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Moyamoya disease (MMD) is a unique cerebrovascular disease characterized by progressive stenosis of the

distal internal carotid artery (ICA) and a hazy network of basal collaterals. Differentiation of MMD from intracranial atherosclerotic disease (ICAD) is important for the treatment of patients with intracranial occlusive disease (revasculariza-tion surgery for MMD versus aggressive medical treatment for ICAD). However, it is often difficult, especially in Asians, in whom both MMD and ICAD are prevalent.

With the high-resolution magnetic resonance imaging (HR-MRI) techniques, vessel wall imaging findings for dif-ferent causes of intracranial stenosis have been reported.1–3 However, wall imaging of MMD is seldom reported.1,4 In this study, we compared vessel wall imaging findings for MMD and ICAD on HR-MRI in a large cohort.

MethodsPatientsWe prospectively recruited patients ≥18 years with middle cerebral artery (MCA) steno-occlusive disease. Thirty-two patients with digital subtraction angiographically (DSA) proven MMD were enrolled, with 16 patients with acute infarction from ICAD as controls. Diagnosis of

MMD was made with current diagnostic criteria,5,6 and patients who had significant stenosis of relevant artery and did not show basal col-laterals on DSA or time-of-flight MR angiography were categorized under ICAD. Patients with potential sources of cardioaortic embolism, ≥50% extracranial stenosis, or other stroke mechanisms were exclud-ed. Local institutional review boards approved this study. All patients or patients’ guardians provided informed consent.

MRI ProtocolsAll patients underwent 3-Tesla MRI. Three-dimensional (3D), time-of-flight MR angiography of intracranial arteries was initially ob-tained. Black-blood HR-MRI using spatial presaturation technique was performed: (1) axial/sagittal proton-density (repetition time [TR]/echo time [TE]=2150/12.5 ms, echo train length=10, slice thickness=2 mm, flip angle=90°, matrix=280×280, field of view [FOV]=14 cm, number of average=2); (2) axial/sagittal T2-weighted images (TR/TE=2150/100 ms, echo train length=10, slice thickness=2 mm, flip angle=90°, matrix=280×280, FOV=14 cm, number of average=2); (3) sagittal T1 fluid-attenuated inversion recovery pre- and postcontrast (TR/TE=2100/10 ms, inversion time=860 ms, echo train length=6, slice thickness=2 mm, flip angle=90°, matrix=280×280, FOV=14 cm, number of average=2); (4) axial postcontrast 3D T1-weighted volu-metric isotropic turbo spin echo acquisition (VISTA; TR/TE=350/20 ms, turbo spin echo factor=25, 0.5 mm isotropic voxel, flip angle=90°, matrix=360×360, FOV=18 cm, number of average=2).

Background and Purpose—Diagnosis of Moyamoya disease (MMD) is based on the characteristic angiographic findings. However, differentiating MMD from intracranial atherosclerotic disease (ICAD) is difficult. We compared vessel wall imaging findings on high-resolution magnetic resonance imaging between MMD and ICAD.

Methods—High-resolution magnetic resonance imaging was performed on 32 patients with angiographically proven MMD and 16 patients with acute infarcts because of ICAD. Bilateral internal carotid arteries and steno-occlusive middle cerebral artery were analyzed for wall enhancement and remodeling.

Results—Enhancement patterns and distribution were different. Most patients with MMD (90.6%) showed concentric enhancement on distal internal carotid arteries and middle cerebral arteries, whereas focal eccentric enhancement was observed on the symptomatic segment in ICAD. MMD was characterized by middle cerebral artery shrinkage; the remodeling index and wall area were lower in MMD than in ICAD (remodeling index, 0.19±0.11 versus 1.00±0.43; wall area, 0.32±0.22 versus 6.00±2.72; P<0.001).

Conclusions—MMD was characterized by concentric enhancement on bilateral distal internal carotid arteries and shrinkage of middle cerebral artery, regardless of symptoms. (Stroke. 2014;45:2457-2460.)

