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Background and Purpose: Collateral vessels in Moyamoya disease represent potential sources of bleeding. To test whether these cortical distributions vary among subtypes, we investigated cortical terminations using both standardized MR imaging and MRA., Materials and Methods: Patients with Moyamoya disease who underwent MR imaging with MRA in our institution were enrolled in this study. MRA was spatially normalized to the Montreal Neurological Institute space; then, collateral vessels were measured on MRA and classified into 3 types of anastomosis according to the parent artery: lenticulostriate, thalamic, and choroidal. We also obtained the coordinates of collateral vessel outflow to the cortex. Differences in cortical terminations were compared among the 3 types of anastomosis., Results: We investigated 219 patients with Moyamoya disease, and a total of 190 collateral vessels (lenticulostriate anastomosis, n  = 72; thalamic anastomosis, n  = 21; choroidal anastomosis, n  = 97) in 46 patients met the inclusion criteria. We classified the distribution patterns of collateral anastomosis as follows: lenticulostriate collaterals outflowing anteriorly ( P  < .001; 95% CI, 67.0-87.0) and medially ( P  < .001; 95% CI, 11.0-24.0) more frequently than choroidal collaterals; lenticulostriate collaterals outflowing anteriorly more frequently than thalamic collaterals ( P  < .001; 95% CI, 34.0-68.0); and choroidal collaterals outflowing posteriorly more frequently than thalamic collaterals ( P  < .001; 95% CI, 14.0-34.0). Lenticulostriate anastomoses outflowed to the superior or inferior frontal sulcus and interhemispheric fissure. Thalamic anastomoses outflowed to the insular cortex and cortex around the central sulcus. Choroidal anastomoses outflowed to the cortex posterior to the central sulcus and the insular cortex., Conclusions: Cortical distribution patterns appear to differ markedly among the 3 types of collaterals., (© 2020 by American Journal of Neuroradiology.)

Background and Purpose: Although chronic ischemia is known to induce myelin and axonal damage in animal models, knowledge regarding patients with Moyamoya disease is limited. We aimed to investigate the presence of myelin and axonal damage in Moyamoya disease and their relationship with cognitive performance., Materials and Methods: Eighteen patients with Moyamoya disease (16-55 years of age) and 18 age- and sex-matched healthy controls were evaluated with myelin-sensitive MR imaging based on magnetization transfer saturation imaging and 2-shell diffusion MR imaging. The myelin volume fraction, which reflects the amount of myelin sheath; the g-ratio, which represents the ratio of the inner (axon) to the outer (axon plus myelin) diameter of the fiber; and the axon volume fraction, which reflects axonal components, were calculated and compared between the patients and controls. In the patients with Moyamoya disease, the relationship between these parameters and cognitive task-measuring performance speed was also evaluated., Results: Compared with the healthy controls, the patients with Moyamoya disease showed a significant decrease in the myelin and axon volume fractions ( P < .05) in many WM regions, while the increases in the g-ratio values were not statistically significant. Correlations with cognitive performance were most frequently observed with the axon volume fraction ( r = 0.52-0.54; P < .03 in the right middle and posterior cerebral artery areas) and were the strongest with the g-ratio values in the right posterior cerebral artery region ( r = 0.64; P = .004)., Conclusions: Myelin-sensitive MR imaging and diffusion MR imaging revealed that myelin and axonal damage exist in patients with Moyamoya disease. The relationship with cognitive performance might be stronger with axonal damage than with myelin damage., (© 2020 by American Journal of Neuroradiology.)

