ACTA NEUROCHIRURGICA 9 by Springet-Verlag 1978
Acta Neurochirurgica 45, 133--145 (1978)
Departments of Neurosurgery and Pathology, Ciudad Sanitaria "1 ~ de Octubre", Madrid, Spain
M u l t i p l e Inttacranial Arterial O c c l u s i o n s ( M o y a m o y a D i s e a s e ) in Patients With N e u r o f i b r o m a t o s i s One Case Report With Autopsy By
E. Lamas, R. Diez Lobato, A. Cabello, and J. M. Abad With 6 Figures
Summary The authors report two cases of multiple intracranial arteriaI occlusive disease occurring in patients affected by neurofibromatosis. Clinicoradiological presentation was, in both cases, typical of the so-called Moyamoya disease. Special emphasis on the anatomopathologicat necropsy findings in the second case is made, because, to the authors' knowledge, this is the first reported case in the literature. Cases of the so-called M o y a m o y a disease started to be reported in 1961 ~3. The disease, which is not exclusive to the Japanese race, but also occurs in Caucasians and Negroes, has been reported under various names 12, 14, 16, 20, 25, ~2, 34 Both the clinical and angiographic pictures of this condition have been repeatedly discussed in the literature, and are w e l l - k n o w n 1~, 13, 14, 16, 17, 20, 21, 2~, ~5, 32, 33 H o w ever, its aetiology and p a t h o l o g y are still unclear. The onset of the clinical symptoms in patients with M o y a m o y a disease is most p r o b a b l y before 20 years of age, and females are more frequently affected than males 12, 16, is, 20, ~2, 34 Sudden presentation of focal m o t o r deficit of rapid onset convulsions, and visual disturbances, are the common manifestations in younger people 16, 2o while subarachnoid haemorrhage is the most frequent method of onset in patients over 20 years of age 16, 18, 2% The majority of the cases run a remitting course, and only occasionally do the patients get progressively worse, or die 20, 3~, 34 0001-6268/78/0045/0133/$ 02.60
134
E. Lamaset
al.:
The most characteristic angiographic finding in Moyamoya disease is bilateral stenosis or complete occlusion of the supractinoid carotid artery associated with a large network of fine vessels in the region of the basal ganglia 12, 13, 16, s0, 2a, 2.~, as, aa Other sources of collateral circuiado~ for the ~sdxaemic areas are [eptome~ingea[ end-to-end anastomoses, particularly between the posterior cerebral artery and the anterior and middle cerebral arteries ~z, ~a Transdnral anastomoses between extracranial and intracranial arteries (rete mirabile) usually develop, and these are wider in cases in which basilar artery occlusion is present 12, so, a2, 34 Nevertheless, the vertebrobasilar tree and the posterior cerebral arteries are rarely involved by the disease. Sometimes cerebral arteries are segmentally stenosed or occluded 12, la Most authors disagree with the idea that Moyamoya disease is a form of congenital hypoplasia of the intracranial vessels associated with basal haemangiomatous malformation 3, l~. la, 14, 16, 27, 812, a4, 61 More probably it is an acquired disorder, and the abnormal vascular network in the basal region of the brain develops as a collateral circulation secondary to the stenosis of the internal carotid arteries 34. Besides a congenital origin other aetlologies have been considered, such as arteriosclerosis, trauma, and non-specific inflammation 13, 27. 32, a4 Arteriosclerosis does not seem to play a significant role because of the age distribution of the reported cases, and there is nothing in the few autopsy cases reported in this condition to indicate an inflammatory origin *, a, i4, 17, 20, 2=, 2~, as, 40 Multiple nonspecific factors such meningitis la, 21, embolism ,a, neurocutaneous syndromes 13, si&le cell anaemia a*, collagen disease 6 teEralogy of Fallot 2,, and overtransfusion 21, have been recogaized as producing internal carotid stenosis or occlusion, with associated vascular networks in the basa~ ~eg{on of "~he brain. The almost universal finding of internal carotid narrowing below the point of stenosis has been attributed by some authors to true carotid hypoplasia ~7. 