•
Adult Arteriosclerotic Moyamoya 1 David
•
Neuroradiology
1:1. Hinshaw, Jr., M.D.,2 Joseph R. Thompson, M.D., and Anton N. Hasso, M.D.
Progressive idiopathic distal internal carotid artery occlusion in children and young adults associated with the development of bridging channels and tortuous, plethoric intracerebral arterial networks has been termed moyamoya or Nishimoto's disease. It is now generally recognized that this unusual angiographic pattern results from collateral supply pathways and is not a primary angiomatous process. The authors describe 2 middleaged patients with intracranial arteriosclerotic occlusive lesions demonstrating secondary collateral patterns angiographically identical to moyamoya. INDEX TERMS: Arteries, cerebral • Arteries, choroidal • Arteries, lenticulostriate. Arteries, thalamoperforate • Carotid Arteries, stenosis Radiology 118:633-636, March 1976
• rating arteries are called moyamoya after the Japanese word for "cloud" or "puff of smoke." It has been reported that moyamoya-type collateral vessels are not seen with arterial occlusions acquired late in life or with arteriosclerosis (7). We have recently examined two middleaged patients with arterial occlusive disease, both demonstrating moyamoya collaterals angiographically.
(Nishimoto's disease) consists chiefly of a syndrome in children and young adults manifested by progressive and intermittent hemiplegic episodes with an occasional presentation of subarachnoid hemorrhage (particularly in young adults) (1-6). Angiographically, there is usually bilateral but asymmetric idiopathic progressive occlusion of the distal internal carotid artery with simultaneous enqorqernent and dilatation of the anterior choroidal, lenticulostriate and thalamoperforate vessels in an attempt at collateralization. These dilated, tortuous, deep cerebral perfoEREBROVASCULAR MOYAMOYA
C
CASE REPORTS CASE I:
S. L., a 61-year-old woman with a long history of diabe-
Fig. 1. CASE I. Vertebral (A) and right common carotid angiogram (B) showing occlusion of the right middle cerebral and right posterior cerebral artery. Note tortuosity and engorgement of many deep cerebral arteries including the thalamoperforate, lenticulostriate, and anterior and posterior choroidal vessels. 1 From the Department of Radiology, Loma Linda University School of Medicine, Section of Neuroradiology, Loma Linda, Calif. Presented at the 13th Annual Meeting of the American Society of Neuroradiology, Vancouver, S.C., June 3-7, 1975. Accepted for publication in September 1975. 2 Present address: Second General Hospital, Box 11,Radiology APO NY 19180. shan
633
634
DAVID
B. HINSHAW, Jr.
AND OTHERS
Table I:
March 1976
Potential Collateral Pathways
Perforating internal carotid artery branches Anterior cerebral recurrent branches (Huebner's, etc.) Lenticulostriate branches of middle cerebral artery Anterior choroidal artery branches Posterior choroidal artery branches Thalamoperforate arteries Dorsal callosal arteries Ophthalmic artery, ethmoidal branches Meningeal-cortical and cortical-cortical arterial anastomoses
Table II:
Possible Origins of Moyamoya Syndrome
Idiopathic (arteritis?) Radiation arteritis Tumoral arterial obstruction Arteri osclerosis Infectious (tuberculous meningitis)
Fig. 2. CASE II. Vertebral angiogram demonstrating the infraand supratentorial vasculature supplied solely from the vertebrobasilar circulation. The deep thalamoperforate, lenticulostriate, choroidal and dorsal callosal arteries are very prominent. tes mellitus, suffered sudden onset of right hemiplegia, depression and aphasia. There was no previous history of neurologic incident. Treatment and convalescence were carried out at another hospital but some intellectual impairment and dysphasia remained. Three months after the stroke she was admitted to our medical center. The patient was an obese, hypertensive lady with marked diabetic retinopathy, right neck bruit and absent leg pulses below both femoral arteries. An arch aortogram without selective carotid studies was obtained and showed critical eccentric narrowing of the mid left common carotid artery, occlusion of the left internal carotid artery at its origin and severe stenosis of the right internal carotid artery at its origin. A