Background and Purpose: Very few data are available with regard to high-resolution intracranial vessel wall imaging characteristics of Moyamoya disease and their relation to ischemic stroke risk. We investigated the high resolution imaging characteristics of MMD and its correlation with recent ischemic events., Materials and Methods: Patients with Moyamoya disease confirmed by DSA, including patients after revascularization, were enrolled. All the patients underwent high-resolution intracranial vessel wall imaging. Vessel wall thickening, enhancement, and the remodeling index of the bilateral distal ICA and proximal MCA were noted. The patients were followed up at 3 months and 6 months after high-resolution intracranial vessel wall imaging and the association of ischemic events with imaging characteristics was assessed., Results: Twenty-nine patients with Moyamoya disease were enrolled. The median age at symptom onset was 12 years (range, 1-51 years). A total of 166 steno-occlusive lesions were detected by high-resolution intracranial vessel wall imaging. Eleven lesions with concentric wall thickening (6.6%) were noted in 9 patients. Ten concentric contrast-enhancing lesions were observed in 8 patients, of which 3 patients (4 lesions) showed grade II enhancement. The presence of contrast enhancement ( P  = .01) and wall thickening ( P ≤ .001) showed a statistically significant association with ischemic events within 3 months before and after the vessel wall imaging. Grade II enhancement showed a statistically significant ( P  = .02) association with ischemic events within 4 weeks of high-resolution intracranial vessel wall imaging. The mean ± standard deviation outer diameter of the distal ICA (right, -3.3 ± 0.68 mm; left, 3.4 ± 0.60 mm) and the remodeling index (right, 0.71 ± 0.13; left, 0.69 ± 0.13) were lower in Moyamoya disease., Conclusions: High-resolution intracranial vessel wall imaging characteristics of concentric wall thickening and enhancement are relatively rare in our cohort of patients with Moyamoya disease. The presence of wall thickening and enhancement may predict future ischemic events in patients with Moyamoya disease., (© 2020 by American Journal of Neuroradiology.)

Background and Purpose: Moyamoya disease is a chronic neurovascular steno-occlusive disease of the internal carotid artery and its main branches, associated with the development of compensatory vascular collaterals. Literature is lacking about the precise description of these compensatory vascular systems. Usually, the posterior circulation is less affected, and its vascular flow could compensate the hypoperfusion of the ICA territories. The aim of this study was to describe these natural connections between the posterior cerebral artery and the anterior cerebral artery necessary to compensate the lack of perfusion of the anterior cerebral artery territories in the Moyamoya population., Materials and Methods: All patients treated for Moyamoya disease from 2004 to 2018 in 4 neurosurgical centers with available cerebral digital subtraction angiography were included. Forty patients (80 hemispheres) with the diagnosis of Moyamoya disease were evaluated. The presence of anastomoses between the posterior cerebral artery and the anterior cerebral artery was found in 31 hemispheres (38.7%)., Results: Among these 31 hemispheres presenting with posterior cerebral artery-anterior cerebral artery anastomoses, the most frequently encountered collaterals were branches from the posterior callosal artery (20%) and the posterior choroidal arteries (20%). Another possible connection found was pio-pial anastomosis between cortical branches of the posterior cerebral artery and the anterior cerebral artery (15%). We also proposed a 4-grade classification based on the competence of these anastomoses to supply retrogradely the territories of the anterior cerebral artery., Conclusions: We found 3 different types of anastomoses between the anterior and posterior circulations, with different abilities to compensate the anterior circulation. Their development depends on the perfusion needs of the territories of the anterior cerebral artery and can provide the retrograde refilling of the anterior cerebral artery branches., (© 2019 by American Journal of Neuroradiology.)

Background and Purpose: Simple-but-precise evaluation of cerebral perfusion is crucial for the treatment of Moyamoya disease. We aimed to develop a standardized scoring system for MR perfusion suitable for Moyamoya disease evaluation and investigate the postoperative serial changes and outcome predictors., Materials and Methods: From January 2013 to December 2016, patients diagnosed with Moyamoya disease and receiving indirect revascularization were recruited prospectively. Clinical data and serial imaging studies were analyzed. The TTP maps were standardized using cerebellar reference values. We developed a scoring system of standardized TTP maps: 14 points for each hemisphere with higher points indicating better perfusion., Results: In total, 24 children (4-17 years of age, 41 hemispheres) and 20 adults (18-51 years of age, 34 hemispheres) were included. The mean preoperative TTP scores were higher in children (7.34 ± 3.90) than in adults (4.88 ± 3.24). The standardized TTP maps revealed dynamic improvement with an increase in the corresponding scores at the 1-, 3-, and 6-month postoperative follow-ups; the scores stabilized after 6 months. The mean improvement in the 6-month scores of the pediatric and adult groups was 4.15 ± 3.55 and 6.03 ± 3.04, respectively. The 6-month TTP score improvements were associated with Matsushima grades. If we took score improvement as the outcome, the preoperative TTP score was the only significant predictor in multivariable analysis., Conclusions: The standardized TTP maps and scoring system facilitated the quantification of the sequential perfusion changes during Moyamoya disease treatment. The preoperative perfusion status was the only predictor of indirect revascularization outcome., (© 2019 by American Journal of Neuroradiology.)

