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Table of Contents    
Year : 2011  |  Volume : 59  |  Issue : 5  |  Page : 733-738

Adult onset moyamoya disease: Institutional experience

Department of Imaging Sciences and Interventional Radiology, Sree Chitra Tirunal Institute for Medical Sciences and Technology, Trivandrum, India

Date of Submission29-May-2011
Date of Decision30-Jun-2011
Date of Acceptance07-Aug-2011
Date of Web Publication22-Oct-2011

Correspondence Address:
Hima Shriniwas Pendharkar
Department of Imaging Sciences and Interventional Radiology, Sree Chitra Tirunal Institute for Medical Sciences and Technology, Trivandrum
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0028-3886.86550

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 » Abstract 

Moyamoya disease is a progressive steno-occlusive disease of bilateral carotid forks with the formation of fine collateral vascular network and is an angiographic diagnosis. We analyzed case records of 11 patients with "adult-onset moyamoya disease." Six patients presented with intracranial hemorrhage (intracerebral and/or intraventricular) and 5 with focal ischemia. Angiography revealed bilateral Internal carotid artery involvement in 8 patients and unilateral involvement in 3. Posterior cerebral artery involvement was seen in 3 patients. Saccular aneurysm involving posterior circulation was seen in only 1 patient. Although rare, adult-onset moyamoya disease should be considered as one of the causes for intracerebral and intraventricular hemorrhage in adults.

Keywords: Adult, angiography, arteries, hemorrhage, moyamoya disease

How to cite this article:
Chinchure SD, Pendharkar HS, Gupta AK, Bodhey N, Harsha K J. Adult onset moyamoya disease: Institutional experience. Neurol India 2011;59:733-8

How to cite this URL:
Chinchure SD, Pendharkar HS, Gupta AK, Bodhey N, Harsha K J. Adult onset moyamoya disease: Institutional experience. Neurol India [serial online] 2011 [cited 2022 Aug 17];59:733-8. Available from: https://www.neurologyindia.com/text.asp?2011/59/5/733/86550

 » Introduction Top

Idiopathic form of moyamoya disease (MMD) remains largely an angiographic diagnosis and is defined as a nonatherosclerotic, noninflammatory, and nonamyloid vasculopathy characterized by chronic progressive stenosis or occlusion of the terminal internal carotid arteries (ICA) and/or the proximal portion of the anterior cerebral arteries (ACA) and/or middle cerebral arteries (MCA). [1] MMD is characterized by irregular perforating vascular collateral networks called moyamoya vessels near the occluded or stenotic regions corresponding to the lenticulostriate and thalamoperforating arteries. These abnormal vessels at the base of the brain were first described by the Japanese-Takeuchi and Shimizu in 1957-as having a "hazy, cloudy puff of smoke" appearance, which led to the term "moyamoya." [1] In view of marked heterogeneity in demographics and clinical presentation of adult-onset idiopathic form of MMD, we reviewed our institutional experience in this article.

 » Materials and Methods Top

Eleven angiographically proven "moyamoya disease" adult patients seen in our institute between January 2006 and November 2010 were included in this study. The clinical details were reviewed from the case records. The imaging features and angiographic findings were also reviewed in detail. Workup for secondary causes of moyamoya was negative in all but 1 patient who had a mitral valve replacement done for rheumatic heart disease. Cross-sectional imaging was available in all the patients: 3 had nonenhanced computed tomography (NECT) scan, whereas 8 patients had magnetic resonance imaging (MRI) out of which 3D TOF angiogram/contrast-enhanced magnetic resonance angiogram (CEMRA) was available in 4 patients. All patients had digital subtraction angiography (DSA) and the diagnosis was based on angiographic images.

 » Results Top

Of the 11 patients [M:F 6:5; mean age 37.1 years (range 25-52 years)], 6 patients presented with intracranial hemorrhage and 5 patients with ischemic focal deficits. Of the 6 patients with intracranial hemorrhage, 4 had intraventricular hemorrhage, 1 had basal ganglia hemorrhage, and the remaining 1 had subdural hemorrhage (SDH); this patient was also on oral anticoagulants. Clinical features, computed tomography, and MRI findings are given in [Table 1]. DSA showed bilateral ICA involvement in 8 patients and unilateral involvement in 3 patients (case 2, 4, and 5). Two patients showed posterior cerebral artery (PCA) stenosis with moyamoya collateralization (case 8, 11). The DSA findings have been detailed in [Table 2]. Of the 11 patients, 3 patients underwent revascularization surgery: 2 underwent superficial temporal artery (STA) -middle cerebral artery (MCA) bypass (case 5, 10) and 1 underwent pial synangiosis (case 3).
Table 1: Clinical presentation and sectional imaging data

