Angiographic Staging Research Articles

Abstract 51: Peripheral Regulatory T cells and Th17 Cells Is Associated With Pathogenesis of Moyamoya Disease

Background: Despite unclear pathogenesis, previous studies have suggested immune responses may play a pivotal role in the process of Moyamoya disease (MMD), a rare cerebrovascular occlusive disorder. The objective of this study is aimed to explore the change of peripheral Treg/Th17 in MMDpatients and whether the change is associated with pathogenesis of MMD. Methods: In the present study, we collected 26 MMD patients diagnosed by angiography according to the diagnostic criteria of definitive MMD and recruited 32 healthy volunteers. To explore the balance of peripheral Treg/Th17 in MMD patients, lymphocytes in peripheral blood were harvested and flow cytometry was used to measure the percentage of Treg and Th17in CD4+ Tcells, respectively. Meanwhile, relevant cytokines in serum were measured to evaluate the function of Treg and Th17 cells. Results: According to Suzuki’s angiographic staging of moyamoya disease, patients were divided into subgroups of the preliminary-term, medium-term and late-term. Cerebral hemorrhage is thefirstsymptom of onset occuringin half of patients, followed bycerebral ischemia.Our data revealed that both the percentage of Treg and Th17 cells in peripheral blood lymphocytes was increased in MMD patients compared with volunteer group. Meanwhile, the levels of IL-6, IL-10,IL-12, IL-17, TNF-α, VEGF and TGF-β in serum were significantly increased in MMD patients. In this study, the level of HMGB-1, a middle-late period inflammation biomarker, in serum of MMD patients is obviously elevated compared with volunteers. However, the ratio of Treg/Th17 had no significant difference in MMD patients compared to healthy volunteers. Intriguingly, our data revealed that ratio of Treg/Th17 was significantly increased in late-term MMD patients compared with medium-term patients as evidenced by elevated percentage of Treg cells.. In addition, TGF-β level in later-term MMD patients was significantly higher than this in medium-term MMD patients. No difference was observed in the way of onset and gender between two groups. Conclusion: Enhanced peripheral Treg and Th17 in MMD patients suggested that there may be an immunological component in the pathogenesis of MMD. Peripheral Treg may be associated with pathological process of MMD.

Surgical outcomes following encephaloduroarteriosynangiosis in adult moyamoya disease associated with Type 2 diabetes.

OBJECTIVE Debate exists regarding the merits and shortcomings of an indirect bypass procedure for treating adult patients with moyamoya disease (MMD). Considerable variation in neovascularization occurs among different organs in patients with diabetes mellitus. Here, the effect of encephaloduroarteriosynangiosis on MMD associated with Type 2 diabetes mellitus (T2DM) is evaluated. METHODS A retrospective and 1:2 matched case-control study was conducted in moyamoya patients with or without T2DM (n = 180). Postoperative collateral formations were graded according to the Modified Collateral Grading System that originated from the Matsushima Angiographic Stage Classification. Neurological function outcomes before and after the operation were evaluated according to the modified Rankin Scale. Univariate and multivariate logistic regression analyses were performed to determine the risk factors for clinical outcome. RESULTS There was no statistically significant difference in the constituent ratios of initial symptom and preoperative Suzuki stage between patients with and without T2DM. Progression of angiopathy around the circle of Willis was postoperatively observed in bilateral internal carotid arteries in both groups. Patients with T2DM had a higher postoperative Suzuki stage (p < 0.01) and more frequent development of collateral angiogenesis germinating from the external carotid after indirect revascularization procedures in the surgical cerebral hemisphere (82.7% vs 72.2%; p < 0.05). The extent of postoperative collateral formation in patients with diabetes mellitus was significantly higher (p < 0.01). Postoperative clinical improvement in the diabetes group was more common after revascularization procedures (p < 0.05), and the diabetes group had lower modified Rankin Scale scores (p < 0.05) in comparison with the nondiabetes group. Late postoperative stroke and posterior cerebral artery involvement were identified as predictors of unfavorable clinical outcome in both groups, while T2DM was associated with a favorable clinical outcome. CONCLUSIONS Encephaloduroarteriosynangiosis is an efficacious treatment for adult patients with MMD. Patients with T2DM could achieve better collateral circulation and clinical improvement following surgery.