Background and Purpose: Impaired cerebrovascular reactivity has been associated with decreased cortical thickness in patients with arterial occlusive diseases. This study tests the hypothesis that severe hemodynamic impairment, indicated by increased oxygen extraction fraction ratios on positron-emission tomography with 15 O tracers, is associated with decreased cortical thickness in patients with Moyamoya phenomenon., Materials and Methods: Patients with unilateral or bilateral idiopathic Moyamoya phenomenon were recruited. Oxygen extraction fraction ratio maps were generated from cerebral images of O[ 15 O] counts divided by H 2 [ 15 O] counts with normalization by corresponding cerebellar counts. The normal range of the oxygen extraction fraction ratio was estimated from historically available healthy control subjects. Cortical thickness was estimated from T1-weighted MR imaging and FreeSurfer. Regional samples of oxygen extraction fraction ratios and cortical thicknesses were drawn using FreeSurfer parcellations, retaining only parcellations from the vascular territory of the middle cerebral artery., Results: Complete MR imaging and PET datasets were available in 35 subjects, including 23 women; the mean age at scanning was 44 years. Patients with Moyamoya phenomenon had a significantly increased regional oxygen extraction fraction ratio compared with 15 healthy control subjects ( P < .001). Regional oxygen extraction fraction ratio and age were significant predictors of cortical thickness ( P < .001 for each) in a generalized linear mixed-effects model. Using hemisphere averages and patient averages, we found that only age was a significant predictor of cortical thickness ( P < .001)., Conclusions: Chronic hemodynamic impairment, as indicated by a higher regional oxygen extraction fraction ratio, was significantly predictive of reduced cortical thickness in mixed-effects analysis of FreeSurfer regions. This phenomenon may be related to reversible metabolic down-regulation., (© 2018 by American Journal of Neuroradiology.)

Background and Purpose: Moyamoya disease is a progressive neurovascular pathology defined by steno-occlusive disease of the distal internal carotid artery and associated with the development of compensatory vascular collaterals. The etiology and exact anatomy of vascular collaterals have not been extensively studied. The aim of this study was to describe the anatomy of collaterals developed between the ophthalmic artery and the anterior cerebral artery in a Moyamoya population., Materials and Methods: All patients treated for Moyamoya disease from 2004 to 2016 in 4 neurosurgical centers with available cerebral digital subtraction angiography were included. Sixty-three cases were evaluated, and only 38 met the inclusion criteria. Two patients had a unilateral cervical internal carotid occlusion that limited analysis of ophthalmic artery collaterals to one hemisphere. This study is consequently based on the analysis of 74 cerebral hemispheres., Results: Thirty-eight patients fulfilled the inclusion criteria. The most frequently encountered anastomosis between the ophthalmic artery and cerebral artery was a branch of the anterior ethmoidal artery (31.1%, 23 hemispheres). In case of proximal stenosis of the anterior cerebral artery, a collateral from the posterior ethmoidal artery could be visualized (16 hemispheres, 21.6%). One case (1.4%) of anastomosis between the lacrimal artery and the middle meningeal artery that permitted the vascularization of a middle cerebral artery territory was also noted., Conclusions: Collaterals from the ophthalmic artery are frequent in Moyamoya disease. Their development depends on the perfusion needs of the anterior cerebral artery territories. Three other systems of compensation could be present (callosal circle, leptomeningeal anastomosis, and duro-pial anastomoses)., (© 2018 by American Journal of Neuroradiology.)