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Table 2: Angiographic features

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Illustrative cases

Case 1

B/L MMD with basilar tip aneurysm: A 40-year-old man without known comorbidities presented with sudden onset holocranial headache of few days duration associated with vomiting. Examination revealed no focal neurologic deficit. Imaging [Figure 1] revealed bilateral MMD with a basilar tip aneurysm.
Figure 1: b/l MMD with basilar tip aneurysm: SWI (a) shows bleed in right occipital horn. CEMRA (b) revealed uniform narrowing of bilateral ICA. 3D TOF source image (c) shows multiple tiny collaterals in suprasellar cistern and basilar top bulbosity. SSD image (d) of DSA shows the basilar tip bulbosity. DSA shows severe narrowing of bilateral supraclinoid ICA with abnormal moyamoya collateralization in lenticulostriate region (e,f). Bilateral ECAs are hypertrophied. Vertebral artery injection (g,h) shows filling of bilateral MCA and a fusisaccular aneurysm at basilar top

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Case 5

Unilateral stage II MMD: A 28-year-old lady, 2 months postpartum, presented with transient weakness of right upper and lower limb. Power in upper limb improved completely and improved partially in lower limbs within 24 h. MRI brain did not reveal any infarct. DSA showed short segment occlusion of M1 segment of left MCA with enlarged lenticulostriate collaterals forming distal MCA [Figure 2]. She underwent STA-MCA bypass.
Figure 2: Unilateral stage III moyamoya: Selective injection of right ICA in frontal view (a) does not show any abnormality. Selective injection of left ICA (b,c) shows short segment occlusion of M1 segment of left MCA with enlarged lenticulostriate collaterals forming distal MCA. Posterior circulation was normal (d). Few ECA collaterals noted reperfusing cerebral parenchyma on selective left ECA injection (e)

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Case 11

Bilateral MMD: A 27-year-old lady presented with recurrent episodes of giddiness since last 4 years. At presentation, there was no focal neurologic deficit. Imaging features are illustrated in [Figure 3]. STA-MCA bypass was not possible as distal branches of MCA were not visualized.
Figure 3: Bilateral MMD: 3D TOF MR angiogram source image (a) showed multiple collaterals in the suprasellar cistern. DSA showed bilateral supraclinoid ICA stenosis with nonvisualization of circle of Willis, moyamoya collaterals, and enlarged extracranial collaterals (b,c,f). Left proximal PCA (P1) was stenosed with hypertrophied perforators as seen on left vertebral artery injection (d,e).
(* Suzuki and Takaku: Cerebrovascular "moyamoya" disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 20:288-299, 1969)

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 » Discussion Top

MMD is a primary progressive steno-occlusive disease of bilateral carotid forks with the formation of fine collateral vascular network known as "moyamoya" vessels. [2] The typical dense angiographic blush "puff of smoke" appearance is seen in the arterial phase and represents both hypertrophy of perforator branches and true neoangiogenesis around the circle of Willis. After its first description by Kudo, [3] its etiology still remains unclear. Hereditary, congenital, as well as acquired factors are debated.

Clinical presentation of adult-onset MMD differs from childhood form. About 40%-65% of adults present with intracranial bleed, either intraparenchymal hemorrhage with intraventricular extension or subarachnoid hemorrhage. In children only 10% present with hemorrhage while majority present with focal ischemic deficits. [4] Suzuki and Kodama [5] had shown that adults have less ability to form collateral vessels as compared to children. It has been reported that angiographically evident MMD shows dynamic rapid progression in early childhood till adolescence and slow progression after adolescence with static course in adulthood [6],[7],[8] Females have a higher risk of disease progression than male patients. [9] Suzuki and Takaku [10] had described 6 angiographic stages based on the progression of the disease: Stage 1: Stenosis of distal intracranial ICAs, often bilaterally; Stage 2: Formation of moyamoya collateral vessels at the base of the brain; Stage 3: Further prominence of moyamoya vessels as stenosis of the anterior circulation progresses; Stage 4: severe stenosis or occlusion of the entire circle of Willis along with narrowing of the dilated moyamoya vessels and formation of extracranial collateral networks; Stage 5: Enlargement of extracranial collateral vessels; and Stage 6: Oocclusion of the distal ICAs, disappearance of the basal moyamoya vessels, and cerebral vascularization from extracranial sources only. Two types of collateral from extracranial to intracranial arteries are recognised, ethmoidal and vault. Ethmoidal collaterals arise from ophthalmic artery, anterior and posterior ethmoidal arteries and other branches of external carotid artery (ECA). These are mainly seen in children and represent severity of intracranial disease, while in adults these collaterals are poorly formed irrespective of disease severity. [6] On the other hand, vault moyamoya vessels develop from transdural anastomotic channels from middle meningeal and superficial temporal arteries.

