:Acta NTeuroch
Acta Neurochir (Wien) (1992): 116: 147-149
.
. rurglca
9 Springer-Verlag 1992 Printed in Austria
Tumours of the Limbic and Paralimbic System* M. G. Yasargil 1 and J. D. Reeves 2 1Department of Neurosurgery, Universit/itsspital, Ziirich, Switzerland and 2 Department of Neurosurgery, School of Medicine, Louisiana State University, New Orleans, LA, U.S.A.
Summary 240 patients with tumours of the limbic and paralimbic areas are presented. The following turnout growth patterns have been observed: - they remain isolated to areas within the allocortex; - they spread throughout allocortical regions; - they spread from allocortical to mesocortical zones. With the exeption of advanced malignant turnouts there seems to be a tendency for tumours to spare the adjacent neocortical and medial structures. The tumours can be approached and extirpated using the transSylvian approach and microneurosurgical technique. 56% have been histologically benign. 60% were below 40 years of age. Seizures were the leading manifestation (77%). In 95% the postoperative results were good. There was no peri-operative mortality.
Keywords: Tumours; limbic system; paralimbic system; symptoms; operative management; results.
This paper presents the preliminary observations and results of 240 patients with tumours of the limbic and paralimbic areas. They represent a subset of approximately 1500 patients with brain tumours operated upon using microneurosurgical techniques at the Universitfitsspital, Zfirich, during the past two decades. They display a remarkable set of common features and deserve recognition as a distinct variety of cerebral tumours. As described by neuro-anatomists and behavioural neurologists, the limbic (def: girdle) system comprises those structures interposed between the diencephalon and the massive cerebral hemispheres. In 1878, Broca described this large convolution on the medial surface of the hemisphere and suggested the term "le grande lobe limbique ''1. Interest in its neural connections heightened in 1937 when Papez theorized that it played a role in emotional behaviour 9. In 1952, McLean sug* Invited Lecture presented at the European Congress of Neurosurgery, Moscow, June 23-29, 1991
gested the term "limbic system" as a designation for the limbic cortex and the brain stem structures with which it has primary connections 4. Limbic system structures appear very early in mammalian evolution. The phylogenetically older limbic system assumes a position on the medial and basal surface of the hemisphere during the complex sequence of events that leads to the final topographic structure of the human brain. The architectonic features of the cortical layers increase in complexity as one moves from these phylogenetically older areas to newer ones. Using regional differences in neuronal and myelin architecture and "connectivity", anatomists have divided the entire cortical mantle into subtypes which display a gradual increase in structural complexity and differentiation. Limbic areas display the most primitive cortex, exhibiting microscopic cortical layering that ranges from a pattern of no definite lamination (septal regions, substantia innominata, and amygdala) to twolayered cortex (hippocampal and piriform cortex). Collectively, these areas are called allocortex. Paralimbie structures display three to five layered cortex and are known as mesocortex. These anatomical areas include the caudal orbitofrontal cortex, insula, temporal pole, parahippocampal gyri, and cingulate gyri. The mesocortex is interposed anatomically and connectively between the allocortex and neoeortex 5. One is referred to the excellent monograph by Mesulam for detailed descriptions and functional implications of this arrangement. Additional articles regarding cortical phylogeny and architectonics can be found in the writings of Klingler 3, Pandya 7, 8, and Mesulam 6. This gross and microscopic model of the limbic system serves as a useful model on which to build our surgical observations. A variety of tumour growth patterns have been observed. The tumours have been noted
148
M.G. Ya~argil and J. D. Reeves: Tumours of the Limbic and Paralimbic System
to remain isolated to areas within the allocortex (e.g., amygdala, hippocampus), spread throughout allocortical regions (e.g., from hippocampal to amygdala and parahippocampus), or spread from allocortical to mesoeortical zones (e.g. insula to orbitofrontal cortex and temporal pole). Extreme examples of tumour extension within the limbic/paralimbic system include 2 cases of extension of glioma along the pathway from hippocampus to fornix to mammillary bodies and anterior structures, and of the entire limbic/paralimbic belt seen unilaterally in one case, bilaterally in another. These cases highlight a curious phenomenon observed in all but the most advanced malignant tumours, i.e., a propensity to spread within the confines of these allocortieal/mesocortical zones while sparing the adjacent