0489: Interest of the calcium score in addition to the J-CTO score for grading CTO difficulty for PCI

To evaluate the incremental interest of performing a calcium score before CTO procedures, compared to the angiographic J-CTO score alone. Prospective cohort of 109 consecutive patients with 119 de novo CTO lesions. Angiographic grading with the J-CTO score was compared with CT + angiographic staging (calcium score cut off>400) and a “corrected” J-CTO score, by ROC curve analysis to predict a successful recanalization. Thirty-two lesions (27%) had a calcium score >400.13 (11%) patients were reclassified in the “corrected” J-CTO score because calcifications were not seen in the angiogram. The factors significantly associated with the failure of the procedure were J-CTO score (OR 0.486 [0.32-0.73], p<0.001), corrected J-CTO score (OR 0.494 [0.33-0.73], p<0.001), a blunt lesion (OR 0399 [0182-0871], p=0.021) and a second attempt (OR 0322 [0121-0856], p=0.110). The calcium score >400 was not found associated with the failure of the procedure (OR 0.545 [0239-1243], p<0.149). By multivariate analysis, both J-CTO score (OR 0.645 [0418-0995], p=0.047) and the corrected J-CTO score (OR 0.631 (0410-0972] were significantly associated with a successful recanalization. However, calibration of the corrected J-CTO score was less good than the angiographic J-CTO score alone. This study suggested that calcium score evaluation before CTO procedures is not useful for grading PCI difficulty. Abstract 0489 – Figure: ROC curves analysis to predict success of the CTO

Clinical features and disease progression in moyamoya disease patients with Graves disease.

The present study aimed to clarify the incidence and clinical features of disease progression in adult moyamoya disease (MMD) patients with Graves disease (GD) for better management of these patients. During the past 18 years, 320 adult Chinese patients at West China Hospital were diagnosed with MMD, and 29 were also diagnosed with GD. A total of 170 patients (25 with GD; 145 without GD) were included in this study and were followed up. The mean follow-up was 106.4 ± 48.6 months (range 6-216 months). The progression of the occlusive lesions in the major intracranial arteries was measured using cerebral angiography and was evaluated according to Suzuki's angiographic staging. Information about cerebrovascular strokes was obtained from the records of patients' recent clinical visits. Both angiographic progression and strokes were analyzed to estimate the incidences of angiographic progression and strokes using Kaplan-Meier analysis. A multivariate logistic regression model was used to test the effects of sex, age at MMD onset, disease type, strokes, and GD on the onset of MMD progression during follow-up. During follow-up, the incidence of disease progression in MMD patients with GD was significantly higher than in patients without GD (40.0% vs 20.7%, respectively; p = 0.036). The interval between initial diagnosis and disease progression was significantly shorter in MMD patients with GD than in patients without GD (p = 0.041). Disease progression occurred in both unilateral MMD and bilateral MMD, but the interval before disease progression in patients with unilateral disease was significantly longer than in patients with bilateral disease (p = 0.021). The incidence of strokes in MMD patients with GD was significantly higher than in patients without GD (48% vs 26.2%, respectively; p = 0.027). The Kaplan-Meier survival curve showed significant differences in the incidence of disease progression (p = 0.038, log-rank test) and strokes (p = 0.031, log-rank test) between MMD patients with GD and those without GD. Multivariate analysis suggested that GD may contribute to disease progression in MMD (OR 5.97, 95% CI 1.24-33.76, p = 0.043). The incidence of disease progression in MMD patients with GD was significantly higher than that in MMD patients without GD, and GD may contribute to disease progression in MMD patients. The incidence of strokes was significantly higher in MMD patients with GD than in patients without GD. Management guidelines for MMD patients with GD should be developed.

Current status of revascularization surgery for Moyamoya disease: special consideration for its 'internal carotid-external carotid (IC-EC) conversion' as the physiological reorganization system.

Moyamoya disease is a chronic cerebrovascular disease with unknown etiology, which is characterized by bilateral steno-occlusive changes at the terminal portion of the internal carotid artery and an abnormal vascular network formation at the base of the brain. Moyamoya disease is known to have unique and dynamic nature to convert the vascular supply for the brain from internal carotid (IC) system to the external carotid (EC) system, as indicated by Suzuki's angiographic staging established in 1969. Insufficiency of this 'IC-EC conversion system' may result in cerebral ischemia, as well as in intracranial hemorrhage from inadequate collateral vascular network, both of which represent the clinical presentation of moyamoya disease. Therefore, surgical revascularization by extracranial-intracranial bypass is the preferred procedure for moyamoya disease to complement 'IC-EC conversion' and thus to avoid cerebral infarction and/or intracranial hemorrhage. Long-term outcome of revascularization surgery for moyamoya disease is favorable, but rapid increase in cerebral blood flow on the affected hemisphere could temporarily cause unfavorable phenomenon such as cerebral hyperperfusion syndrome. We would review the current status of revascularization surgery for moyamoya disease based on its basic pathology, and sought to discuss the significance of measuring cerebral blood flow in the acute stage and intensive perioperative management.

