UNILATERAL MOYAMOYA DISEASE, INTRACRANIAL ANEURYSM, AND A PITUITARY ADENOMA: A CASE REPORT Robert E. Hardy, MD, Ifeanyi Obianyo, MD, Hee Suck Shu, MD, and Luther Adair, MD Nashville, Tennessee
A case of unilateral moyamoya disease is reported in an adult, associated with an aneurysm of the circle of Willis and a nonfunctional pituitary adenoma. A review of the literature is discussed. Young individuals presenting with signs of acute cerebrovascular changes of undetermined cause should be evaluated for moyamoya disease. (J Nati Med Assoc. 1991 ;83:827-830.) Key words * moyamoya disease * subarachnoid hemorrhage * saccular aneurysm * basal collaterals The constellation of bilateral carotid artery occlusion and sequelae associated with collateral vessel formation at the base of the brain was first reported by Takeuchi in 1961.1 The name "moyamoya" was given by Suzuki and Takaku because of its angiographic appearance, which is similar to a "puff of smoke."2 Since these early reports from Japan, a number of cases that included other features have been published worldwide, further elucidating the natural history of this disease. In this report, a young black female presented with a subarachnoid hemorrhage from a saccular aneurysm. From the Departments of Medicine and Radiology, Meharry Medical College, Nashville, Tennessee. Requests for reprints should be addressed to Dr Robert E Hardy, Department of Medicine, Meharry Medical College, 1005 D.B. Todd Blvd, Nashville, TN 37208. JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION, VOL. 83, NO. 9
She was found to have unilateral carotid artery occlusion and vascular changes, including basal collaterals characteristic of moyamoya disease. She was also found to have a nonfunctioning pituitary adenoma. This case represents the second report with unilateral moyamoya disease and the first report of an associated pituitary adenoma.
CASE REPORT A 27-year-old black female was admitted to the hospital with severe persistent headaches. One week prior to presentation, she had paroxysmal non- productive cough. Five days prior to entry, the paroxysmal cough was associated with severe headaches that culminated in a syncopal episode. The patient was subsequently seen in an emergency room at another hospital where she was admitted. She was treated and released after 5 days with a diagnosis of upper respiratory tract infection. Later on the day of discharge, she presented to our emergency room still with a severe persistent headache. The headache was described as diffuse, throbbing and constant, with marked intensity in the frontal region. This headache was exacerbated by movement and was not relieved by Tylenol. There was no associated nausea or vomiting, and the patient denied fever, chills, dizziness, dyspnea, chest pain, or palpitations, but did admit to some neck discomfort. Her past medical history was unremarkable. There was no family history of hypertension, diabetes mellitus, asthma, or cerebrovascular disease. She had a 10-pack 827
MOYAMOYA DISEASE
Figure 1 CT scan showing contrast enhancement of lesionrostral tothe right corpus callosum indicative of right communicating artery aneurysm. a year history of cigarette smoking. She denied alcohol use, but admitted to recreational use of marijuana. She
had no known allergies and was on no medication. The patient's temperature was 97F, her pulse was 98 per minute and respirations were 28 per minute. Her blood pressure was 160/1 10 mm Hg. On examination, the patient was a well-nourished, well-developed female who appeared to be in acute distress. She was alert and oriented. The head was
normal, and the pupils were equal and reacted normally to light bilaterally. The fundi did not reveal any
hemorrhage, exudate, or papilledema. She had nuchal rigidity but Kernig's and Brudzinski's signs were negative. Her lungs were normal. The heart revealed a Grade IIINVI systolic ejection murmur at the apex. The abdominal examination was normal with negative hemoccult stool. There were no focal neurologic deficits. The hematocrit was 46.a1%, the white cell count was 10 3000/mm3 with normal differential. Platelet count 828