The pathophysiologic role of hemodynamic alteration to peripheral vessels in Moyamoya angiopathy and the formation of microaneurysms remains unclear. The purpose of this study was to investigate microaneurysms in collateral Moyamoya vessels by using 7T ultra-high-field MR imaging. Ten patients with Moyamoya disease were evaluated with TOF-MRA at 7T acquired with 0.22 × 0.22 × 0.41 mm(3) resolution. In 10 patients, 4 microaneuryms located in the ventricles were delineated. The mean diameters of collateral vessels and microaneurysms arising from those vessels were 0.87 mm (range, 0.79-1.07 mm) and 0.80 mm (range, 0.56-0.96 mm), respectively. In 1 case with follow-up scans 6 months after a direct extracranial-intracranial bypass operation, the microaneurysm disappeared. Ventricular microaneurysms in Moyamoya angiopathy collateral vessels, inaccessible by conventional imaging techniques, can be detected by 7T TOF-MRA., (© 2016 by American Journal of Neuroradiology.)

Background and Purpose: Encephaloduroarteriosynangiosis has been shown to generate collateral vessels from the extracranial-to-intracranial circulation in patients with Moyamoya disease and intracranial arterial steno-occlusive disease. The mechanisms involved are not well-understood. We hypothesized that angiogenesis is the leading mechanism forming collaterals after encephaloduroarteriosynangiosis because there are no pre-existing connections. Angiogenesis-generated collaterals should exhibit higher architectural complexity compared with innate collaterals., Materials and Methods: Pre- and postoperative digital subtraction angiograms were analyzed in patients enrolled in a prospective trial of encephaloduroarteriosynangiosis surgery. Branching angioscore, tortuosity index, and local connected fractal dimension were compared between innate and postoperative collaterals., Results: One hundred one angiograms (50 preoperative, 51 postoperative) were analyzed from 44 patients (22 with intracranial atherosclerosis and 22 with Moyamoya disease). There was a significantly higher median branching angioscore (13 versus 4, P < .001) and a lower median tortuosity index (1.08 versus 1.76, P < .001) in the encephaloduroarteriosynangiosis collaterals compared with innate collaterals. Higher mean local fractal dimension peaks (1.28 ± 0.1 versus 1.16 ± 0.11, P < .001) were observed in the encephaloduroarteriosynangiosis collaterals compared with innate collaterals for both intracranial atherosclerosis (P < .001) and Moyamoya disease (P < .001) groups. The observed increase in high connectivity was greater in the intracranial atherosclerosis group compared with patients with Moyamoya disease (P = .01)., Conclusions: The higher median branching angioscore and local connected fractal dimension, along with the lower median tortuosity index of encephaloduroarteriosynangiosis collaterals, are consistent with the greater complexity observed in the process of sprouting and splitting associated with angiogenesis., (© 2016 by American Journal of Neuroradiology.)

Background and Purpose: DTI is widely used for the evaluation of white matter integrity in various neurologic diseases. The purpose of this study was to investigate changes in white matter integrity by using DTI in NAWM of patients with MMD and to evaluate the correlation between diffusion and perfusion characteristics through an interhemispheric comparison., Materials and Methods: We retrospectively reviewed 20 primary MMD patients with asymmetric disease stage and 20 age-matched healthy controls. FA(CS) and ADC(CS) values of bilateral centrum semiovale were measured by using region of interest analysis. Mean FA(CS) and ADC(CS) were compared between patient and control groups by unpaired t test. Interhemispheric differences in FA(CS) and ADC(CS) were assessed and compared between the H-TTP(delayed) and the H-TTP(shorter) by using paired t test. AIs also were assessed to verify interhemispheric differences., Results: The patient group showed a significantly lower mean FA(CS) and a higher mean ADC(CS) value than the control group. In the patient group, the H-TTP(delayed) had a significantly lower FA(CS) and higher ADC(CS) value than the H-TTP(shorter). Both AI(FA) and AI(ADC) were significantly higher in the patient compared with the control group., Conclusions: DTI can describe subtle changes in white matter integrity in NAWM of patients with primary MMD that are not detected by conventional MR imaging. In addition, diffusion characteristics are well correlated with perfusion characteristics. We believe that DTI is a useful ancillary tool to evaluate patients with MMD.