Patterns of Cerebral Ischemia in Children With Moyamoya

BackgroundMoyamoya disease is characterized by progressive cerebrovascular stenosis with recurrent cerebral ischemic events. Transient ischemic attacks are often associated with hyperventilation in children with moyamoya, suggesting hypoperfusion rather than thrombotic vaso-occlusion as a prominent mechanism. The patterns of ischemia and severity of steno-occlusive disease in such children may elucidate these mechanisms. MethodsChildren, 1 month to 18 years, with moyamoya, observed over 11 years were analyzed. A study neuroradiologist reviewed all presurgical neuroimaging. Ischemic injury was categorized into cortical, subcortical, and watershed infarction. Angiographic findings were staged using a standardized method. ResultsTwenty children, 15 girls, median age 6.4 years, were included. All children had magnetic resonance imaging and angiography, and in 16, conventional angiography was available. All 40 hemispheres, in 20 children, were evaluated. The initial clinical presentation included neurological deficits in 17, recurrent transient ischemic attacks in 7, headache in 8, seizures in 8, and alteration in consciousness in 4 children. Infarcts were bilateral in 13 (65%) children (ischemia alone in 14, ischemic stroke with hemorrhagic transformation in two, and primary hemorrhage in two). Infarcts were cortical and/or subcortical in 13 (65%), both deep and cortical watershed in 11 (55%), and cortical watershed alone in 5 (25%) children. The predominant vascular territory involved was the middle cerebral artery. The internal carotid arterial system was involved in all, with stage IV being the most frequent angiographic stage. ConclusionsIschemic injury in deep watershed zones is common in childhood moyamoya and may reflect non–vaso-occlusive ischemic mechanisms. Location and severity of vascular involvement may correlate with various patterns of ischemic infarction in moyamoya disease and requires further study.

Clinical Course of Asymptomatic Adult Moyamoya Disease

Background: As regular medical check-ups are becoming more common, the prevalence of asymptomatic moyamoya disease (MMD) is increasing. However, the definition and clinical features are still unclear. The lack of precision has hampered the establishment of guidelines for the management of asymptomatic MMD. The purpose of this study was to define and clarify the clinical characteristics of asymptomatic MMD in adults. Methods: We identified all adults (aged ≥18 years) with MMD who underwent digital subtraction angiography or magnetic resonance angiography at our institution from 1995 through 2010. The authors defined asymptomatic MMD as asymptomatic or nonspecific symptom without any infarction or ischemia on magnetic resonance imaging. In our MMD registry, 40 patients (74 hemispheres) were identified and enrolled in this retrospective cohort study. Their demographic, radiological and clinical findings were evaluated. The log-rank test was used to assess prognostic factors. Pearson's correlation test and the Mann-Whitney U test were used to identify correlation angiographic staging and age or perfusion status. Results: Overall, 6 patients underwent indirect bypass surgery and 36 received antiplatelet medication. On initial single positron emission tomography (35 patients, 67 affected hemispheres), basal and acetazolamide stress brain perfusion were decreased in 19 (28.4%) and 22 (32.8%) hemispheres, respectively. Among 70 angiographically evaluated hemispheres, 6 were unilateral MMD; 27 of 64 affected hemispheres (42.2%) had transdural collateral at evaluation. Age (p = 0.309, Pearson's correlation test) and hemodynamic impairment (p = 0.614, Mann-Whitney U test) did not correlate with angiographic staging. During a median 32-month (range 6-203) clinical follow-up, 3 nonsurgically treated patients had a transient ischemic attack, which was associated with decreased vascular reserve (p < 0.001, log-rank test) and smoking (p = 0.017). Other variables did not show a significant association with clinical progression. During a median 24-month (range 12-108) radiological follow-up, 3 patients displayed angiographic progression and 3 displayed new hemodynamic abnormalities. Radiological progressions were related to hypertension only (p = 0.022). In this case series, there was no case of ischemic or hemorrhagic stroke. Conclusion: The findings suggest that asymptomatic MMD in adults is not a stable disease in our definition. However, stroke rate (0%) was lower than previous reports. Lifestyle modification, stroke risk factor control and/or antiplatelet medication seem to be appropriate initial treatments for patients with normal cerebrovascular reserve. A clear definition of asymptomatic MMD and further clarification of its clinical course are needed to set precise treatment guidelines.