right carotid endarterectomy was performed. Histologic examination of the specimen showed "markedly atherosclerotic intima." The patient was readmitted nine months later with continued neurologic deficits and poor diabetic control. Cerebral angiography demonstrated occlusion of the right middle cerebral and right posterior cerebral arteries, severe stenosis of the right internal carotid artery siphon and the previously discovered left internal carotid artery occlusion. In addition, marked enlargement and tortuosity of small, deep, right cerebral vessels was obvious (Fig. 1). CASE II: J. C., a 50-year-old man, had a sudden onset of expressive aphasia lasting 3-4 days as the first manifestation of neurologic illness. Angiography at another institution showed left carotid artery occlusion. Three years later, he had a second, similar episode and repeat angiography at the same hospital demonstrated bilateral internal carotid artery occlusions. Three months later he was referred for a superficial temporal artery to middle cerebral artery microneurosurgical anastomosis to augment cerebral blood flow. Bilateral anastomoses were performed with complete brachiocephalic
Fig. 3. CASE II. A. Left external carotid angiogram showing meningeal-cortical arterial anastomoses (arrow). B. Right external carotid angiogram demonstrating opacification of anterior cerebral artery branches via anterior ethmoidal perforating branches (arrows).
635
ADULT ARTERIOSCLEROTIC MOYAMOYA
Vol. 118
Neuroradiology
and cerebral angiography following the first anastomotic procedure. The study revealed nonopacification of either internal carotid artery from its origin to the supraclinoid segment and nonpatency of the right-sided surgical anastomosis. Eccentric irregularities of the subclavian and brachiocephalic arteries were seen. Selective left vertebral angiography revealed opacification of both posterior cerebral, anterior cerebral and middle cerebral arteries. Marked engorgement and tortuosity of thalamoperforate and lenticulostriate arteries were apparent (Fig. 2). Meningeal-cortical, leptomeningeal and orbito-ethmoidal to anterior cerebral artery communications were also present (Fig. 3). The second (left-sided) anastomosis has freed the patient from further aphasic attacks and he has been able to return to work.
DISCUSSION
Most of the literature to date emphasizes the moyamoya pattern as characteristic of a particular syndrome in children and young adults. There has been considerable debate regarding its origin: Nishimoto and colleagues believe it to be a primary vascular malformation (1) while others (2, 5, 7) feel that these arteries are merely dilated pre-existent collateral channels attempting to bypass critical arterial obstructive lesions. Zulch (8) has presented a case in an elderly patient that he attributed to arteriosclerotic occlusive disease. Debrun et a/. (9) emphasized the etiologic nonspecificity of the moyamoya pattern. Our cases of arteriosclerotic cerebrovascular occlusive disease demonstrate changes identical to the classic smoke-like clusters of deep cerebral small arteries which have been described previously as moyamoya disease in children and young adults. At 61 and 50 years, our 2 patients, [as in Zulch's case (8)] are well beyond the typical moyamoya age group and lack the long clinical history of exacerbations generally noted in classical moyamoya disease. Also, our patients show a multiplicity of stenotic lesions, generally eccentric in type, quite in keeping with arteriosclerosis obliterans. The atherosclerotic lesion in the right internal carotid artery origin of S. L. (CASE I) was surgically treated and pathologically documented. We agree with Debrun that moyamoya collaterals probably develop in association with certain sites of slowly progressive arterial Obstruction, generally when the usual large collateral pathways, such as the ophthalmic artery and circle of Willis branches, are unable to supply sufficient regional blood flow (7). This predisposition is seen typically in progressive occlusion of the distal internal carotid artery beyond the origin of the ophthalmic artery and particularly if there is concomitant involvement or atresia of major, adjacent circle of Willis branches. The potential moyamoya-type collateral routes in these specific sites have been previously mentioned. As related by Pecker (7), the basal fibrillar vessels arise from perforating internal carotid artery branches, Heubner's recurrent artery, middle cerebral artery lenticulostriate branches, and capsular and pallidal anterior choroidal artery branches. Ethmoidal branches of the ophthalmic artery may also participate via antegrade
Deep Cerebral and Upper Brain Stem Arteries AC
- PROXIMAL (MEDIAL STRIATEI DISTAL (SEPTAL, FORNICEAL, CALLOS ALI
MC
- MEDIAL STRIATE LATERAL STR IATE
ACh
- PROXIMAL LATERAL MEDIAL DISTAL
5-10 1-3
3+ 3+ 4+ 5+
PCom -
7-10
PC
3-6 3-4 3-5 I
- THALAMOPERFORATE CHOROI DAL THALAMOGEN ICULATE QUA DR IGEM INAL SPLENIAL
1
Ophth - ANTERIOR ETHMOI DAL POSTERIOR ETHMOIDAL
AVERAGE TOTAL DEEP ARTERIES
60
Fig. 4. Diagrammatic representation of the many deep cerebral and upper brain stem arteries which frequently take part in the moyamoya appearance. AC = anterior cerebral artery; MC = middle cerebral artery; Ach = anterior choroidal artery; Pcom = posterior communicating artery; PC = posterior cerebral artery; Ophth ophthalmic artery.