neocortical areas and medial structures such as the claustrum, putamen, paltidum, and internal capsule. This suggests an affinity of these tumours for the phylogenetically primitive zones, an idea which was introduced by Filiminoff in 19472 and later developed by Yakovlev in 19591~ However, this concept has received little attention in the tumour literature. Examples of these tumour types are shown in the radiographs 13. Many of these tumours would be deemed inoperable by most neurosurgeons. Careful review of these radiographs reveals the capability, using microsurgical techniques, for complete removal of these tumours. All procedures have been performed using the interfascial pterional craniotomy 11. These tumours can be approached and extirpated via the transSylvian approach without recourse to cortical incision in the superficial layers or temporal lobectomy. A detailed description of the operative approach to the insula and amygdala/hippocampus has been previously published 12, although modifications to this operation are necessary when extirpating tumours. Tumours ranged in size from less than 2cm to greater than 10 cm, with 67% being greater than 5 cm in diameter. The majority of the tumours were leftsided (53%) and histologically benign (56%). Unlike most large series of primary brain tumours, the majority of patients in this particular series were young. Sixty per cent were below forty years of age. Seventyeight per cent of the patients less than thirty had benign histologies. Pre-operatively, the overwhelmingly most common symptom which brought patients to medical attention was a seizure, present in 77% of the group. Approximately 80% of the seizures were partial, with
or without secondary generalization. Despite the proximity to the brain stem, internal capsule, and optic pathways, these large tumours did not cause symptoms other than seizure in 46% of patients, even in the presence of midline shift and herniation. Among the patients with " h a r d " neurological deficit, those with malignant turnouts predominated. Postoperatively, 95 % of the patients were placed in the " g o o d " category. They had no or very minor deficits which did not interfere with their activities of daily living. They were able to return home, function independently, and, in many cases, return to school or work. No patients required extended hospital or nursing care. There were no peri-operative deaths. This series has demonstrated the efficacy of highly skilled microsurgical attack on these tumours. There have been no peri-operative deaths and minimal postoperative complications. Benign tumour patients, who are young and thus with full-working capacity, have benefitted most. The vast majority of patients have enjoyed a good outcome.
References 1. Broca P (1878) Anatomie compar~e des circonvolutionsc~r6brales. Le grand lobe limbique et la scissure limbique dans la s6rie des mammifbres. Rev Anthrop 1:385-498 2. FiliminoffIN (1947) A rational subdivision of the cerebralcortex. Arch Neurol Psychiatry 58:296-311 3. KlinglerJ, Gloor P (1960)The connectionsof the amygdalaand of the anterior temporal cortex in human brain. J Comp Neurol 115:333-369 4. McLean P (1952) Some psychiatricimplications of physiologic studies on frontotemporalportion of the limbic system(visceral brain). ElectroencephalogrClin Neurophysiol4:407-418 5. MesulamM (1985)Patterns in behaviouralanatomy:association areas, the limbic system, and hemispheric specialization. In: Mesulam M (ed) Principles of behavioural neurology. F. A. Davis, Philadelphia, pp 1-70 6. Mesulam M, Mufson EJ (1985)The Insula of Reil in Man and monkey-architectonics, connectivity, and function. In: Jones EG, Peters AA (eds) Cerebralcortex. PlenumPress, New York, pp 179ff 7. Pandya DN, van Hoesen GW, Domesick V (1973) A cinguloamygdaloid projection in the rhesus monkey. Brain Res 61: 369-373 8. Pandya DN, van Hoesen GW, Mesniam M (1981)Efferentconnections of the cingulategyrus in the rhesus monkey.Exp Brain Res 42:319-330 9. Papez J (1937)A proposed mechanismof emotion.Arch Neurol Psychiatry 38:725-743 I0. YakovlevPI (1959)Pathoarchitectonicstudies of cerebral malformations. J Neuropath Exp Neurol 18:22-55
M. G. Yasargil and J. D. Reeves: Tumours of the Limbic and Paralimbic System 11. Ya~argil MG, Smith RD, Young PH, et al (1984) Interfascial pterional craniotomy. In: Ya~argil MG (ed) Microneurosurgery, Vol 1. Thieme, Stuttgart New York, pp 215-233 12. Ya~argil MG, Teddy PJ, Roth P (1985) Selective amygdalohippocampeetomy-operative anatomy and surgical technique. In: Symon I etal (eds) Advances and technical standards in neurosurgery, Vo112. Springer, Wien New York, pp 93-123
149
13. Ya~argil MG, Reeves JD, Cavazos E, Doczi T, von Ammon K: Tumours of the limbic and paralimbic systems (in press)
Correspondence and Reprints: M. Gazi Ya~argil, M.D., Professor and Chairman, Department of Neurosurgery, University Hospital of Ziirich, RLmistraBe 100, CH-8091 Ziirich, Switzerland.