Clinical and Angiographic Features and Stroke Types in Adult Moyamoya Disease

This study was conducted to elucidate the association between clinical and angiographic characteristics and stroke types in adult Moyamoya disease that has been rarely evaluated. We analyzed the clinical and radiologic data obtained from a retrospective adult Moyamoya disease cohort with acute strokes, which were classified into 7 categories: large-artery infarct, hemodynamic infarct, perforator infarct, deep intracerebral hemorrhage, lobar intracerebral hemorrhage, intraventricular hemorrhage, and SAH. With conventional angiography, which was performed in the hemispheres with acute strokes, the Suzuki angiographic stage, intracranial aneurysm, major artery occlusion, and collateral vessel development were confirmed within 1 month of stroke onset. This study included 79 patients with acute ischemic stroke and 96 patients with acute hemorrhagic stroke. The angiographic stage had a strong tendency to be more advanced in the hemorrhagic than the ischemic patients (P = .061). Intracranial aneurysms were more frequently found in the hemorrhagic than ischemic or control hemispheres (P = .002). Occlusions of the anterior cerebral artery and development of fetal-type posterior cerebral artery were more frequently observed in the hemorrhagic than the ischemic (P = .001 and .01, respectively) or control hemispheres (P = .011 and .013, respectively). MCA occlusion (P = .039) and collateral flow development, including the ethmoidal Moyamoya vessels (P = .036) and transdural anastomosis of the external carotid artery (P = .022), occurred more often in the hemorrhagic than the ischemic hemispheres. Anterior cerebral artery occlusion occurred more frequently in patients with deep intracerebral hemorrhage or intraventricular hemorrhage than with lobar intracerebral hemorrhage (P = .009). In adult Moyamoya disease, major artery occlusion and collateral compensation occurred more often in the hemorrhagic than in the ischemic hemispheres. Thus, anterior cerebral artery occlusion with or without MCA occlusion and intracranial aneurysms may be the main contributing factors to hemorrhagic stroke in adult patients with Moyamoya disease.

Practical Clinical Use of Dynamic Susceptibility Contrast Magnetic Resonance Imaging for the Surgical Treatment of Moyamoya Disease

Precise evaluation of hemodynamic stress is important for the treatment of moyamoya disease (MMD). To explore whether dynamic susceptibility contrast magnetic resonance imaging could predict the effects and risk of indirect bypass surgery on MMD. Clinical data of patients with MMD who were evaluated preoperatively and postoperatively with dynamic susceptibility contrast magnetic resonance imaging and digital subtraction angiography were evaluated retrospectively. Indirect bypass surgery was performed on 115 hemispheres of 69 patients (mean age, 15 years; range, 3-54 years). We examined the correlations of ischemic events and revascularization with the mean transit time (MTT) delay to cerebellum. The hemispheres that caused the ischemic events (responsible hemisphere) had a significantly longer preoperative MTT delay than the nonresponsible hemispheres (2.66 ± 1.34 vs 1.57 ± 1.09 seconds). The postoperative MTT delay fell significantly in the patients whose symptoms disappeared (preoperative, 2.61 ± 1.35 seconds; postoperative, 1.35 ± 0.96 seconds). Perioperative infarction occurred in 4 hemispheres (3.5%), and the MTT delay was significantly longer in those hemispheres than in the others (3.97 ± 1.20 vs 2.38 ± 1.34 seconds). The MTT delay was significantly longer in patients with higher angiographic stages. Indirect bypass surgery ameliorated the MTT delay to the same degree in adults and children. Digital subtraction angiography revealed that the induced revascularization was far superior in areas with longer MTT delays. Dynamic susceptibility contrast magnetic resonance imaging proved to be a useful clinical imaging method for patients with MMD. It may be helpful for selecting candidates for MMD intervention and for predicting the effects and risks of surgery. DSC-MRI, dynamic susceptibility contrast magnetic resonance imagingMMD, moyamoya diseaseMTT, mean transit timeROI, region of interest.