Background and Purpose: SWI is a high spatial resolution MR imaging technique showing magnetic inhomogeneity that could demonstrate increased oxygen extraction in focal cerebral ischemia. The aim of this study was to investigate the characteristics in the signal intensity of DMVs by using SWI and to determine whether this method could indicate the severity of the hemodynamics in MMD by evaluating the correlation between SWI stage and hemodynamics on SPECT., Materials and Methods: Consecutive MMD patients were prospectively analyzed before treatment. Routine MR imaging including SWI was performed, and the number of the conspicuous DMVs draining into the subependymal veins was classified: stage 1, mild (< 5); stage 2, moderate (5-10); and stage 3, severe (> 10). The SWI stage was evaluated in correlation with clinical presentations, and CBF and CVR were quantified by using a SPECT iodine 123 N-isopropyl-p-iodoamphetamine split-dose method., Results: Patients were 12 males and 21 females (range, 8-66 years), consisting of 4 asymptomatic patients, 13 patients with TIA, 9 patients with infarct, and 7 patients with hemorrhage. There was a significant difference in CVR among clinical presentations, though there was no difference in age, Suzuki stage, or CBF. Conversely, SWI stage was significantly higher in patients with TIA and infarct than asymptomatic patients (P < .01). Higher SWI stage significantly had lower CBF and CVR in the middle cerebral artery area (P < .05)., Conclusions: SWI stage strongly correlates with ischemic presentations in MMD and also correlates with hemodynamics on SPECT, especially CVR. Increased conspicuity of DMVs, known as "brush sign", could predict the severity of MMD.

Background and Purpose: The "ivy" sign that is identified on FLAIR images in patients with Moyamoya disease is considered to be leptomeningeal collaterals. The aim of our study was to evaluate the correlation between postoperative decrease in ivy sign and cerebral hemodynamic status in the bypass-established hemisphere., Materials and Methods: Twenty-two patients with Moyamoya disease were enrolled. Postoperative changes in the ivy sign on FLAIR images were examined in each patient after bypass surgery. The correlation between postoperative changes in the ivy sign and hemodynamic status was examined in 10 patients by using SPECT., Results: Of the 22 preoperative ivy-positive patients, 21 showed decreased ivy signs on the operative side. Average intervals between the operation day and the date when the decreased or vanished ivy sign was first recognized were 157.6 days in patients who underwent direct bypass and 212.2 days in patients who underwent indirect bypass. A postoperative decrease in ivy signs was found to be significantly correlated with an improved hemodynamic status of the surgically treated hemisphere, resulting in a postoperative increase in regional vascular reserve and a decreased proportion of the misery perfusion area (P < .01)., Conclusions: Postoperative changes in the ivy sign can be used as a marker for identifying improved hemodynamics and also for testing the effectiveness of cerebral revascularization.

Background and Purpose: BOLD MR imaging combined with a technique for precision control of end-tidal pCO(2) was used to produce quantitative maps of CVR in patients with Moyamoya disease. The technique was validated against measures of disease severity by using conventional angiography; it then was used to study the relationship between CVR, vascular steal, and disease severity., Materials and Methods: A retrospective analysis comparing conventional angiography with BOLD MR imaging was performed on 11 patients with Moyamoya disease. Iso-oxic cycling of end-tidal pCO(2) between 2 target values was performed during BOLD MR imaging. CVR was calculated as the BOLD signal difference per Delta pCO(2). CVR was correlated with the presence of Moyamoya or pial collaterals and the degree of Moyamoya disease as graded by using a modified Suzuki score., Results: A good correlation between mean CVR and Suzuki score was found for the MCA and ACA territories (Pearson correlation coefficient, -0.7560 and -0.6140, respectively; P < .0001). A similar correlation was found between mean CVR and the presence of pial and Moyamoya collateral vessels for combined MCA and ACA territories (Pearson correlation coefficient, -0.7466; P < .0001). On a voxel-for-voxel basis, there was a greater extent of steal within vascular territories with increasing disease severity (higher modified Suzuki score). Mean CVR was found to scale nonlinearly with the extent of vascular steal., Conclusions: Quantitative measures of CVR show direct correlation with impaired vascular supply as measured by the modified Suzuki score and enable direct investigation of the physiology of autoregulatory reserve, including steal phenomenon, within a given vascular territory.