Acta Neurochir (Wien) (1992): 116: 147-149
.
. rurglca
9 Springer-Verlag 1992 Printed in Austria
Tumours of the Limbic and Paralimbic System* M. G. Yasargil 1 and J. D. Reeves 2 1Department of Neurosurgery, Universit/itsspital, Ziirich, Switzerland and 2 Department of Neurosurgery, School of Medicine, Louisiana State University, New Orleans, LA, U.S.A.
Summary 240 patients with tumours of the limbic and paralimbic areas are presented. The following turnout growth patterns have been observed: - they remain isolated to areas within the allocortex; - they spread throughout allocortical regions; - they spread from allocortical to mesocortical zones. With the exeption of advanced malignant turnouts there seems to be a tendency for tumours to spare the adjacent neocortical and medial structures. The tumours can be approached and extirpated using the transSylvian approach and microneurosurgical technique. 56% have been histologically benign. 60% were below 40 years of age. Seizures were the leading manifestation (77%). In 95% the postoperative results were good. There was no peri-operative mortality.
Keywords: Tumours; limbic system; paralimbic system; symptoms; operative management; results.
This paper presents the preliminary observations and results of 240 patients with tumours of the limbic and paralimbic areas. They represent a subset of approximately 1500 patients with brain tumours operated upon using microneurosurgical techniques at the Universitfitsspital, Zfirich, during the past two decades. They display a remarkable set of common features and deserve recognition as a distinct variety of cerebral tumours. As described by neuro-anatomists and behavioural neurologists, the limbic (def: girdle) system comprises those structures interposed between the diencephalon and the massive cerebral hemispheres. In 1878, Broca described this large convolution on the medial surface of the hemisphere and suggested the term "le grande lobe limbique ''1. Interest in its neural connections heightened in 1937 when Papez theorized that it played a role in emotional behaviour 9. In 1952, McLean sug* Invited Lecture presented at the European Congress of Neurosurgery, Moscow, June 23-29, 1991
gested the term "limbic system" as a designation for the limbic cortex and the brain stem structures with which it has primary connections 4. Limbic system structures appear very early in mammalian evolution. The phylogenetically older limbic system assumes a position on the medial and basal surface of the hemisphere during the complex sequence of events that leads to the final topographic structure of the human brain. The architectonic features of the cortical layers increase in complexity as one moves from these phylogenetically older areas to newer ones. Using regional differences in neuronal and myelin architecture and "connectivity", anatomists have divided the entire cortical mantle into subtypes which display a gradual increase in structural complexity and differentiation. Limbic areas display the most primitive cortex, exhibiting microscopic cortical layering that ranges from a pattern of no definite lamination (septal regions, substantia innominata, and amygdala) to twolayered cortex (hippocampal and piriform cortex). Collectively, these areas are called allocortex. Paralimbie structures display three to five layered cortex and are known as mesocortex. These anatomical areas include the caudal orbitofrontal cortex, insula, temporal pole, parahippocampal gyri, and cingulate gyri. The mesocortex is interposed anatomically and connectively between the allocortex and neoeortex 5. One is referred to the excellent monograph by Mesulam for detailed descriptions and functional implications of this arrangement. Additional articles regarding cortical phylogeny and architectonics can be found in the writings of Klingler 3, Pandya 7, 8, and Mesulam 6. This gross and microscopic model of the limbic system serves as a useful model on which to build our surgical observations. A variety of tumour growth patterns have been observed. The tumours have been noted
148
M.G. Ya~argil and J. D. Reeves: Tumours of the Limbic and Paralimbic System
to remain isolated to areas within the allocortex (e.g., amygdala, hippocampus), spread throughout allocortical regions (e.g., from hippocampal to amygdala and parahippocampus), or spread from allocortical to mesoeortical zones (e.g. insula to orbitofrontal cortex and temporal pole). Extreme examples of tumour extension within the limbic/paralimbic system include 2 cases of extension of glioma along the pathway from hippocampus to fornix to mammillary bodies and anterior structures, and of the entire limbic/paralimbic belt seen unilaterally in one case, bilaterally in another. These cases highlight a curious phenomenon observed in all but the most advanced malignant tumours, i.e., a propensity to spread within the confines of these allocortieal/mesocortical zones while sparing the adjacent neocortical