Impaired Dynamic Cerebral Autoregulation in Moyamoya Disease

Moyamoya disease (MMD) is a cerebrovascular disease with unknown etiology, characterized by progressive stenosis of the internal carotid artery (ICA). The predominant feature of MMD is the “puff-of-smoke” vessels at the base of the brain, where the pathology of vascular network known as the dilated perforating arteries function as collateral pathways, to compensate for the reduced perfusion [1]. However, it was shown that this compensative mechanism may impair the function of arterioles and thus autoregulation [2,3], which is a protective mechanism that maintains cerebral blood flow constant despite variations in arterial blood pressure (ABP). It remains unknown from which stage this protective mechanism begins to impair and how the dysautoregulation is in association with the stages of MMD. We therefore applied a noninvasive method to investigate the autoregulation at different angiographic stages of MMD

Abstract TP158: Angiographic Feature And Stroke Presentation Of Adult Moyamoya Disease

Background and Purpose: Adult moyamoya disease (MMD) has a different clinical presentation compared as pediatric MMD. The present study was conducted to elucidate the correlation of angiographic characteristics and stroke presentation in adult MMD patients. Methods: We conducted a retrospective analysis of radiologic features of 315 adult patients with definite moyamoya disease which was proved by digital subtraction angiography according to the guidelines of the Research Committee on Spontaneous Occlusion of the Circle of Willis (MMD) of the Ministry of Health and Welfare in 1997. Comparison of angiographic stage and stroke patterns for 630 hemispheres was performed according to stroke presentation. Results: The mean age of diagnosis was 41.5 ( ± 11.7) years. Male to female ratio was 1 to 1.85. One hundred eighty five patients (57.8%) experienced the acute stroke at diagnosis. There was stroke episode prior to diagnosis in 139 patients (43.4%). Among 63 patients (19.7%) who had not experienced any stroke, there was TIA in 44 (13.7%) and no symptoms in 19 (5.9%). Angiographic stage was 50 in 1 (7.8%), 170 in 2 (26.6%), 221 in 3 (35.5%), 129 in 4 (20.2%), 61 in 5 (9.5%) and 9 in 6 (1.4%). Stroke rates were significantly different according to angiographic stage (P=0.041). The occlusion of middle cerebral artery was a significant association with ipsilateral acute stroke (P=0.01). The occlusion of anterior cerebral artery (ACA), middle cerebral artery (MCA), fetal-type posterior cerebral artery was significantly associated with stroke type (P=0.001, 0.002, 0.018). Cerebral blood flow and cerebral vascular reactivity were also strongly associated with ipsilateral acute stroke (P&lt;0.001). Conclusions: In adult moyamoya disease, angiographic stage, MCA occlusion and hemodynamic status are associating factors with stroke development. Occlusion patterns of major arteries are different according to stroke type.

Abstract TMP37: Adult Moyamoya Disease : Clinical Presentation, Treatment Outcome and Prognostic Factor

Background and Purpose: This study was aimed to investigate treatment results and outcome predictors in adult patients with moyamoya disease. Methods: During the period from 2000 to 2011, a clinical database of adult patients with definite moyamoya disease were collected retrospectively from 8 participating centers in Korea during the period from 2000 to 2011. Among total 399 elligible patients, 355 cases were evaluated about clinical and radiological outcomes through medical records. Stroke-free survival rate and prognostic factors for stroke recurrence were measured by Kaplan-Meier and Cox regression methods. Neurologic outcome was assessed according to surgical revascularization and conservative observation. Results: The mean age of symptom onset was 39.4 ( ± 13.8) years. Male to female ratio was 1 to 2.16. Presenting symptoms were ischemia in 197 (55.5%), hemorrhage in 118 (33.2%), and asymptomatic in 40 (11.3%) patients. The median follow-up was 34.3 months (range 0.4 to 284.8). One hundred thirty seven (38.6%) of the 355 patients received observational conservative management. The remaining 218 (61.4%) patients underwent one of direct, indirect or combined revascularization. In the total adult moyamoya patients, 5 year stroke-free survival rate of surgery and observation group was 82.8% vs 73.4%, respectively. In the ischemic moyamoya cases, 5 year stroke-free survival rate of surgery and observation group was 80.9% vs 76.2%, respectively. In the hemorrhagic moyamoya cases, 5 year stroke-free survival rate of surgery and observation group was 83.7% vs 70.1%, respectively. In the asymptomatic cases, 5 year stroke-free survival rate of surgery and observation group was 95.3% vs 83.1%. There was no significant difference between surgical and observation group in Kaplan Meier Survival analysis. Angiographic stage was only a significant factor for stroke recurrence (HR 3.275, 95% CI; 1.251-8.575, P=0.016). Neurologic outcome tended to be better in the surgical group than the observation group (88.5% vs 81.8%, P=0.074) Conclusions: In adult moyamoya patients, the long-term prognosis of surgical treatment may be better than that of conservative observation under real-world setting. Angiographic stage is a predictor of future stroke