20. 4o and related by others to the amount of diminished flow through the artery 3~. That the disease is an evolving condition has clinical as well as angiographic support 12, as, a4 Nevertheless, many factors point to the congenital ba&ground of the disease ~4, ,6, 20, 25, as, 36 Among them are its preference for the Japanese race, the usual symmetrical involvement of the internal carotid arteries, the similarity between its angiographic appearance and the cerebral vascular tree in the human 11-16 mm embryo, and its association with some neurocutaneous syndromes and congenital vascular anomalies such as intracavernous aneurysms 6, persistent trigeminal arteries and primitive carotid-basilar anastomoses 12. Finally, the familial occurrence of the disease has also been reported 2%
Multiple Intracranial Arterial Occlusions in Patients
135
Case Reports Case 1. This 9-years-old girl with a history of chronic mental retardation suffered during the year before admission from repeated left focal motor fits, followed by transitory hemiparesis. During this period she also complained of frontal non-specific headaches. She had two brothers in good health, and there was no family history of seizures or neurofibromatosis. Physical examination: extensive "caf6 au lair" spots were present on the chest, perineal region, and thighs. Smaller, but similar, spots were profusely disseminated over the body. The left upper and lower limbs were shorter than the right by 2 and 4 cm respectively. The rest of the physical examination was within normal
Fig. 1. Case 1. Right common carotid angiography. Internal carotid artery is occluded at supraclinoid level. Enlarged posterior cerebral and anterior choroidal arteries giving leptomeningeal anastomoses to the anterior and middle cerebral arteries. Retrograde filling of these last arteries via posterior pericallosal artery (small double arrows) and anterior choroidal artery (small arrow), may be appreciated. The vascular network above carotid stenosis is clearly seen (big arrow) limits. Routine blood and urine test were normal. LE preparations and VDRL were negative. LCR examination was normal. EEG showed a right frontoparietaI slow wave focus. A pre-excitation anomaly of LGL type (short PR without delta wave), was detected in the ECG. Plain skull films showed an absence of the left innominnate line. A right common carotid angiogram revealed an occlusion of the supraclinoid internal carotid artery with an associated vascular network localized in the basal region of the brain. Distal branches of the hypertrophied posterior cerebral and anterior choroidal arteries anastomosed, via leptomeningeal connections, with the anterior and middle cerebral arteries. There were also signs of hydrocephalus (Fig. 1). The left common carotid angiogram showed similar findings, but the transdural external-internal anastomoses were more obvious. Two segmental occlusions of the anterior cerebral artery were seen. Vertebrobasilar
136
E. Lamas et al.:
Fig. 2. Case 2. Upper: right common carotid angiography; A-P and lateral projections. Internal carotid artery is partially obstructed at supraclinoid level. Basal telangiectasia (big arrow) and enlargement of both the ophthalmic and anterior ethmoidal (small arrows) arteries may be seen. Lower: left common carotid angiography; A-P and lateral projections. Infraclinoid carotid artery has a diminished calibre. Supraclinoid carotid artery is severely stenosed (big arrow). Basal telangiectasia and an enlarged anterior falx artery (small arrows), may be seen arteriography was normal. Pneumoencephalography showed communicating hydrocephalus with considerable cortico-subcortical atrophy. Continuous monitoring of the intraventricular pressure and the result of an infusion manometric test were consistent with the diagnosis of hydrocephalus "ex vacuo". The patient was treated with primidone, and recommended for psychological studies.