was normal. The cerebrospinal fluid opening pressure was 280 mm H20. The fluid was xanthochronic. Red blood cells numbered 30 260/mm3, white blood count 356/mm3, protein 9 gm/dL and glucose was 57 mg/dL. The chest X-ray was unremarkable, and an electrocardiogram revealed diffuse T-wave inversion. Symptomatic and supportive management was instituted. CT and MRI scans of the head showed increased density in the area of the corpus callosum (Figure 1). (Evidence of subarachnoid hemorrhage was also seen on the scans.) Bilateral carotid angiography revealed a normal (R) common carotid artery. A 1-cm round anterior communicating artery aneurysm was seen in the midline. There was no significant mass effect. Both anterior cerebral arteries filled from the right side. These arteries were irregular in caliber with alternating areas of narrowing and minimal dilatation. The distal middle cerebral complex was normal. The left common carotid artery seemed normal. There was marked attenuation of the distal-most portion of the cavernous internal carotid artery with complete occlusion of the horizontal segment of the middle cerebral artery. It was bridged by numerous fine collaterals. Following this, the main trunk of the middle cerebral artery was intact, and no definite abnormality of its distal branches was seen. Neither of the anterior cerebral arteries filled from the left side. The left vertebral'artery main trunk and the Basilar artery were normally patent-no aneurysm was seen. There were several areas of fine collateralization in the distal circulation, but the major branches were intact. There was no reflux into the contralateral vertebral artery. The right vertebral artery was slightly larger than the left, and its main trunk appeared normal. There was good opacification of the Basilar artery, which was normally patent. The posterior circulation on the right side was normal. There was more than the usual amount of filling of distal sylvian branches on both vertebral injections due to the occlusion of the left middle cerebral complex (Figure 2).
MANAGEMENT After the initial evaluation and appropriate delay for a reduction in vasospasm, the patient underwent a craniotomy and clipping of the right anterior communicating aneurysm. A biopsy was taken from the pituitary gland, which appeared to be enlarged. Baseline endocrine tests were normal. The patient was discharged home without any neurological or other complications. JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION, VOL. 83, NO. 9
MOYAMOYA DISEASE
DISCUSSION Occlusive disease of the carotids associated with angiographic evidence of collateral arterial vessel formation at the base of the brain was first reported in 1961 by Takeuchi.' Since then, 1000 cases have been reported.3 While seen more commonly in Japanese descendants, the entity has been reported in all races. It is defined angiographically by partial or complete occlusion of both carotid arteries at the siphon, in association with extensive collateral vessel formation at the base of the brain.2 The entity has a bimodal distribution, being found most often in children during the first decade of life and in adults during their fourth decade of life.4 It occurs slightly more frequently in females than in males. The clinical presentation in children is more dynamic and progressive, showing signs of vascular occlusion including paraparesis, speech problems, and mental changes. The entity in adults commonly presents as subarachnoid or other intracranial hemorrhage.4 The etiology of this disease is unknown; however, it has been reported in association with a number of disorders including: congenital arterial dysplasia,5 sickle cell disease,6 connective tissue disorders,7 neurofibromatosis,8 phakomatosis,9 leptospirosis,10 tuberculous meningitis,1' and radiation therapy.'2 There is also a possibility of familial predisposition. Suzuki and Kodama4 found an increased association with a prior history of cervical (neck) inflammation, and they were able to produce pathologic changes similar to moyamoya disease in dogs by inducing inflammation. They found that sympathetic denervation of superior cervical ganglia could reduce this occlusive process.4 The likelihood of moyamoya arising from a single cause, however, is remote. Most probably it is or can be the process or end result (vessel occlusion) of numerous potential inciting problems operating through a common mechanism. The radiologic presentation of this case is classic in terms of the occlusion of the carotid artery near its clinoid region as well as the characteristic irregular narrowing of distal branches in association with basilar collateral vessel formation (Figure 1). This patient was also found to have an anterior communicating saccular aneurysm of the circle of Willis, seen both on CT scan and by angiography (Figure 2). This finding is associated with moyamoya in 14% of cases.13 These hemorrhagic episodes arise most commonly from pseudoaneurysm of abnormal "collateral" vessels, but they may also arise from saccular aneurysms of the circle of Willis.14 The latter type of aneurysm may be the result of increased flow through the circle vessels because of altered circulation. Pathologically, the most JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION, VOL. 83, NO. 9
~ r~ ~ ~ ~ . . .