Moyamoya disease: a summary

Moyamoya, meaning a "hazy puff of smoke" in Japanese, is a chronic, occlusive cerebrovascular disease involving bilateral stenosis or occlusion of the terminal portion of the internal carotid arteries (ICAs) and/or the proximal portions of the anterior cerebral arteries and middle cerebral arteries (MCAs). The Ministry of Health and Welfare of Japan has defined 4 types of moyamoya disease (MMD): ischemic, hemorrhagic, epileptic, and "other." The ischemic type has been shown to predominate in childhood, while the hemorrhagic type is more often observed in the adult population. The highest prevalence of MMD is found in Japan, with a higher female to male ratio. Studies have shown a possible genetic association of MMD linked to chromosome 17 in Japanese cases as well as in cases found in other demographics. During autopsy, intracerebral hematoma is found and most commonly serves as the major cause of death in patients with MMD. Moyamoya vessels at the base of the brain are composed of medium-sized or small muscular arteries emanating from the circle of Willis, mainly the intracranial portions of ICAs, anterior choroidal arteries, and posterior cerebral arteries, forming complex channels that connect with distal positions of the MCAs. Off of these channels are small tortuous and dilated vessels that penetrate into the base of the brain at the site of the thalamoperforate and lenticulostriate arteries. On angiography, there is the characteristic stenosis or occlusion bilaterally at the terminal portion of the ICAs as well as the moyamoya vessels at the base of the brain. Six angiographic stages have been described, from Stage 1, which reveals a narrowing of the carotid forks, to Stage 6, in which the moyamoya vessels disappear and collateral circulation is produced solely from the external carotid arteries. Cases with milder symptoms are usually treated conservatively; however, more severe symptomatic cases are treated using revascularization procedures. Surgical treatments are divided into 3 types: direct, indirect, and combined/other methods. Direct bypass includes superficial temporal artery-MCA bypass or use of other graft types. Indirect procedures bring in circulation to the intracranial regions by introducing newly developed vasculature from newly approximated tissues. These procedures may not be enough to prevent further ischemia; therefore, a combination of direct and indirect procedures is more suitable. This article will give a review of the epidemiology, natural history, pathology, pathophysiology, and diagnostic criteria, including imaging, and briefly describe the surgical treatment of MMD.

Quantitative Cerebrovascular Reserve Measured by Acetazolamide-Challenged Dynamic CT Perfusion in Ischemic Adult Moyamoya Disease: Initial Experience with Angiographic Correlation

CT perfusion is a much more readily accessible imaging method to assess cerebral hemodynamic status than single-photon emission CT. We prospectively assessed quantitative cerebrovascular reserve by using acetazolamide (ACZ)-challenged CT perfusion for evaluating hemodynamic impairment in ischemic adult Moyamoya disease and compared it with angiographic findings. Sixteen adult patients with ischemic Moyamoya disease and 12 age-matched normal control subjects underwent both ACZ-challenged CT perfusion and digital subtraction angiography. Normalized baseline hemodynamic parameters and their percent changes (PCs) were calculated in 56 hemispheres. We classified the degrees of distal carotid artery stenosis according to modified Suzuki stage and determined the presence of basal Moyamoya vessels (BMVs). The values of normalized parameters and their PCs were compared with angiographic findings. Normalized baseline mean transit time (MTT) and PC of normalized cerebral blood flow (CBF) were significantly correlated with angiographic stages in all of the vascular territories; however, the correlation coefficient of the normalized baseline MTT was lower than that of the PC of CBF. In the external borderzone and the middle cerebral arterial territory, the hemispheres with extensive BMVs exhibited significantly lower PC values of CBF and significantly higher normalized baseline MTT values than those in hemispheres with diminished BMVs and in normal control subjects. Among the hemodynamic parameters measured by ACZ-challenged CT perfusion, the PC of CBF correlated highly significantly with angiographic stage; however, the normalized baseline CT perfusion parameters showed weak or no significant correlation.