Multiple Intracranial Arterial Occlusions in Patients
137
Case 2. This 50-years-old normotensive man suddenly presented twenty four hours before admission with a frontonuchal headache followed by convulsions of the left limbs and left hemiplegia. When he was being examinated in the emergency room, the headache increased, generalized convulsions occurred, and the patient
Fig. 3. Upper: seriography of the two posterior thirds of the left cerebral hemisphere injected with Micropaque. Posterior cerebral artery (small arrows), and its branches, among them the posterior pericallosal artery (footed arrows) are shown. Basal telangiectasia (bigger arrows), may also be seen. Lower: postmortem preparation of the left internal carotid tree. Stenosis of the proximal segments of both the anterior and middle cerebral arteries (footed arrows), is shown. Filiform anastomotic connections between the lenticulostriated arteries (arrows), may be seen became unconscious with bilateral decerebrate rigidity. Spinal tap revealed a haemorrhagic CSF. Right common carotid angiography was performed revealing an incomplete occlusion of the supraclinoid carotid artery with an associated vascular network in the base of the brain. The ophthalmic artery, which was hypertrophied, fed a large anterior ethmoidal artery. There was a midline shift
138
E. Lamas et aL: Multiple IntracraniaI Arterial Occlusions in Patients
(Fig. 2). Left common carotid angiography showed similar findings. The ophthalmic artery was also markedly hypertrophied on this side, feeding an enlarged anterior falx artery (Fig. 2). Vertebrobasilar arteriography was not performed. The patient died several hours after carotid angiography. Necropsy Study: Multiple "caf~ au laW' spots were present all over the body, but mostly on the back. Numerous small subcutaneous nodules were also found on the trunk and limbs. The viscera were grossly unremarkable. A diffuse sub-
Fig. 4. Coronal sections of the brain at parieto-occipital level. Intracerebral haematoma in the right centrum semiovale inundating the ventricular system arachnoid haemorrhage covered both the convexity and the base of the brain Bilateral Micropaque perfusions of the carotid and vertebral arteries were perJ formed before formalin fixation. The fixed brain weighed 1,720 g. It was markedly swollen, showing diffuse gyral flattening and a larger right cerebral hemisphere. Bilateral nncal herniation, more prominent on the right side, was present. There was not a trace of atheromatosis in the vessels of the circle of Willis at naked eye inspection. Both intrapetrosal segments of the internal carotid arteries showed concentric luminal stenosis (about 50~ and these arteries appeared hypoplastic at supraclinoid level without luminal stenosis. The left middle cerebral artery also showed concentric luminal stenosis (about 30~ Both
Fig. 5. A) Intrapetrosal segment of the left internal carotid artery. Diffuse hyperplasia of the intimal layer producing luminal stenosis (PAS-Orcein 5
Acta Neurochirurgica 45, 133--145 (1978)
Departments of Neurosurgery and Pathology, Ciudad Sanitaria "1 ~ de Octubre", Madrid, Spain
M u l t i p l e Inttacranial Arterial O c c l u s i o n s ( M o y a m o y a D i s e a s e ) in Patients With N e u r o f i b r o m a t o s i s One Case Report With Autopsy By
E. Lamas, R. Diez Lobato, A. Cabello, and J. M. Abad With 6 Figures
Summary The authors report two cases of multiple intracranial arteriaI occlusive disease occurring in patients affected by neurofibromatosis. Clinicoradiological presentation was, in both cases, typical of the so-called Moyamoya disease. Special emphasis on the anatomopathologicat necropsy findings in the second case is made, because, to the authors' knowledge, this is the first reported case in the literature. Cases of the so-called M o y a m o y a disease started to be reported in 1961 ~3. The disease, which is not exclusive to the Japanese race, but also occurs in Caucasians and Negroes, has been reported under various names 12, 14, 16, 20, 25, ~2, 34 Both the clinical and angiographic pictures of this condition have been repeatedly discussed in the literature, and are w e l l - k n o w n 1~, 13, 14, 16, 17, 20, 21, 2~, ~5, 32, 33 H o w ever, its aetiology and p a t h o l o g y are still unclear. The onset of the clinical symptoms in patients with M o y a m o y a disease is most p r o b a b l y before 20 years of age, and females are more frequently affected than males 12, 16, is, 20, ~2, 34 Sudden presentation of focal m o t o r deficit of rapid onset convulsions, and visual disturbances, are the common manifestations in younger people 16, 2o while subarachnoid haemorrhage is the most frequent method of onset in patients over 20 years of age 16, 18, 2% The majority of the cases run a remitting course, and only occasionally do the patients get progressively worse, or die 20, 3~, 34 0001-6268/78/0045/0133/$ 02.60