Figure 2. Right carotid angiogram revealing basilar neovascularization, carotid artery tapering (cavernous portion), and anterior communicating artery aneurysm.
prominent feature of moyamoya is intimal fibrocellular thickening and excessive folding and thickening or deficiencies in the internal elastic lamina.15 An arteritis of vessel walls has not been documented. Moyamoya disease should be considered as a potential cause of cerebrovascular accidents, both thrombotic and hemorrhagic, in young individuals. This is especially important since associated aneurysms may be clipped and effectively neutralized. Anticoagulants should be avoided because of the tendency to bleed from aneurysms and pseudoaneurysms. Various surgical interventions may be useful, especially if employed early. Further basic study of the at-risk population and young individuals with the disease(s) may further illuminate its pathophysiology and lead to new surgical and pharmacologic interventions. Literature Cited 1. Takeuchi K. Occlusive disease of the carotid artery. Shinker Shimpo. 1961;5:511-513. 829
MOYAMOYA DISEASE
2. Suzuki J, Takaku A. Cerebral vascular 'Moya Moya' disease: a disease showing abnormal net-like vessels in base of brain. Arch Neurol. 1969;20:288-299. 3. Meriweather RP, Barnett HG, Echols DH. Moya Moya disease as a cause of subarachnoid hemorrhage in a Negro patient. J Neurol Surg. 1976; 44:620-622. 4. Suzuki J, Kodama A. Moya Moya disease-a review. Stroke. 1983;14:104-109. 5. Dumas MP, Girard L, Collomb H. Occlusions bilateraes de la carotide interne associee on une circulation de suppleance cortico-corticale, transdurale, et du type 'Moya Moya' ches l'enfant noire. J Neurol Sci. 1969;1 6:1-25. 6. Stockman JA, Nigro MA, Mishkin MM, Oski FA. Occlusion of large cerebral vessels in sickle cell anemia. N Engl J Med. 1972;287:846-849. 7. Richman DP, Watts HG, Parsons D, Schmid K, Glimcher NJ. Familiar Moya Moya associated with biochemical abnormalities of connective tissue. Neurology. 1977;27:382-386. 8. Tomsick TA, Lukin RR, Chambers AA, Benton C. Neurofibromatosis and intracranial arterial occlusive disease. Neuroradiology. 1976;1 1:229-234.
830
9. Hilal SK, Solomon GE, Gold AP. Primary cerebral arterial occlusive disease in children, part II: neurocutaneous syndromes. Radiology. 1971;99:87-93. 10. Ximin I, Xuzhong R, Zhuan C, Burun Y, Shangpu, Yunhg G. Moya Moya disease caused by leptospiral cerebral arteries. Chin Med J. 1980;93:596-604. 11. Mathew NT, Abraham J, Chandy J. Cerebral angiographic features in tuberculous meningitis. Neurology. 1970;20:1015-1019. 12. Rajakulasingam K, Cerullo J, Raidmond AJ. Childhood Moya Moya syndrome postradiation pathogenesis. Child's Brain. 1979;5:467. 13. Konshi Y, Kadwvaki C, Rum M. Aneurysms associated with Moya Moya disease. Neurosurgery. 1985;4:484-488. 14. Sato M, Kohama A, Fukuda A. Moya Moya-like disease associated with ventricular hemorrhages: report of three cases. Neurosurgery. 1985;17:260-266. 15. Coakman HB, Duehen LW, Scaravilli F. Moya Moya disease: clinical and pathological report of a case with associated myopathy. J Neurol Neurosurg Psychiatry. 1 979;42:289-297.
JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION, VOL. 83, NO. 9
A case of unilateral moyamoya disease is reported in an adult, associated with an aneurysm of the circle of Willis and a nonfunctional pituitary adenoma. A review of the literature is discussed. Young individuals presenting with signs of acute cerebrovascular changes of undetermined cause should be evaluated for moyamoya disease. (J Nati Med Assoc. 1991 ;83:827-830.) Key words * moyamoya disease * subarachnoid hemorrhage * saccular aneurysm * basal collaterals The constellation of bilateral carotid artery occlusion and sequelae associated with collateral vessel formation at the base of the brain was first reported by Takeuchi in 1961.1 The name "moyamoya" was given by Suzuki and Takaku because of its angiographic appearance, which is similar to a "puff of smoke."2 Since these early reports from Japan, a number of cases that included other features have been published worldwide, further elucidating the natural history of this disease. In this report, a young black female presented with a subarachnoid hemorrhage from a saccular aneurysm. From the Departments of Medicine and Radiology, Meharry Medical College, Nashville, Tennessee. Requests for reprints should be addressed to Dr Robert E Hardy, Department of Medicine, Meharry Medical College, 1005 D.B. Todd Blvd, Nashville, TN 37208. JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION, VOL. 83, NO. 9
She was found to have unilateral carotid artery occlusion and vascular changes, including basal collaterals characteristic of moyamoya disease. She was also found to have a nonfunctioning pituitary adenoma. This case represents the second report with unilateral moyamoya disease and the first report of an associated pituitary adenoma.
CASE REPORT A 27-year-old black female was admitted to the hospital with severe persistent headaches. One week prior to presentation, she had paroxysmal non- productive cough. Five days prior to entry, the paroxysmal cough was associated with severe headaches that culminated in a syncopal episode. The patient was subsequently seen in an emergency room at another hospital where she was admitted. She was treated and released after 5 days with a diagnosis of upper respiratory tract infection. Later on the day of discharge, she presented to our emergency room still with a severe persistent headache. The headache was described as diffuse, throbbing and constant, with marked intensity in the frontal region. This headache was exacerbated by movement and was not relieved by Tylenol. There was no associated nausea or vomiting, and the patient denied fever, chills, dizziness, dyspnea, chest pain, or palpitations, but did admit to some neck discomfort. Her past medical history was unremarkable. There was no family history of hypertension, diabetes mellitus, asthma, or cerebrovascular disease. She had a 10-pack 827
MOYAMOYA DISEASE
Figure 1 CT scan showing contrast enhancement of lesionrostral tothe right corpus callosum indicative of right communicating artery aneurysm. a year history of cigarette smoking. She denied alcohol use, but admitted to recreational use of marijuana. She
had no known allergies and was on no medication. The patient's temperature was 97F, her pulse was 98 per minute and respirations were 28 per minute. Her blood pressure was 160/1 10 mm Hg. On examination, the patient was a well-nourished, well-developed female who appeared to be in acute distress. She was alert and oriented. The head was
normal, and the pupils were equal and reacted normally to light bilaterally. The fundi did not reveal any
hemorrhage, exudate, or papilledema. She had nuchal rigidity but Kernig's and Brudzinski's signs were negative. Her lungs were normal. The heart revealed a Grade IIINVI systolic ejection murmur at the apex. The abdominal examination was normal with negative hemoccult stool. There were no focal neurologic deficits. The hematocrit was 46.a1%, the white cell count was 10 3000/mm3 with normal differential. Platelet count 828