Intracranial Hemodynamic Changes During Adult Moyamoya Disease Progression

Background and purposeThis study evaluated the changes in blood flow velocity in the anterior and posterior intracranial circulations according to the progression of moyamoya disease in adult patients.MethodsWe evaluated Suzuki's angiographic stage and mean blood flow velocity (MBFV) changes in intracranial vessels from both sides in 19 adult moyamoya patients. We then analyzed the linearity of MBFV changes from early to late moyamoya stages in each intracranial vessel using piecewise linear regression models.ResultsThe MBFV in the middle cerebral artery, terminal internal carotid artery, and anterior cerebral artery increased non linearly until stage III, and then decreased progressively up to stage VI. The ophthalmic artery also showed nonlinear velocity changes, with an increase in MBFV up to stage IV, followed by a decrease in MBFV up to stage VI. The MBFV of the basilar artery increased linearly from a normal velocity at an early moyamoya stage to a stenotic velocity at a late stage. There was no statistically significant regression model for the relationship between the MBFV in the posterior cerebral artery and moyamoya stage.ConclusionsThe nonlinear and/or linear MBFV changes associated with variable intracranial vessels might be useful in initial and follow-up evaluations of different stages of moyamoya disease.

Novel Magnetic Resonance Angiography Stage Grading for Moyamoya Disease

Background: Magnetic resonance angiography (MRA) has been acknowledged as a noninvasive diagnostic modality for moyamoya disease. However, in terms of staging of moyamoya disease, conventional angiography is still the gold standard. Therefore, the purpose of this study was to establish MRA grades for moyamoya disease as an alternative to conventional angiography. Methods: Twenty-two patients (44 sides) with moyamoya disease diagnosed by conventional angiography were evaluated by MRA during the past 5 years. MRA scores were assigned based on the severity of occlusive changes of the internal carotid artery, the horizontal portion of the middle cerebral artery, the anterior and the posterior cerebral arteries and the signals of the distal branches of these arteries. Total points ranged from 0 (normal) to 10 (most severe). Results: MRA scores (0–10) were significantly consistent with the conventional angiographic staging. Four grades based on this novel MRA scores correlated well with Suzuki’s stages, with high sensitivity and specificity. Conclusions: These novel MRA grades can be a reliable alternative to conventional staging. By employing these novel MRA grades, the use of conventional angiography can be avoided for the purpose of evaluation of the stages of moyamoya disease.

Prevalence of stenoocclusive lesions in the renal and abdominal arteries in moyamoya disease.

The extracranial involvement of moyamoya disease has been reported in several studies. The main purpose of this study was to determine the prevalence of stenoocclusive lesions in the renal and major abdominal arteries in moyamoya disease. Abdominal angiography was performed in 73 patients with idiopathic moyamoya disease. The findings of abdominal angiography were retrospectively reviewed for the presence and appearance of stenosis in the renal and other major abdominal arteries. Four (5%) of 73 patients presented with unilateral renal artery stenosis. Three patients had moderate stenosis, and one patient had mild stenosis. In the three patients with moderate stenosis, the renal artery stenosis was located in the proximal region of the main branch. Two patients (3%) with moderate stenosis of the unilateral renal artery had renovascular hypertension. No statistically significant differences were observed in age, sex, and the cerebral angiographic stage between patients with and without renal artery stenosis. No stenosis was found in the abdominal aorta or celiac, superior mesenteric, common hepatic, splenic, and proximal common iliac arteries. No occlusions were found in any abdominal arteries. The prevalence of renal artery stenosis in patients with moyamoya disease was 5% (4/73). Involvement of the proximal region of the renal artery was dominant. No stenosis was found in other abdominal arteries.