=
ophthalmic flow (as opposed to the retrograde flow generally seen in more proximal carotid lesions). Thalamoperforate arteries arising from the basilar artery tip, proximal posterior cerebral and posterior communicating arteries along with posterior choroidal and dorsal callosal arteries also are frequently involved (TABLE I) (Fig. 4). CONCLUSION
In view of our findings of moyamoya vascular patterns in association with clinical situations resulting from (in one case pathologically correlated) arteriosclerotic occlusive disease, and in light of other reports linking this pattern to radiation arteritis (9, 10), tumoral arterial obstruction (11), and possibly tuberculous meningitis (12), we suggest that moyamoya is merely a nonspecific response of a multitude of previously present small vessels to occlusive arterial disease of any type located at specific sites in the basal arteries of the brain.
636
DAVID
B. HINSHAW,
REFERENCES 1. Nishimoto A, Takeuchi S: Abnormal cerebrovascular network related to the internal carotid arteries. J Neurosurg 29:255260, Sep 1968 2. Suzuki J, Takaku A: Cerebrovascular "moyamoya" disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol (Chicago) 20:288-299, Mar 1969 3. Taveras JM: Multiple progressive intracranial arterial occlusions: a syndrome of children and young adults. Am J Roentgenol 106:235-268, Jun 1969 4. Harwood-Nash DC, McDonald P, Argent W: Cerebral arterial disease in children: an angiographic study of 40 cases. Am J RoentgenoI111:672-686, Apr 1971 5. Handa J, Handa H: Progressive cerebral arterial occlusive disease: analysis of 27 cases. Neuroradiology 3: 119-133, Mar 1972 6. Hilal SK, Solomon GE, Gold AP, et al: Primary cerebral arterial occlusive disease in children. Radiology 99:71-86; 93-94, Apr 1971 7. Pecker J, Simon J, Guy G, et al: Nishimoto's disease: significance of its angiographic appearances. Neuroradiology 5:223230, Aug 1973
Jr. AND OTHERS
March 1976
8. Zulch KJ, Dreesbach HA, Eschbach 0: Occlusion of the middle cerebral artery with the formation of an abnormal arterial collateral system-moyamoya type-23 months later. Neuroradiology 7:19-24, Feb 1974 9. Debrun G, Sauvegrain J, Aicardi J, et al: Moyamoya, a nonspecific radiological syndrome. Neuroradiology 8:241-244, Jan 1975 10. Painter MJ, Chutorian AM, Hilal SK: Cerebrovasculopathy following irradiation in childhood. Neurology 25:189-194, Feb 1975 11. Rosengren K: Moya-moya vessels: collateral arteries of the basal ganglia. Malignant occlusion of the anterior cerebral arteries. Acta Radiol [Diag] 15:145-151, Mar 1974 12. Mathew NT, Abraham J, Chandy J: Cerebral angiographic features in tuberculous meningitis. Neurology (Minneap) 20:10151023, Oct 1970
Second General Hospital Box 11, Radiology APO New York 09180
Adult Arteriosclerotic Moyamoya 1 David
•
Neuroradiology
1:1. Hinshaw, Jr., M.D.,2 Joseph R. Thompson, M.D., and Anton N. Hasso, M.D.