Steno-occlusive lesions in MMD usually begin from terminal portion of ICA or proximal portion of MCA or ACA. Only a few case reports of isolated MCA involvement in the initial stages have been reported. [11],[12] Development of additional posterior cerebral artery (PCA) lesions implies increased risk for recurrent ischemic stroke as the PCA plays an important role as a major collateral channel in moyamoya disease. [13] However, it is observed by Jayakumar et al. [14] that ischemic events in the posterior circulation are infrequent, as the posterior circulation acts as collateral pathway for the diseased anterior circulation till late stages of the disease.

Cerebral aneurysms associated with MMD have been classified as major artery aneurysms and peripheral artery aneurysms. [15],[16] Aneurysms involving circle of Willis are referred as major artery aneurysms while those involving moyamoya collateral vessels are referred as peripheral artery aneurysms. The later have been histologically proven to be pseudoaneurysms and usually arise from moyamoya vessels or collateral vessels. Majority of these aneurysms involve anterior or posterior choroidal arteries, which are dilated as collaterals. [16],[17] Rupture of small moyamoya vessels in the parenchyma adjacent to lateral ventricular wall leads to intracerebral hemorrhage with the hemorrhage from these vessels dissecting into the lateral ventricles. These pseudoaneurysms are shown to disappear on follow-up angiograms. [15] Major cerebral aneurysms associated with moyamoya disease occur more frequently in the vertebrobasilar system [15],[17] due to hemodynamic stress on posterior circulation. Follow-up studies in MMD patients have revealed the relationship between development and enlargement of vertebrobasilar aneurysms. [18] Rupture of these major cerebral vessel aneurysm can present as subarachnoid hemorrhage (SAH). Hence DSA is recommended for SAH in MMD to rule out the presence of a saccular aneurysm on the main arterial trunk. [19] In our study 1 patient (case 1) showed a basilar tip aneurysm.

The existence of unilateral MMD is controversial and MMD can be considered "unilateral" if there are typical angiographic findings on one side with normal/equivocal angiographic findings on the contralateral side. In the series by Kelly et al., [20] 18% of patients had angiographically documented unilateral MMD. The level of basic fibroblast growth factor (bFGF) is not elevated in cerebrospinal fluid (CSF) in patients with unilateral moyamoya disease. [21] Previously thought to be infrequent, however, progression from unilateral to typical bilateral MMD is not rare. [22],[23],[24] Predictors of progression to bilateral form include the following: younger age of onset, Asian heritage, family history, and prior cranial irradiation or cardiac anomalies.
"Ivy sign" mainly seen in anterior MCA territory on noncontrast FLAIR images represents decreased cerebrovascular reserve due to dilated pial vessels with slow retrograde filling from leptomeningeal collaterals. [23] None of our patients showed this sign. MR perfusion imaging in MMD plays an important role by providing hemodynamic information and thus allows monitoring patients on treatment, guides better selection of patients for revascularization surgery and provides baseline for postoperative assessment. [25] The goal of surgery in MMD is to improve blood flow to hypoperfused brain parenchyma by establishing collaterals from ECA branches to ICA territories. Available surgical options are direct like STA-MCA bypass and indirect like pial synangiosis. Both these procedures are effective in adults.

The largest Indian study on MMD was by Garg et al., [25] and included both childhood- and adult-onset MMD. The authors discuss their clinical experience with revascularization procedure in MMD as well as patients who were managed conservatively. In their series of 44 patients, 26 were adults and angiographic imaging features were not discussed in detail. Our report mainly presents adult-onset MMD.