Evaluation of Cerebral Hemodynamics with Perfusion MRI in Childhood Moyamoya Disease

The purpose of our study was to evaluate the role of perfusion MRI and to compare the findings with those of conventional imaging in childhood moyamoya disease (MMD). Perfusion MRI was performed preoperatively on 13 cases of childhood MMD. Based on the perfusion MRI findings, patients were classified into four groups: those with normal regional cerebral blood volume (rCBV) and time to peak (TTP) (group 1, n = 2); those with normal rCBV and delayed TTP (group 2, n = 1); those with increased rCBV and delayed TTP (group 3, n = 5), and those with decreased rCBV and delayed TTP (group 4, n = 5). Lesion volume as determined using the rCBV map was compared with that on MRI and single photon emission computerized tomography (SPECT). The characteristics of groups 1, 2 and 3 were a high frequency of transient ischemic attacks, normal finding on MRI, early angiographic stages, decreased reserve on SPECT and favorable operative outcome. In group 3, angiography revealed abundant collateral channels. In group 4, all cases had infarction on MRI and abnormal perfusion on SPECT. Angiographic stages tended to have progressed, and operative outcome was less favorable. Perfusion MRI documented hemodynamic asymmetries in the five cases with normal MRI. Perfusion MRI is suggested to have a sensitivity intermediate between rest and acetazolamide SPECTs. We conclude that perfusion MRI may be a valuable tool for characterizing and monitoring ischemia in MMD. Perfusion MRI provides additional functional information not available from conventional MRI and has a potential role comparable to SPECT in the evaluation of MMD.

Elevation of nitric oxide metabolites in the cerebrospinal fluid of patients with moyamoya disease.

To investigate whether nitric oxide (NO) contributes to formation of abnormal collateral circulation in patients with moyamoya disease. Cerebrospinal fluid (CSF) samples were obtained from the subarachnoid space of the Sylvian fissure during combined bypass surgery for moyamoya disease and kept frozen until NO metabolites, nitrate and nitrite, were measured using a Griess method. Compared with control CSF obtained from 18 patients with hemifacial spasm, unruptured aneurysm, etc., concentrations of NO metabolites in 26 CSF samples of 18 patients with moyamoya disease were significantly higher (mean +/- SE; 17.6 +/- 1.2 vs. 10.5 +/- 1.0 microM, p < 0.01). In eight patients, the CSF samples from both the first and second operation could be obtained. NO metabolite concentrations (20.5 +/- 2.3 microM) in CSF obtained from the first surgery decreased to 15.7 +/- 1.8 microM (p < 0.01) in CSF obtained from the second, contralateral procedure. The cases of moyamoya disease with greater development of moyamoya vessels at angiographic stage 3 and 4 tended to show higher concentrations of NO metabolites than cases at earlier or later stages with a few moyamoya vessels. Nitric oxide concentrations in CSF are chronically elevated in moyamoya disease, probably reflecting development of abnormal collateral circulation. i.e. moyamoya vessels. Vascular bypass surgery can reduce abnormal collateral circulation with reduced production of nitric oxide.

Moyamoya disease in adults: characteristics of clinical presentation and outcome after encephalo-duro-arterio-synangiosis

To determine the clinical characteristics and the effectiveness of encephalo-duro-arterio-synangiosis (EDAS) in adulthood-onset Moyamoya disease (MMD), the authors retrospectively reviewed 26 patients suffering from MMD who were admitted to Seoul National University Hospital between 1987 and 1995. When they showed major symptoms, all were more than 16 years-old. The most common presenting symptom was intracranial hemorrhage (ICrH), found in 12 patients or 46% of the total; the second was infarction and transient ischemic attack, each found in seven or 27% of them. Only one patient was found to have seizures, which were associated with a cerebral infarction. The Suzuki angiographic stage 3 and less than stage 3 accounted for 73% of all 52 hemispheres. A total of 15 patients underwent single photon emission computed tomography (SPECT) preoperatively. When the derangement of cerebral perfusion was estimated with four SPECT grades (SG), 70% of their hemispheres revealed normal (SG1) or localized decreased-perfusion (SG2). The other 30% had extensive decreased-perfusion or localized perfusion defects (SG3). There was no case who had extensive perfusion defects (SG4). A total of 17 patients underwent EDAS operations (EDAS group) and nine did not undergo any operation (no-op group). The EDAS group had significantly better clinical outcomes than the no-op group after a 12-month median follow-up period (P<0.05). The angiographic and SPECT follow-up studies comprised six and seven cases, respectively. There was also satisfactory angiographic revascularization in all follow-up cases and improvement in cerebral perfusion at SPECT follow-up in six of seven cases. It is concluded that the involvement of posterior circulation of MMD is not frequent and cerebral perfusion is preserved in adulthood-onset MMD patients. These findings may explain the reason why hemorrhages are frequent and the late onset of symptoms in adulthood-onset MMD. Surgical treatment with EDAS seems to be effective in adulthood-onset MMD in terms of clinical improvement.