Progressive idiopathic distal internal carotid artery occlusion in children and young adults associated with the development of bridging channels and tortuous, plethoric intracerebral arterial networks has been termed moyamoya or Nishimoto's disease. It is now generally recognized that this unusual angiographic pattern results from collateral supply pathways and is not a primary angiomatous process. The authors describe 2 middleaged patients with intracranial arteriosclerotic occlusive lesions demonstrating secondary collateral patterns angiographically identical to moyamoya. INDEX TERMS: Arteries, cerebral • Arteries, choroidal • Arteries, lenticulostriate. Arteries, thalamoperforate • Carotid Arteries, stenosis Radiology 118:633-636, March 1976
• rating arteries are called moyamoya after the Japanese word for "cloud" or "puff of smoke." It has been reported that moyamoya-type collateral vessels are not seen with arterial occlusions acquired late in life or with arteriosclerosis (7). We have recently examined two middleaged patients with arterial occlusive disease, both demonstrating moyamoya collaterals angiographically.
(Nishimoto's disease) consists chiefly of a syndrome in children and young adults manifested by progressive and intermittent hemiplegic episodes with an occasional presentation of subarachnoid hemorrhage (particularly in young adults) (1-6). Angiographically, there is usually bilateral but asymmetric idiopathic progressive occlusion of the distal internal carotid artery with simultaneous enqorqernent and dilatation of the anterior choroidal, lenticulostriate and thalamoperforate vessels in an attempt at collateralization. These dilated, tortuous, deep cerebral perfoEREBROVASCULAR MOYAMOYA
C
CASE REPORTS CASE I:
S. L., a 61-year-old woman with a long history of diabe-
Fig. 1. CASE I. Vertebral (A) and right common carotid angiogram (B) showing occlusion of the right middle cerebral and right posterior cerebral artery. Note tortuosity and engorgement of many deep cerebral arteries including the thalamoperforate, lenticulostriate, and anterior and posterior choroidal vessels. 1 From the Department of Radiology, Loma Linda University School of Medicine, Section of Neuroradiology, Loma Linda, Calif. Presented at the 13th Annual Meeting of the American Society of Neuroradiology, Vancouver, S.C., June 3-7, 1975. Accepted for publication in September 1975. 2 Present address: Second General Hospital, Box 11,Radiology APO NY 19180. shan
633
634
DAVID
B. HINSHAW, Jr.
AND OTHERS
Table I:
March 1976
Potential Collateral Pathways
Perforating internal carotid artery branches Anterior cerebral recurrent branches (Huebner's, etc.) Lenticulostriate branches of middle cerebral artery Anterior choroidal artery branches Posterior choroidal artery branches Thalamoperforate arteries Dorsal callosal arteries Ophthalmic artery, ethmoidal branches Meningeal-cortical and cortical-cortical arterial anastomoses
Table II:
Possible Origins of Moyamoya Syndrome
Idiopathic (arteritis?) Radiation arteritis Tumoral arterial obstruction Arteri osclerosis Infectious (tuberculous meningitis)
Fig. 2. CASE II. Vertebral angiogram demonstrating the infraand supratentorial vasculature supplied solely from the vertebrobasilar circulation. The deep thalamoperforate, lenticulostriate, choroidal and dorsal callosal arteries are very prominent. tes mellitus, suffered sudden onset of right hemiplegia, depression and aphasia. There was no previous history of neurologic incident. Treatment and convalescence were carried out at another hospital but some intellectual impairment and dysphasia remained. Three months after the stroke she was admitted to our medical center. The patient was an obese, hypertensive lady with marked diabetic retinopathy, right neck bruit and absent leg pulses below both femoral arteries. An arch aortogram without selective carotid studies was obtained and showed critical eccentric narrowing of the mid left common carotid artery, occlusion of the left internal carotid artery at its origin and severe stenosis of the right internal carotid artery at its origin. A
right carotid endarterectomy was performed. Histologic examination of the specimen showed "markedly atherosclerotic intima." The patient was readmitted nine months later with continued neurologic deficits and poor diabetic control. Cerebral angiography demonstrated occlusion of the right middle cerebral and right posterior cerebral arteries, severe stenosis of the right internal carotid artery siphon and the previously discovered left internal carotid artery occlusion. In addition, marked enlargement and tortuosity of small, deep, right cerebral vessels was obvious (Fig. 1). CASE II: J. C., a 50-year-old man, had a sudden onset of expressive aphasia lasting 3-4 days as the first manifestation of neurologic illness. Angiography at another institution showed left carotid artery occlusion. Three years later, he had a second, similar episode and repeat angiography at the same hospital demonstrated bilateral internal carotid artery occlusions. Three months later he was referred for a superficial temporal artery to middle cerebral artery microneurosurgical anastomosis to augment cerebral blood flow. Bilateral anastomoses were performed with complete brachiocephalic