Key Words: angiography ◼ magnetic resonance imaging ◼ Moyamoya disease

High-Resolution Magnetic Resonance Wall Imaging Findings of Moyamoya Disease

Sookyung Ryoo, MD; Jihoon Cha, MD; Suk Jae Kim, MD; Jin Wook Choi, MD; Chang-Seok Ki, MD; Keon Ha Kim, MD; Pyoung Jeon, MD; Jong-Soo Kim, MD;

Seung-Chyul Hong, MD; Oh Young Bang, MD, PhD

Received January 9, 2014; final revision received May 13, 2014; accepted May 13, 2014.From the Departments of Neurology (S.R., S.J.K., O.Y.B.) and Radiology (J.C., J.W.C., K.H.K., P.J.), Laboratory Medicine and Genetics (C.-S.K.), and

Neurosurgery (J.-S.K., S.-C.H.), Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea.The online-only Data Supplement is available with this article at http://stroke.ahajournals.org/lookup/suppl/doi:10.1161/STROKEAHA.

114.004761/-/DC1.Correspondence to Oh Young Bang, MD, PhD, Department of Neurology, Samsung Medical Center, Sungkyunkwan University, 50 Irwon-dong,

Gangnam-gu, Seoul 135–710, South Korea. E-mail neuroboy50@naver.com© 2014 American Heart Association, Inc.

Stroke is available at http://stroke.ahajournals.org DOI: 10.1161/STROKEAHA.114.004761

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2458 Stroke August 2014

Imaging AnalysisWe evaluated vessel walls of MCA at the site of maximal stenosis or just proximal to the occlusion on 3D time-of-flight MR angiography and bilateral distal ICAs immediately after branching ophthalmic arteries.

The vessel boundaries were traced manually on T2/proton-densi-ty–weighted images. Wall area was estimated as the difference be-tween vessel area and lumen area. Remodeling index was the ratio of vessel area at MCA to the reference vessel. The percentage degree of stenosis was calculated as (1–lumen area of MCA/reference lumen area)×100%. Because most patients with MMD did not have a normal MCA, midbasilar artery served as reference values.

We compared pre- and postcontrast T1 fluid-attenuated inversion recovery images to determine the presence and pattern of enhance-ment. Enhancement was regarded as concentric if it was circumferen-tial or uniform. Enhancement was considered eccentric if it was not 360° circumferential or if the thickest part was more than twice the thinnest part where circumferential enhancement was observed. All the measurement was made blinded to clinical information.

ResultsBaseline CharacteristicsOf 32 patients with MMD, 25 had definite MMD and 7 prob-able MMD; 9 had acute stroke (within 4 weeks), 17 chronic stroke, and 6 asymptomatic. Female and younger patients were more frequent in MMD, whereas diabetes mellitus and dyslipidemia were more common in patients with ICAD (P<0.05; Table 1).

Changes in Vessel Wall and Luminal AreasMMD was characterized by MCA shrinkage (Table 1; Figure). Wall area and Remodeling index were smaller in MMD than in ICAD although the degree of stenosis was higher in patients with MMD (P<0.001).

Enhancement of VesselsPatients with MMD had a distinct pattern and distribution of enhancement (Table 1; Figure). Patients with MMD showed concentric enhancement on distal ICA, regardless of the pres-ence of symptoms (93.3% in symptomatic versus 73.5% in asymptomatic segments). However, in most patients with ICAD, enhancement was observed on symptomatic (68.8%) but not on asymptomatic segments (25.0%; MMD versus ICAD; P<0.001). Many patients with MMD had concentric enhancement, whereas all patients with ICAD except 1 showed eccentric enhancement (P<0.001). Concentric enhancement on bilateral distal ICAs was observed exclusively in patients with MMD (56.3% versus 0%; P<0.001). The pattern and dis-tribution of MCA enhancement was similar to distal ICA in both patients with MMD and patients with ICAD.

Subgroup Analysis of MMDWe performed subgroup analysis to validate our HR-MRI find-ings for MMD. Two distinct findings, MCA shrinkage and con-centric enhancement on distal ICA, were consistent, irrespective of subtype (definite versus probable), angiographic stage (Suzuki grade), or presence of symptoms (acute symptomatic versus chronic symptomatic versus asymptomatic; Table 2).

Receiver Operating Curve AnalysisHR-MRI showed high diagnostic accuracy as DSA. Sensitivity was 90.6% for HR-MRI finding of concentric enhancement of

distal ICA or MCA, 93.8% for MRI finding of thinning of stenotic segment, and 84.4% for both findings. Area under the receiver operating curves were 0.89, 0.91, and 0.92, respec-tively (Figure I in the online-only Data Supplement).