was normal. The cerebrospinal fluid opening pressure was 280 mm H20. The fluid was xanthochronic. Red blood cells numbered 30 260/mm3, white blood count 356/mm3, protein 9 gm/dL and glucose was 57 mg/dL. The chest X-ray was unremarkable, and an electrocardiogram revealed diffuse T-wave inversion. Symptomatic and supportive management was instituted. CT and MRI scans of the head showed increased density in the area of the corpus callosum (Figure 1). (Evidence of subarachnoid hemorrhage was also seen on the scans.) Bilateral carotid angiography revealed a normal (R) common carotid artery. A 1-cm round anterior communicating artery aneurysm was seen in the midline. There was no significant mass effect. Both anterior cerebral arteries filled from the right side. These arteries were irregular in caliber with alternating areas of narrowing and minimal dilatation. The distal middle cerebral complex was normal. The left common carotid artery seemed normal. There was marked attenuation of the distal-most portion of the cavernous internal carotid artery with complete occlusion of the horizontal segment of the middle cerebral artery. It was bridged by numerous fine collaterals. Following this, the main trunk of the middle cerebral artery was intact, and no definite abnormality of its distal branches was seen. Neither of the anterior cerebral arteries filled from the left side. The left vertebral'artery main trunk and the Basilar artery were normally patent-no aneurysm was seen. There were several areas of fine collateralization in the distal circulation, but the major branches were intact. There was no reflux into the contralateral vertebral artery. The right vertebral artery was slightly larger than the left, and its main trunk appeared normal. There was good opacification of the Basilar artery, which was normally patent. The posterior circulation on the right side was normal. There was more than the usual amount of filling of distal sylvian branches on both vertebral injections due to the occlusion of the left middle cerebral complex (Figure 2).
MANAGEMENT After the initial evaluation and appropriate delay for a reduction in vasospasm, the patient underwent a craniotomy and clipping of the right anterior communicating aneurysm. A biopsy was taken from the pituitary gland, which appeared to be enlarged. Baseline endocrine tests were normal. The patient was discharged home without any neurological or other complications. JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION, VOL. 83, NO. 9
MOYAMOYA DISEASE
DISCUSSION Occlusive disease of the carotids associated with angiographic evidence of collateral arterial vessel formation at the base of the brain was first reported in 1961 by Takeuchi.' Since then, 1000 cases have been reported.3 While seen more commonly in Japanese descendants, the entity has been reported in all races. It is defined angiographically by partial or complete occlusion of both carotid arteries at the siphon, in association with extensive collateral vessel formation at the base of the brain.2 The entity has a bimodal distribution, being found most often in children during the first decade of life and in adults during their fourth decade of life.4 It occurs slightly more frequently in females than in males. The clinical presentation in children is more dynamic and progressive, showing signs of vascular occlusion including paraparesis, speech problems, and mental changes. The entity in adults commonly presents as subarachnoid or other intracranial hemorrhage.4 The etiology of this disease is unknown; however, it has been reported in association with a number of disorders including: congenital arterial dysplasia,5 sickle cell disease,6 connective tissue disorders,7 neurofibromatosis,8 phakomatosis,9 leptospirosis,10 tuberculous meningitis,1' and radiation therapy.'2 There is also a possibility of familial predisposition. Suzuki and Kodama4 found an increased association with a prior history of cervical (neck) inflammation, and they were able to produce pathologic changes similar to moyamoya disease in dogs by inducing inflammation. They found that sympathetic denervation of superior cervical ganglia could reduce this occlusive process.4 The likelihood of moyamoya arising from a single cause, however, is remote. Most probably it is or can be the process or end result (vessel occlusion) of numerous potential inciting problems operating through a common mechanism. The radiologic presentation of this case is classic in terms of the occlusion of the carotid artery near its clinoid region as well as the characteristic irregular narrowing of distal branches in association with basilar collateral vessel formation (Figure 1). This patient was also found to have an anterior communicating saccular aneurysm of the circle of Willis, seen both on CT scan and by angiography (Figure 2). This finding is associated with moyamoya in 14% of cases.13 These hemorrhagic episodes arise most commonly from pseudoaneurysm of abnormal "collateral" vessels, but they may also arise from saccular aneurysms of the circle of Willis.14 The latter type of aneurysm may be the result of increased flow through the circle vessels because of altered circulation. Pathologically, the most JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION, VOL. 83, NO. 9
~ r~ ~ ~ ~ . . .