134
E. Lamaset
al.:
The most characteristic angiographic finding in Moyamoya disease is bilateral stenosis or complete occlusion of the supractinoid carotid artery associated with a large network of fine vessels in the region of the basal ganglia 12, 13, 16, s0, 2a, 2.~, as, aa Other sources of collateral circuiado~ for the ~sdxaemic areas are [eptome~ingea[ end-to-end anastomoses, particularly between the posterior cerebral artery and the anterior and middle cerebral arteries ~z, ~a Transdnral anastomoses between extracranial and intracranial arteries (rete mirabile) usually develop, and these are wider in cases in which basilar artery occlusion is present 12, so, a2, 34 Nevertheless, the vertebrobasilar tree and the posterior cerebral arteries are rarely involved by the disease. Sometimes cerebral arteries are segmentally stenosed or occluded 12, la Most authors disagree with the idea that Moyamoya disease is a form of congenital hypoplasia of the intracranial vessels associated with basal haemangiomatous malformation 3, l~. la, 14, 16, 27, 812, a4, 61 More probably it is an acquired disorder, and the abnormal vascular network in the basal region of the brain develops as a collateral circulation secondary to the stenosis of the internal carotid arteries 34. Besides a congenital origin other aetlologies have been considered, such as arteriosclerosis, trauma, and non-specific inflammation 13, 27. 32, a4 Arteriosclerosis does not seem to play a significant role because of the age distribution of the reported cases, and there is nothing in the few autopsy cases reported in this condition to indicate an inflammatory origin *, a, i4, 17, 20, 2=, 2~, as, 40 Multiple nonspecific factors such meningitis la, 21, embolism ,a, neurocutaneous syndromes 13, si&le cell anaemia a*, collagen disease 6 teEralogy of Fallot 2,, and overtransfusion 21, have been recogaized as producing internal carotid stenosis or occlusion, with associated vascular networks in the basa~ ~eg{on of "~he brain. The almost universal finding of internal carotid narrowing below the point of stenosis has been attributed by some authors to true carotid hypoplasia ~7. 20. 4o and related by others to the amount of diminished flow through the artery 3~. That the disease is an evolving condition has clinical as well as angiographic support 12, as, a4 Nevertheless, many factors point to the congenital ba&ground of the disease ~4, ,6, 20, 25, as, 36 Among them are its preference for the Japanese race, the usual symmetrical involvement of the internal carotid arteries, the similarity between its angiographic appearance and the cerebral vascular tree in the human 11-16 mm embryo, and its association with some neurocutaneous syndromes and congenital vascular anomalies such as intracavernous aneurysms 6, persistent trigeminal arteries and primitive carotid-basilar anastomoses 12. Finally, the familial occurrence of the disease has also been reported 2%
Multiple Intracranial Arterial Occlusions in Patients
135
Case Reports Case 1. This 9-years-old girl with a history of chronic mental retardation suffered during the year before admission from repeated left focal motor fits, followed by transitory hemiparesis. During this period she also complained of frontal non-specific headaches. She had two brothers in good health, and there was no family history of seizures or neurofibromatosis. Physical examination: extensive "caf6 au lair" spots were present on the chest, perineal region, and thighs. Smaller, but similar, spots were profusely disseminated over the body. The left upper and lower limbs were shorter than the right by 2 and 4 cm respectively. The rest of the physical examination was within normal
Fig. 1. Case 1. Right common carotid angiography. Internal carotid artery is occluded at supraclinoid level. Enlarged posterior cerebral and anterior choroidal arteries giving leptomeningeal anastomoses to the anterior and middle cerebral arteries. Retrograde filling of these last arteries via posterior pericallosal artery (small double arrows) and anterior choroidal artery (small arrow), may be appreciated. The vascular network above carotid stenosis is clearly seen (big arrow) limits. Routine blood and urine test were normal. LE preparations and VDRL were negative. LCR examination was normal. EEG showed a right frontoparietaI slow wave focus. A pre-excitation anomaly of LGL type (short PR without delta wave), was