Table 1. Baseline Characteristics and HR-MRI Findings

MMD (n=32) ICAD (n=16) P Value

Age, y 47.8±15.1 60.8±14.8 0.007

Women, n (%) 23 (71.9) 6 (37.5) 0.022

Risk factors

Thyroid disease, n (%) 9 (28.1) 0 (0) 0.302

Hypertension, n (%) 12 (37.5) 8 (50.0) 0.458

Diabetes mellitus, n (%) 4 (12.5) 8 (50.0) 0.012

Dyslipidemia, n (%) 9 (28.1) 10 (62.5) 0.027

History of stroke/TIA, n (%) 6 (18.8) 3 (18.8) >0.999

Coronary artery disease, n (%) 0 (0) 0 (0) N/A

Current smoker, n (%) 4 (12.5) 5 (31.3) 0.239

Laboratory findings

Total cholesterol, mg/dL 169.3±35.5 213.6±41.1 <0.001

Triglyceride, mg/dL 141.0±83.0 176.9±133.3 0.272

High-density lipoprotein cholesterol, mg/dL

46.2±12.3 46.1±13.3 0.974

Low-density lipoprotein cholesterol, mg/dL

101.5±26.7 138.1±37.4 <0.001

C-reactive protein, mg/dL 0.04 (0.03–0.18) 0.08 (0.03–0.24) 0.363

HR-wall MRI findings

MCA stenosis

Wall area, mm2 0.32±0.22 6.00±2.72 <0.001

Remodeling index 0.19±0.11 1.00±0.43 <0.001

Stenosis degree, % 83.6±9.6 72.0±13.5 <0.001

Enhancement on vessels

Distal ICA, n (%) 29 (90.6) 12 (75%) 0.201

MCA, n (%) 18 (56.3) 14 (87.5) 0.030

Enhancement on symptomatic segment*

Distal ICA, n (%) 28 (93.3) 11 (68.8) 0.121

Concentric 23 (82.1) 1 (9.1) <0.001

Eccentric 5 (17.9) 10 (90.9) ...

MCA, n (%) 19 (63.3) 14 (87.5) 0.302

Concentric 18 (94.7) 1 (7.1) <0.001

Eccentric 1 (1.7) 13 (92.9) ...

Enhancement on asymptomatic segment*

Distal ICA, n (%) 25 (73.5) 4 (25.0) <0.001

Concentric 21 (84.0) 0 (0) 0.005

Eccentric 4 (16.0) 4 (100) ...

MCA, n (%) 6 (22.2) 2 (12.5) >0.999

Concentric 4 (66.7) 0 (0) >0.999

Eccentric 2 (33.3) 2 (100) ...

Bilateral concentric enhancement on distal ICAs, n (%)

18 (56.3) 0 (0) <0.001

HR indicates high-resolution; ICA, internal carotid artery; ICAD, intracranial atherosclerotic disease; MCA, middle cerebral artery; MMD, Moyamoya disease; MRI, magnetic resonance imaging; and TIA, transient ischemic attack.

*Of all 64 MMD segments, 30 were symptomatic and 34 were asymptomatic. ICAD showed 16 symptomatic and 16 asymptomatic segments.

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Ryoo et al HR-Wall MRI in Moyamoya Disease 2459

DiscussionThe main findings of this study were that MMD was char-acterized by shrinkage of MCA and concentric enhance-ment on bilateral distal ICAs and MCA on HR-wall MRI, regardless of symptoms or stages. These are the first HR-MRI data comparing MMD with ICAD for a relatively large cohort.

HR-MRI wall imaging of MMD has been previously reported. Two case series reported no thickening or enhance-ment in patients with MMD.1,4 However, the case number was small, with little data on the presence or acuteness of symptoms or MMD severity. In our study of 32 patients with MMD of various stages, HR-wall MRI consistently showed a small vessel diameter, thin vessel wall, and diffuse concentric

Figure. Cases of Moyamoya disease (MMD) and intracranial atherosclerotic disease (ICAD) and a normal control showing different high-resolution MRI findings. A, MMD showing shrinking middle cerebral artery (MCA; arrows) and concentric enhancement on bilateral distal internal carotid arteries (ICAs; arrowheads). B, Thick MCA with positive remodeling (arrows) in ICAD. Enhancement of the left distal ICA is eccentric (arrowhead). C, Normal control has MCA without shrinkage or plaque and no enhancement on distal ICAs. PD indicates proton-density; and T1CE, T1 contrast-enhanced.