Fig. 3. CASE II. A. Left external carotid angiogram showing meningeal-cortical arterial anastomoses (arrow). B. Right external carotid angiogram demonstrating opacification of anterior cerebral artery branches via anterior ethmoidal perforating branches (arrows).
635
ADULT ARTERIOSCLEROTIC MOYAMOYA
Vol. 118
Neuroradiology
and cerebral angiography following the first anastomotic procedure. The study revealed nonopacification of either internal carotid artery from its origin to the supraclinoid segment and nonpatency of the right-sided surgical anastomosis. Eccentric irregularities of the subclavian and brachiocephalic arteries were seen. Selective left vertebral angiography revealed opacification of both posterior cerebral, anterior cerebral and middle cerebral arteries. Marked engorgement and tortuosity of thalamoperforate and lenticulostriate arteries were apparent (Fig. 2). Meningeal-cortical, leptomeningeal and orbito-ethmoidal to anterior cerebral artery communications were also present (Fig. 3). The second (left-sided) anastomosis has freed the patient from further aphasic attacks and he has been able to return to work.
DISCUSSION
Most of the literature to date emphasizes the moyamoya pattern as characteristic of a particular syndrome in children and young adults. There has been considerable debate regarding its origin: Nishimoto and colleagues believe it to be a primary vascular malformation (1) while others (2, 5, 7) feel that these arteries are merely dilated pre-existent collateral channels attempting to bypass critical arterial obstructive lesions. Zulch (8) has presented a case in an elderly patient that he attributed to arteriosclerotic occlusive disease. Debrun et a/. (9) emphasized the etiologic nonspecificity of the moyamoya pattern. Our cases of arteriosclerotic cerebrovascular occlusive disease demonstrate changes identical to the classic smoke-like clusters of deep cerebral small arteries which have been described previously as moyamoya disease in children and young adults. At 61 and 50 years, our 2 patients, [as in Zulch's case (8)] are well beyond the typical moyamoya age group and lack the long clinical history of exacerbations generally noted in classical moyamoya disease. Also, our patients show a multiplicity of stenotic lesions, generally eccentric in type, quite in keeping with arteriosclerosis obliterans. The atherosclerotic lesion in the right internal carotid artery origin of S. L. (CASE I) was surgically treated and pathologically documented. We agree with Debrun that moyamoya collaterals probably develop in association with certain sites of slowly progressive arterial Obstruction, generally when the usual large collateral pathways, such as the ophthalmic artery and circle of Willis branches, are unable to supply sufficient regional blood flow (7). This predisposition is seen typically in progressive occlusion of the distal internal carotid artery beyond the origin of the ophthalmic artery and particularly if there is concomitant involvement or atresia of major, adjacent circle of Willis branches. The potential moyamoya-type collateral routes in these specific sites have been previously mentioned. As related by Pecker (7), the basal fibrillar vessels arise from perforating internal carotid artery branches, Heubner's recurrent artery, middle cerebral artery lenticulostriate branches, and capsular and pallidal anterior choroidal artery branches. Ethmoidal branches of the ophthalmic artery may also participate via antegrade
Deep Cerebral and Upper Brain Stem Arteries AC
- PROXIMAL (MEDIAL STRIATEI DISTAL (SEPTAL, FORNICEAL, CALLOS ALI
MC
- MEDIAL STRIATE LATERAL STR IATE
ACh
- PROXIMAL LATERAL MEDIAL DISTAL
5-10 1-3
3+ 3+ 4+ 5+
PCom -
7-10
PC
3-6 3-4 3-5 I
- THALAMOPERFORATE CHOROI DAL THALAMOGEN ICULATE QUA DR IGEM INAL SPLENIAL
1
Ophth - ANTERIOR ETHMOI DAL POSTERIOR ETHMOIDAL
AVERAGE TOTAL DEEP ARTERIES
60
Fig. 4. Diagrammatic representation of the many deep cerebral and upper brain stem arteries which frequently take part in the moyamoya appearance. AC = anterior cerebral artery; MC = middle cerebral artery; Ach = anterior choroidal artery; Pcom = posterior communicating artery; PC = posterior cerebral artery; Ophth ophthalmic artery.