detected in the ECG. Plain skull films showed an absence of the left innominnate line. A right common carotid angiogram revealed an occlusion of the supraclinoid internal carotid artery with an associated vascular network localized in the basal region of the brain. Distal branches of the hypertrophied posterior cerebral and anterior choroidal arteries anastomosed, via leptomeningeal connections, with the anterior and middle cerebral arteries. There were also signs of hydrocephalus (Fig. 1). The left common carotid angiogram showed similar findings, but the transdural external-internal anastomoses were more obvious. Two segmental occlusions of the anterior cerebral artery were seen. Vertebrobasilar
136
E. Lamas et al.:
Fig. 2. Case 2. Upper: right common carotid angiography; A-P and lateral projections. Internal carotid artery is partially obstructed at supraclinoid level. Basal telangiectasia (big arrow) and enlargement of both the ophthalmic and anterior ethmoidal (small arrows) arteries may be seen. Lower: left common carotid angiography; A-P and lateral projections. Infraclinoid carotid artery has a diminished calibre. Supraclinoid carotid artery is severely stenosed (big arrow). Basal telangiectasia and an enlarged anterior falx artery (small arrows), may be seen arteriography was normal. Pneumoencephalography showed communicating hydrocephalus with considerable cortico-subcortical atrophy. Continuous monitoring of the intraventricular pressure and the result of an infusion manometric test were consistent with the diagnosis of hydrocephalus "ex vacuo". The patient was treated with primidone, and recommended for psychological studies.
Multiple Intracranial Arterial Occlusions in Patients
137
Case 2. This 50-years-old normotensive man suddenly presented twenty four hours before admission with a frontonuchal headache followed by convulsions of the left limbs and left hemiplegia. When he was being examinated in the emergency room, the headache increased, generalized convulsions occurred, and the patient
Fig. 3. Upper: seriography of the two posterior thirds of the left cerebral hemisphere injected with Micropaque. Posterior cerebral artery (small arrows), and its branches, among them the posterior pericallosal artery (footed arrows) are shown. Basal telangiectasia (bigger arrows), may also be seen. Lower: postmortem preparation of the left internal carotid tree. Stenosis of the proximal segments of both the anterior and middle cerebral arteries (footed arrows), is shown. Filiform anastomotic connections between the lenticulostriated arteries (arrows), may be seen became unconscious with bilateral decerebrate rigidity. Spinal tap revealed a haemorrhagic CSF. Right common carotid angiography was performed revealing an incomplete occlusion of the supraclinoid carotid artery with an associated vascular network in the base of the brain. The ophthalmic artery, which was hypertrophied, fed a large anterior ethmoidal artery. There was a midline shift
138
E. Lamas et aL: Multiple IntracraniaI Arterial Occlusions in Patients
(Fig. 2). Left common carotid angiography showed similar findings. The ophthalmic artery was also markedly hypertrophied on this side, feeding an enlarged anterior falx artery (Fig. 2). Vertebrobasilar arteriography was not performed. The patient died several hours after carotid angiography. Necropsy Study: Multiple "caf~ au laW' spots were present all over the body, but mostly on the back. Numerous small subcutaneous nodules were also found on the trunk and limbs. The viscera were grossly unremarkable. A diffuse sub-
Fig. 4. Coronal sections of the brain at parieto-occipital level. Intracerebral haematoma in the right centrum semiovale inundating the ventricular system arachnoid haemorrhage covered both the convexity and the base of the brain Bilateral Micropaque perfusions of the carotid and vertebral arteries were perJ formed before formalin fixation. The fixed brain weighed 1,720 g. It was markedly swollen, showing diffuse gyral flattening and a larger right cerebral hemisphere. Bilateral nncal herniation, more prominent on the right side, was present. There was not a trace of atheromatosis in the vessels of the circle of Willis at naked eye inspection. Both intrapetrosal segments of the internal carotid arteries showed concentric luminal stenosis (about 50~ and these arteries appeared hypoplastic at supraclinoid level without luminal stenosis. The left middle cerebral artery also showed concentric luminal stenosis (about 30~ Both
Fig. 5. A) Intrapetrosal segment of the left internal carotid artery. Diffuse hyperplasia of the intimal layer producing luminal stenosis (PAS-Orcein 5
