstrated an associated loss of axons in the demyelinated zones. The presence of left spastic hemiplegia, therefore, implied that there was a terminal crossing of corticospinal axons in the right anterior funiculus to the interneuronal or anterior horn cell synapses in the left side of the cord. n Similarly, in our second case, there was a right hemiplegia with preservation of the right anterior corticospinal tract. Some form of decussation, perhaps of individual corticospinal axons at all levels of the cord with inner neuronal or anterior horn cell synapses in the left side of the cord, must be postulated to explain the preservation of left-sided motor function. Clearly, many of the central nervous system and systemic anomalies, including those frequently associated with the Dandy-Walker syndrome, are known to develop very early in embryonic life, long before the foramina of Luschka and Magendie normally open. The plethora of anomalies associated with the Dandy-Walker syndrome suggest a complex, possibly cascading, pattern of malformations, the exact pathogenesis of which remains obscure. Indeed, the intrauterine insult, whether genetic or teratogenic, may extend from the sixth week to the end of the fourth month of intrauterine life. It is difficult to ascertain whether or not the failure of pyramidal tract decussation is directly related to the Dandy-Walker syndrome, but the simultaneous development of the pyramids and the opening of the outlet foramina of the fourth ventricle makes this idea particularly attractive. Acknowledgment The author expressly wishes to thank Dr. Lucien J. Rubenstein for the case material presented and for his personal assistance in preparation of the manuscript. References 1. Benda CE: The Dandy-Walker syndrome or the so, called atresia of the foramen of Magendie. J Neuropathol Exp Neurol 13:14-29, Brodal A, Hauglie-Hanssen E: Congenital hydrocephalus with defective development of the cerebellar vermis (Dandy-Walker syndrome). Clinical and anatomical findings in two cases with particular reference to the so-called atresia of the foramina of Magendie and Luschka. J Neurol Neurosurg Psychiatry 22:99-108, D'Agostino AN, Kernohan JW, Brown JR: The Dandy- Walker syndrome. J Neuropathnl Exp Neurol 22: , Dandy WE, Blackfan KD: Internal hydrocephalus. An experimental, clinical and pathological study. Am J Dis Child 8: , Gardner E, O'Rahilly R, Prolo D: The Dandy-Walker and Arnold-Chiari malformations. Clinical, developmental, and teratological considerations. Arch Neuroi 32: , Hart MN, Malamud N, Ellis WG: The Dandy-Walker syndrome. A clinicopathological study based on 28 cases. Neurology 22: , Hess C: Das Foramen Magendie und die Oeffnungen an den Recessus lateralis des iv. Ventrikels. Morphol Jahrh 10: , Humphrey T: The development of the pyramidal tracts in human fetuses. Correlated with cortical differentiation, in Tower DB, Schade JP (eds): Proceedings of the Second International Meeting of Nenrobioingists, 386 J. Neurosurg. / Volume 50 / March, 1979
6 Uncrossed pyramidal tracts Amsterdam, Structure and Function of the Cerebral Cortex. Amsterdam: American Elsevier, 1960, pp Kirschbaum WR: Agenesis of the corpus callosum and associated malformations. J Neuropathol Exp Neurol 6:78-94, Koelliker A: Handbueh tier Gewebelehre des Menschen. Leipzig: Wilhelm Englemann, Luhan JA: Long survival after unilateral stab wound of medulla with unusual pyramidal tract distribution. Arch Neurol 1: , Nyberg-Hansen R, Rinvik E: Some comments on the pyramidal tract, with special reference to its individual variations in man. Acta Neurol Stand 39:1-30, Retzios G: Das Mensehenhirn. Studien in der Makroskopischen Morphologie. Stockholm: PA Norstedt and S~ner, Schlapp MG, Gere B: Occlusion of the aqueduct of Sylvius in relation to internal hydrocephalus. Am J Dis Child 13: , Taggert JK Jr, Walker AE: Congenital atresia of the foramens of Luschka and Magendie. Arch Neurol Psychiatry 48: , Verhaart WJC, Kramer W: Uncrossed pyramidal tract. Acta Psychiatr Neurol Scand 27: , Zenner P: Ein Fall yon Hirngeschwulst in der linken motorischen Sph~ire, linkseitger L~ihmung, Abwesenheit der Pyramidenkreuzung. Neurologisch Zentralbl 17: , 1898 This work was supported in part by Graduate Neuropathology Training Grant 5T01-NS from the National Institute of Neurological and Communicative Disorders and Stroke, USPHS. Address reprint requests to: Raymond L. Lagger, M.D., Department of Neurological Surgery, University of California School of Medicine, San Francisco, California J. Neurosurg. / Volume 50 / March,
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