Background and Purpose: An ivy sign is considered to represent diffuse leptomeningeal collaterals found on fluid-attenuated inversion recovery (FLAIR) images of patients with Moyamoya disease. We evaluated the correlation between unilateral ivy proliferation in a hemisphere and cerebrovascular hemodynamic status to learn the clinical significance of the ivy sign., Materials and Methods: A total of 35 patients with Moyamoya disease were included. Correlation between ivy dominance on FLAIR images and hemodynamic status with use of iodine 123 N-isopropyl-p-iodoamphetamine ((123)I-IMP) single-photon emission CT (SPECT) was evaluated., Results: Distributional differences of ivy signs between both hemispheres were observed in 22 (64.7%) of 34 patients with a positive ivy sign, all of whom showed decreased vascular reserve/reactivity in the ivy-dominant hemisphere (IDH). The proportion of the stage II (misery perfusion) area to IDH was higher than that in the ivy less-dominant hemisphere (ILDH) in the quantitative analysis. The mean vascular reserve was lower in IDH than ILDH. There were 15 of 22 patients who had bypass surgery on IDH because of transient ischemic attack from ischemia of IDH. Patients with symmetric ivy distributions showed a variety of hemodynamic status. MR angiography (MRA) stage of IDH (2.95 +/- 0.39) was higher compared with ILDH (2.60 +/- 0.50; P < .05). Regional arteriocapillary circulation time ratio in IDH was longer compared with ILDH (P < .05). Ivy proliferation decreased in 10 (55.6%) of 18 patients who underwent bypass surgery during the follow-up period., Conclusions: Unilateral hemispheric ivy proliferation correlated highly with the existence of an ipsilateral decreased vascular reserve associated with the development of leptomeningeal collaterals in patients with Moyamoya disease.

Background and Purpose: Moyamoya disease is an idiopathic occlusive cerebrovascular disorder with abnormal microvascular proliferation. We investigated the clinical utility of leptomeningeal high signal intensity (ivy sign) sometimes seen on fluid-attenuated inversion recovery images in Moyamoya disease., Materials and Methods: We examined the relationship between the degree of the ivy sign and the severity of the ischemic symptoms in 96 hemispheres of 48 patients with Moyamoya disease. We classified each cerebral hemisphere into 4 regions from anterior to posterior. In 192 regions of 24 patients, we examined the relationship between the degree of the ivy sign and findings of single-photon emission CT, including the resting cerebral blood flow (CBF) and cerebral vascular reserve (CVR)., Results: The degree of the ivy sign showed a significant positive relationship with the severity of the ischemic symptoms (P < .001). Of the 4 regions, the ivy sign was most frequently and prominently seen in the anterior part of the middle cerebral artery region. The degree of the ivy sign showed a negative relationship with the resting CBF (P < .0034) and a more prominent negative relationship with the CVR (P < .001)., Conclusions: The leptomeningeal ivy sign indicates decreased CVR in Moyamoya disease.

Background and Purpose: This study examined abnormalities of the recirculation phase of the contrast medium concentration time course curve in patients with moyamoya disease by using the relative recirculation (rR) parameter. Our aims were to increase understanding of the rR parameter and to assess its possible value in the investigation of moyamoya disease., Methods: Six patients with confirmed moyamoya disease and five normal participants were examined by using dynamic T2*-weighted MR perfusion imaging. Parametric maps of relative cerebral blood volume, time to peak (TTP), and rR were calculated. The width of the normal distribution of TTP and the normal upper limit for rR were derived from the normal participants by identification of the 97.5% confidence limits for the distributions. Major vessels were identified by selection of pixels with relative cerebral blood volume >0.5. Areas of abnormally prolonged TTP and of increased rR were then identified in patients, and the relationship between these parameters and major vessels was examined., Results: The combination of cerebral blood volume >50%, elevated TTP, and elevated rR values accurately identified areas of moyamoya vessel formation seen on angiograms. Larger well-developed meningeal and basal collaterals did not show abnormalities of rR. Areas of prolonged TTP were also observed to occur in the brain distal to arterial occlusion in all cases. In three of these, abnormal elevation of rR was observed in the center of regions of prolonged TTP., Conclusion: These findings support those of our previous work, which suggested that rR can act as an indicator of regional microvascular abnormality, such as that seen in areas of angiogenic activity. They also suggest that measurement of rR may provide valuable additional information regarding patients with moyamoya disease.

The authors present an angiographic follow-up of anastomotic surgery (extra- to intracranial) in a 33-year-old woman with moyamoya disease. The bypass was superficial-temporal to middle-cerebral, with placement of muscle tissue over the open craniotomy; the bypass eventually regressed.