areas and medial structures such as the claustrum, putamen, paltidum, and internal capsule. This suggests an affinity of these tumours for the phylogenetically primitive zones, an idea which was introduced by Filiminoff in 19472 and later developed by Yakovlev in 19591~ However, this concept has received little attention in the tumour literature. Examples of these tumour types are shown in the radiographs 13. Many of these tumours would be deemed inoperable by most neurosurgeons. Careful review of these radiographs reveals the capability, using microsurgical techniques, for complete removal of these tumours. All procedures have been performed using the interfascial pterional craniotomy 11. These tumours can be approached and extirpated via the transSylvian approach without recourse to cortical incision in the superficial layers or temporal lobectomy. A detailed description of the operative approach to the insula and amygdala/hippocampus has been previously published 12, although modifications to this operation are necessary when extirpating tumours. Tumours ranged in size from less than 2cm to greater than 10 cm, with 67% being greater than 5 cm in diameter. The majority of the tumours were leftsided (53%) and histologically benign (56%). Unlike most large series of primary brain tumours, the majority of patients in this particular series were young. Sixty per cent were below forty years of age. Seventyeight per cent of the patients less than thirty had benign histologies. Pre-operatively, the overwhelmingly most common symptom which brought patients to medical attention was a seizure, present in 77% of the group. Approximately 80% of the seizures were partial, with
or without secondary generalization. Despite the proximity to the brain stem, internal capsule, and optic pathways, these large tumours did not cause symptoms other than seizure in 46% of patients, even in the presence of midline shift and herniation. Among the patients with " h a r d " neurological deficit, those with malignant turnouts predominated. Postoperatively, 95 % of the patients were placed in the " g o o d " category. They had no or very minor deficits which did not interfere with their activities of daily living. They were able to return home, function independently, and, in many cases, return to school or work. No patients required extended hospital or nursing care. There were no peri-operative deaths. This series has demonstrated the efficacy of highly skilled microsurgical attack on these tumours. There have been no peri-operative deaths and minimal postoperative complications. Benign tumour patients, who are young and thus with full-working capacity, have benefitted most. The vast majority of patients have enjoyed a good outcome.
References 1. Broca P (1878) Anatomie compar~e des circonvolutionsc~r6brales. Le grand lobe limbique et la scissure limbique dans la s6rie des mammifbres. Rev Anthrop 1:385-498 2. FiliminoffIN (1947) A rational subdivision of the cerebralcortex. Arch Neurol Psychiatry 58:296-311 3. KlinglerJ, Gloor P (1960)The connectionsof the amygdalaand of the anterior temporal cortex in human brain. J Comp Neurol 115:333-369 4. McLean P (1952) Some psychiatricimplications of physiologic studies on frontotemporalportion of the limbic system(visceral brain). ElectroencephalogrClin Neurophysiol4:407-418 5. MesulamM (1985)Patterns in behaviouralanatomy:association areas, the limbic system, and hemispheric specialization. In: Mesulam M (ed) Principles of behavioural neurology. F. A. Davis, Philadelphia, pp 1-70 6. Mesulam M, Mufson EJ (1985)The Insula of Reil in Man and monkey-architectonics, connectivity, and function. In: Jones EG, Peters AA (eds) Cerebralcortex. PlenumPress, New York, pp 179ff 7. Pandya DN, van Hoesen GW, Domesick V (1973) A cinguloamygdaloid projection in the rhesus monkey. Brain Res 61: 369-373 8. Pandya DN, van Hoesen GW, Mesniam M (1981)Efferentconnections of the cingulategyrus in the rhesus monkey.Exp Brain Res 42:319-330 9. Papez J (1937)A proposed mechanismof emotion.Arch Neurol Psychiatry 38:725-743 I0. YakovlevPI (1959)Pathoarchitectonicstudies of cerebral malformations. J Neuropath Exp Neurol 18:22-55
M. G. Yasargil and J. D. Reeves: Tumours of the Limbic and Paralimbic System 11. Ya~argil MG, Smith RD, Young PH, et al (1984) Interfascial pterional craniotomy. In: Ya~argil MG (ed) Microneurosurgery, Vol 1. Thieme, Stuttgart New York, pp 215-233 12. Ya~argil MG, Teddy PJ, Roth P (1985) Selective amygdalohippocampeetomy-operative anatomy and surgical technique. In: Symon I etal (eds) Advances and technical standards in neurosurgery, Vo112. Springer, Wien New York, pp 93-123
149
13. Ya~argil MG, Reeves JD, Cavazos E, Doczi T, von Ammon K: Tumours of the limbic and paralimbic systems (in press)
Correspondence and Reprints: M. Gazi Ya~argil, M.D., Professor and Chairman, Department of Neurosurgery, University Hospital of Ziirich, RLmistraBe 100, CH-8091 Ziirich, Switzerland.