=
ophthalmic flow (as opposed to the retrograde flow generally seen in more proximal carotid lesions). Thalamoperforate arteries arising from the basilar artery tip, proximal posterior cerebral and posterior communicating arteries along with posterior choroidal and dorsal callosal arteries also are frequently involved (TABLE I) (Fig. 4). CONCLUSION
In view of our findings of moyamoya vascular patterns in association with clinical situations resulting from (in one case pathologically correlated) arteriosclerotic occlusive disease, and in light of other reports linking this pattern to radiation arteritis (9, 10), tumoral arterial obstruction (11), and possibly tuberculous meningitis (12), we suggest that moyamoya is merely a nonspecific response of a multitude of previously present small vessels to occlusive arterial disease of any type located at specific sites in the basal arteries of the brain.
636
DAVID
B. HINSHAW,
REFERENCES 1. Nishimoto A, Takeuchi S: Abnormal cerebrovascular network related to the internal carotid arteries. J Neurosurg 29:255260, Sep 1968 2. Suzuki J, Takaku A: Cerebrovascular "moyamoya" disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol (Chicago) 20:288-299, Mar 1969 3. Taveras JM: Multiple progressive intracranial arterial occlusions: a syndrome of children and young adults. Am J Roentgenol 106:235-268, Jun 1969 4. Harwood-Nash DC, McDonald P, Argent W: Cerebral arterial disease in children: an angiographic study of 40 cases. Am J RoentgenoI111:672-686, Apr 1971 5. Handa J, Handa H: Progressive cerebral arterial occlusive disease: analysis of 27 cases. Neuroradiology 3: 119-133, Mar 1972 6. Hilal SK, Solomon GE, Gold AP, et al: Primary cerebral arterial occlusive disease in children. Radiology 99:71-86; 93-94, Apr 1971 7. Pecker J, Simon J, Guy G, et al: Nishimoto's disease: significance of its angiographic appearances. Neuroradiology 5:223230, Aug 1973
Jr. AND OTHERS
March 1976
8. Zulch KJ, Dreesbach HA, Eschbach 0: Occlusion of the middle cerebral artery with the formation of an abnormal arterial collateral system-moyamoya type-23 months later. Neuroradiology 7:19-24, Feb 1974 9. Debrun G, Sauvegrain J, Aicardi J, et al: Moyamoya, a nonspecific radiological syndrome. Neuroradiology 8:241-244, Jan 1975 10. Painter MJ, Chutorian AM, Hilal SK: Cerebrovasculopathy following irradiation in childhood. Neurology 25:189-194, Feb 1975 11. Rosengren K: Moya-moya vessels: collateral arteries of the basal ganglia. Malignant occlusion of the anterior cerebral arteries. Acta Radiol [Diag] 15:145-151, Mar 1974 12. Mathew NT, Abraham J, Chandy J: Cerebral angiographic features in tuberculous meningitis. Neurology (Minneap) 20:10151023, Oct 1970
Second General Hospital Box 11, Radiology APO New York 09180