Figure 2. Right carotid angiogram revealing basilar neovascularization, carotid artery tapering (cavernous portion), and anterior communicating artery aneurysm.
prominent feature of moyamoya is intimal fibrocellular thickening and excessive folding and thickening or deficiencies in the internal elastic lamina.15 An arteritis of vessel walls has not been documented. Moyamoya disease should be considered as a potential cause of cerebrovascular accidents, both thrombotic and hemorrhagic, in young individuals. This is especially important since associated aneurysms may be clipped and effectively neutralized. Anticoagulants should be avoided because of the tendency to bleed from aneurysms and pseudoaneurysms. Various surgical interventions may be useful, especially if employed early. Further basic study of the at-risk population and young individuals with the disease(s) may further illuminate its pathophysiology and lead to new surgical and pharmacologic interventions. Literature Cited 1. Takeuchi K. Occlusive disease of the carotid artery. Shinker Shimpo. 1961;5:511-513. 829
MOYAMOYA DISEASE
2. Suzuki J, Takaku A. Cerebral vascular 'Moya Moya' disease: a disease showing abnormal net-like vessels in base of brain. Arch Neurol. 1969;20:288-299. 3. Meriweather RP, Barnett HG, Echols DH. Moya Moya disease as a cause of subarachnoid hemorrhage in a Negro patient. J Neurol Surg. 1976; 44:620-622. 4. Suzuki J, Kodama A. Moya Moya disease-a review. Stroke. 1983;14:104-109. 5. Dumas MP, Girard L, Collomb H. Occlusions bilateraes de la carotide interne associee on une circulation de suppleance cortico-corticale, transdurale, et du type 'Moya Moya' ches l'enfant noire. J Neurol Sci. 1969;1 6:1-25. 6. Stockman JA, Nigro MA, Mishkin MM, Oski FA. Occlusion of large cerebral vessels in sickle cell anemia. N Engl J Med. 1972;287:846-849. 7. Richman DP, Watts HG, Parsons D, Schmid K, Glimcher NJ. Familiar Moya Moya associated with biochemical abnormalities of connective tissue. Neurology. 1977;27:382-386. 8. Tomsick TA, Lukin RR, Chambers AA, Benton C. Neurofibromatosis and intracranial arterial occlusive disease. Neuroradiology. 1976;1 1:229-234.
830
9. Hilal SK, Solomon GE, Gold AP. Primary cerebral arterial occlusive disease in children, part II: neurocutaneous syndromes. Radiology. 1971;99:87-93. 10. Ximin I, Xuzhong R, Zhuan C, Burun Y, Shangpu, Yunhg G. Moya Moya disease caused by leptospiral cerebral arteries. Chin Med J. 1980;93:596-604. 11. Mathew NT, Abraham J, Chandy J. Cerebral angiographic features in tuberculous meningitis. Neurology. 1970;20:1015-1019. 12. Rajakulasingam K, Cerullo J, Raidmond AJ. Childhood Moya Moya syndrome postradiation pathogenesis. Child's Brain. 1979;5:467. 13. Konshi Y, Kadwvaki C, Rum M. Aneurysms associated with Moya Moya disease. Neurosurgery. 1985;4:484-488. 14. Sato M, Kohama A, Fukuda A. Moya Moya-like disease associated with ventricular hemorrhages: report of three cases. Neurosurgery. 1985;17:260-266. 15. Coakman HB, Duehen LW, Scaravilli F. Moya Moya disease: clinical and pathological report of a case with associated myopathy. J Neurol Neurosurg Psychiatry. 1 979;42:289-297.
JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION, VOL. 83, NO. 9