Table 2. Subgroup Analysis of High-Resolution-Wall MRI Findings

MMD Subtype Definite (n=25) Probable (n=7)Suzuki 1–3

(n=16)Suzuki 4–6

(n=16)Symptomatic

(n=26)Asymptomatic

(n=6)

Acute Symptomatic

(n=9)

Chronic Symptomatic

(n=17)

MCA stenosis

Wall area, mm2 0.32±0.24* 0.35±0.16* 0.35±0.24* 0.30±0.21* 0.34±0.24* 0.28±0.16* 0.34±0.34* 0.33±0.15*

Remodeling index 0.18±0.09* 0.26±0.16† 0.22±0.12* 0.16±0.09* 0.19±0.10* 0.19±0.15† 0.15±0.08* 0.22±0.11*

Stenosis degree, % 84.3±9.6‡ 81.0±9.7 81.9±10.0‡ 85.4±9.1 83.0±10.2‡ 85.7±7.2 87.9±5.1† 79.9±11.4

Enhancement on vessels

Distal ICAs, n (%)

Concentric 41 (87.2)* 3 (60.0) 26 (86.7)* 18 (81.8)* 38 (84.4)* 6 (85.7)† 15 (88.2)* 23 (82.1)*

Eccentric 6 (12.8) 2 (40.0) 4 (13.3) 4 (18.2) 7 (15.6) 1 (14.3) 2 (11.8) 5 (17.9)

MCAs, n (%)

Concentric 20 (87.0)* 2 (100) 13 (86.7)* 9 (90.0)* 21 (87.5)* 1 (100) 9 (100)* 12 (80.0)*

Eccentric 3 (13.0) 0 (0) 2 (13.3) 1 (10.0) 3 (12.5) 0 (0) 0 (0) 3 (20.0)

ICA indicates internal carotid artery; MCA indicates middle cerebral artery; and MMD, Moyamoya disease.All P values were compared with intracranial atherosclerotic disease. *P<0.001, †P<0.01, ‡P<0.05.

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2460 Stroke August 2014

enhancement. Our MRI findings are consistent with recent advances in the understanding of the pathogenesis of MMD and ICAD (Figure II in the online-only Data Supplement). There is increasing evidence that MMD is primarily a pro-liferative disease of the intima. Intimal hyperplasia from pro-liferation of smooth muscle cells or endothelium can cause stenosis.7–10 Therefore, diffuse concentric enhancement within vessels could represent hyperproliferation of the vessel wall components, whereas focal eccentric enhancement in patients with ICAD could represent focal atherosclerotic plaque.11 Second, in contrast to proliferative changes of the intima, MMD was also characterized by thinned media. Caspase-dependent apoptosis and overproduction of matrix metallo-proteinase have been implicated as contributory mechanisms in the associated degradation or remodeling of the arterial wall.12,13 Therefore, diffuse and severe thinning of the wall area in our patients with MMD with could represent media shrinkage, which was not observed in our patients with ICAD.

Our data indicated that HR-wall MRI could be an imaging biomarker specific to MMD. The frequency of characteristic HR-wall MRI findings did not differ by MMD stage (Suzuki grade) or subtype (definite versus probable), or the presence or acuteness of symptoms (acute symptomatic versus remote symptomatic versus asymptomatic). In contrast, none of our patients with ICAD showed characteristic HR-wall MRI find-ings of both diffuse concentric enhancement and shrinkage on the affected segment. Our receiver operating characteristic curves showed that HR-MRI findings had a diagnostic accu-racy for DSA-proven MMD, which raises the possibility of noninvasive diagnosis of MMD (Figure I in the online-only Data Supplement).

Our study has limitations. First, patients with steno-occlu-sive disease other than MMD could have been included in the MMD group because no biomarkers or imaging tools are specific for MMD. However, all MMD cases were confirmed by DSA. Second, additional studies with histological confir-mation are needed. Finally, the wall enhancement observed in our patients may have been because of luminal (and not wall) enhancement coming from slow-moving blood adjacent to the wall of the vessel (pseudoenhancing or slow flow arti-fact). Additional studies using true double-inversion recov-ery sequences are needed. However, in patients with MMD, enhancement was often observed on the nonstenosed segment, either asymptomatic side or nonstenosed distal ICA, on time-of-flight -MR angiography. On the contrary, enhancement was rarely observed on the asymptomatic stenosed segment in patients with ICAD.