 » References Top

1.Takeuchi K, Shimizu K. Hypoplasia of the bilateral internal carotid arteries. Brain Nerve 1957;9:37-43.  Back to cited text no. 1
2.Takahashi A, Sawamura Y, Houkin K, Kamiyama H, Abe H. The cerebrospinal fluid in patients with moyamoya disease (spontaneous occlusion of the circle of Willis) contains high level of basic fibroblast growth factor. Neurosci Lett 1993;160:214-6.  Back to cited text no. 2
3.Kudo T, Takayama R, Mikawauchi K. Occlusion of the internal carotid artery (In Japanese). Proceedings of Fifteenth Annual Meeting of Japan Neurosurgical Society.1956.  Back to cited text no. 3
4.Nishimoto A. Moyamoya disease. Neurol Med Chir (Tokyo) 1979;19: 221-8.  Back to cited text no. 4
5.Kodama N, Suzuki J. Cerebrovascular Moyamoya disease. Ill Report - The study on the aging of the perforating branches and the possibility of collateral pathway. Neurol Med Chir (Tokyo) 1974;14:55-67.  Back to cited text no. 5
6.Suzuki J, Kodama N. Moyamoya disease-a review. Stroke 1983;14:104-9.  Back to cited text no. 6
7.Ezura M, Yoshimoto T, Fujiwara S, Takahashi A, Shirane R, Mizoi K. Clinical and angiographic follow-up of childhood-onset moyamoya disease. Childs Nerv Syst 1995;11:591-4.  Back to cited text no. 7
8.Houkin K, Yoshimoto T, Kuroda S, Ishikawa T, Takahashi A, Abe H. Angiographic analysis of moyamoya disease-how does moyamoya disease progress? Neurol Med Chir (Tokyo) 1996;36:783-8.  Back to cited text no. 8
9.Kuroda S, Ishikawa T, Houkin K, Nanba R, Hokari M, Iwasaki Y. Incidence and clinical features of disease progression in adult moyamoya disease. Stroke 2005;36:2148-53.  Back to cited text no. 9
10.Suzuki J, Takaku A. Cerebrovascular "moyamoya" disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 1969;20:288-99.  Back to cited text no. 10
11.Tomida M, Muraki M, Yamasaki K. Angiographically verified progression of moyamoya disease in an adult. Case report. J Neurosurg 2000;93:1055-7.  Back to cited text no. 11
12.Choi HY, Lee JE, Jung YH, Cho HJ, Kim DJ, Heo JH. Progression of isolated middle cerebral artery stenosis into moyamoya disease. Neurology 2007;68:954.  Back to cited text no. 12
13.Miyamoto S, Kikuchi H, Karasawa J, Nagata I, Ihara I, Yamagata S. Study of the posterior circulation in moyamoya disease. Part 2: Visual disturbances and surgical treatment. J Neurosurg 1986;65:454-60.  Back to cited text no. 13
14.Jayakumar PN, Vasudev MK, Srikanth SG. Posterior circulation abnormalities in moyamoya disease: A radiological study. Neurol India 1999;47:112-7.  Back to cited text no. 14
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15.Kodama N, Suzuki J. Moyamoya disease associated with aneurysm. J Neurosurg 1978;48:565-9.  Back to cited text no. 15
16.Nagamine Y, Takahashi S, Sonobe M. Multiple intracranial aneurysms associated with moyamoya disease. Case report. J Neurosurg 1981;54:673-6.  Back to cited text no. 16
17.Adams HP Jr, Kassell NF, Wisoff HS, Drake CG. Intracranial saccular aneurysm and moyamoya disease. Stroke 1979;10:174-9.  Back to cited text no. 17
18.Satoh T, Yamamoto Y, Asari S, Sakurai M, Suzuki K. Disappearance and development of cerebral aneurysms in moyamoya disease. Case report. J Neurosurg 1983;58:949-53.  Back to cited text no. 18
19.Aoki N, Mizutani H. Does moyamoya disease cause subarachnoid hemorrhage? Review of 54 cases with intracranial hemorrhage confirmed by computerized tomography. J Neurosurg 1984;60:348-53.  Back to cited text no. 19
20.Kelly ME, Bell-Stephens TE, Marks MP, Do HM, Steinberg GK. Progression of unilateral moyamoya disease: A clinical series. Cerebrovasc Dis 2006;22:109-15.  Back to cited text no. 20
21.Smith ER, Scott RM. Progression of disease in unilateral moyamoya syndrome. Neurosurg Focus 2008;24: E17.  Back to cited text no. 21
22.Kuroda S, Hashimoto N, Yoshimoto T, Iwasaki Y; Research Committee on Moyamoya Disease in Japan. Radiological findings, clinical course, and outcome in asymptomatic moyamoya disease: Results of multicenter survey in Japan. Stroke 2007;38:1430-5.  Back to cited text no. 22
23.Mori N, Mugikura S, Higano S, Kaneta T, Fujimura M, Umetsu A, et al. The leptomeningeal "ivy sign" on fluid-attenuated inversion recovery MR imaging in Moyamoya disease: A sign of decreased cerebral vascular reserve? AJNR Am J Neuroradiol 2009;30:930-5.  Back to cited text no. 23
24.Lee M, Zaharchuk G, Guzman R, Achrol A, Bell-Stephens T, Steinberg GK. Quantitative hemodynamic studies in moyamoya disease: A review. Neurosurg Focus 2009;26: E5.  Back to cited text no. 24
25.Garg AK, Suri A, Sharma BS. Ten-year experience of 44 patients with moyamoya disease from a single institution. J Clin Neurosci 2010;17:460-3.  Back to cited text no. 25


  [Figure 1], [Figure 2], [Figure 3]

  [Table 1], [Table 2]

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