In conclusion, MMD was characterized by concentric enhancement on bilateral distal ICAs and shrinkage of MCA. These findings were consistent regardless of clinicoradiologi-cal characteristics. These distinct radiological findings could help explain the pathogenesis of MMD and differentiate MMD from ICAD.

Sources of FundingThis study was supported by the National Research Foundation of Korea, Ministry of Science, ICT (Information, Communication, Technology) and Future Planning (2011–0019389).

DisclosuresNone.

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8. Chmelova J, Kolar Z, Prochazka V, Curik R, Dvorackova J, Sirucek P, et al. Moyamoya disease is associated with endothelial activity detected by anti-nestin antibody. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 2010;154:159–162.

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Pyoung Jeon, Jong-Soo Kim, Seung-Chyul Hong and Oh Young BangSookyung Ryoo, Jihoon Cha, Suk Jae Kim, Jin Wook Choi, Chang-Seok Ki, Keon Ha Kim,

High-Resolution Magnetic Resonance Wall Imaging Findings of Moyamoya Disease

Print ISSN: 0039-2499. Online ISSN: 1524-4628 Copyright © 2014 American Heart Association, Inc. All rights reserved.

is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231Stroke doi: 10.1161/STROKEAHA.114.004761

2014;45:2457-2460; originally published online June 19, 2014;Stroke. 

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SUPPLEMENTAL MATERIALS

Supplemental figure I. ROC analysis

Participants were 32 MMD and 16 ICAD patients. Diagnostic accuracy of HR-MRI findings

as (a) concentric enhancement of distal ICA and/or MCA, (b) thinning of stenotic segment

(RI < 0.4), or (c) both were evaluated. Receiver operating characteristic (ROC) curves were

used to compare discrimination power of conventional angiographic MMD criteria and HR-

MRI criteria.

Criteria using HR-MRI showed high diagnostic accuracy as digital subtraction angiography.

Sensitivity was 90.6% for HR-MRI finding of concentric enhancement of distal ICA and/or

MCA, 93.8% for MRI finding of thinning of stenotic segment, and 84.4% for both findings.

Area under the ROC curves (AUC) were 0.89, 0.91, and 0.92, respectively.

Supplemental figure II. Histological characteristics of MMD and ICAD1-10

Included figures are reprinted from Yin et al1, Copyright (2010), with permission from

Wolters Kluwer Health (right panel) and from Kuroda et al4, Copyright (2008), with

permission from Elsevier (left panel).

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plaques. Virchows Archiv. A: Pathology. Pathologische Anatomie. 1973;361:97-108

3. Kolodgie FD, Nakazawa G, Sangiorgi G, Ladich E, Burke AP, Virmani R. Pathology of

atherosclerosis and stenting. Neuroimaging clinics of North America. 2007;17:285-301, vii

4. Kuroda S, Houkin K. Moyamoya disease: Current concepts and future perspectives. Lancet

neurology. 2008;7:1056-1066

5. Takagi Y, Kikuta K, Nozaki K, Hashimoto N. Histological features of middle cerebral arteries

from patients treated for moyamoya disease. Neurologia medico-chirurgica. 2007;47:1-4

6. Oka K, Yamashita M, Sadoshima S, Tanaka K. Cerebral haemorrhage in moyamoya disease

at autopsy. Virchows Archiv. A, Pathological anatomy and histology. 1981;392:247-261

7. Chmelova J, Kolar Z, Prochazka V, Curik R, Dvorackova J, Sirucek P, et al. Moyamoya

disease is associated with endothelial activity detected by anti-nestin antibody. Biomedical

papers of the Medical Faculty of the University Palacky, Olomouc, Czechoslovakia.

2010;154:159-162

8. Lin R, Xie Z, Zhang J, Xu H, Su H, Tan X, et al. Clinical and immunopathological features of

moyamoya disease. PloS one. 2012;7:e36386

9. Nanba R, Kuroda S, Ishikawa T, Houkin K, Iwasaki Y. Increased expression of hepatocyte

growth factor in cerebrospinal fluid and intracranial artery in moyamoya disease. Stroke; a

journal of cerebral circulation. 2004;35:2837-2842

10. Takagi Y, Kikuta K, Nozaki K, Fujimoto M, Hayashi J, Imamura H, et al. Expression of

hypoxia-inducing factor-1 alpha and endoglin in intimal hyperplasia of the middle cerebral

artery of patients with moyamoya disease. Neurosurgery. 2007;60:338-345; discussion 345