Circulation In Moyamoya Disease Research Articles

The effects of anastomoses between anterior and posterior circulation on postoperative prognosis of patients with moyamoya disease.

Moyamoya disease (MMD) is a chronic ischemic cerebrovascular disease. Collateral circulation in MMD has emerged as a research focus. Our aims were to assess the impact of anastomoses between the anterior and posterior circulations on the prognosis of MMD patients. We reviewed the preoperative digital subtraction angiography images of patients with MMD who underwent revascularization surgery at our hospital between March 2014 and May 2020 and divided the patients into two groups: those with anastomoses (PtoA group) and those without anastomoses (non-PtoA group). The differences in follow-up (more than 6months) collateral vessel establishment (Matsushima grade) and the modified Rankin Scale (mRS) were compared between the two groups as well as between the patients with different degrees of anastomoses. The early complications following revascularization were also compared between the two groups. This study included 104 patients with MMD, of which 38 were non-PtoA and 66 were PtoA. There were no significant differences in Matsushima score (P = 0.252) and mRS score (P = 0.066) between the two groups. In addition, Matsushima score (P = 0.243) and mRS score (P = 0.360) did not differ significantly between patients with different degrees of anastomoses. However, the non-PtoA group had a significantly higher rate of cerebral hyperperfusion syndrome (CHS) than the PtoA group (34.2% vs 16.7%, P = 0.041). MMD patients without anastomoses between anterior and posterior circulations preoperatively should be vigilant of the occurrence of CHS in the early stages after revascularization.

Variants of collateral cerebral circulation in moyamoya disease

Moyamoya disease is a chronic progressive cerebrovascular disease with a complex pathophysiology and unique features of neoangiogenesis. These features are still known only to a few specialists, although they determine clinical course and outcomes of disease. To determine the nature and degree of neoangiogenesis in restructuring the natural collateral circulation in patients with moyamoya disease and its effect on cerebral blood flow. The influence of collateral circulation on postoperative results and factors of its effectiveness will be analyzed in the 2nd part of the study. The study included 65 patients with moyamoya disease who underwent preoperative selective direct angiography with separate contrast enhancement of both internal, external and vertebral arteries. We analyzed 130 hemispheres. Suzuki stage of disease, pathways of collateral circulation and their relationship with reduction of cerebral blood flow and clinical manifestations were assessed. Distal vessels of the middle cerebral artery (MCA) were additionally studied. Suzuki stage 3 was the most common (36 hemispheres, 38%). Leptomeningeal collaterals were the most common among intracranial collateral tracts (82 hemispheres, 66.1%). Extra-intracranial transdural collaterals were found in half of the cases (56 hemispheres). We observed certain changes in distal vessels of the MCA (hypoplasia of M3 branches) in 28 (20.9%) hemispheres. Suzuki stage of disease significantly determined degree of cerebral blood flow insufficiency, i.e. more severe perfusion deficit was observed at the later stages of disease. A well-developed system of leptomeningeal collaterals significantly reflected stages of compensation and subcompensation of cerebral blood flow according to perfusion data (χ2=20.394, p<0.001). Neoangiogenesis is a natural compensatory mechanism in moyamoya disease designed to maintain brain perfusion under reduced cerebral blood flow. Predominant intra-intracranial collaterals are associated with ischemic and hemorrhagic events. Timely restructuring on extra-intracranial ways of collateral circulation prevents adverse manifestations of disease. Assessment and understanding of collateral circulation in patients with moyamoya disease create the prerequisites for substantiating the method of surgical treatment.

Endovascular treatment of main trunk aneurysms in the residual anterior circulation in moyamoya disease.

Main trunk aneurysms in the residual anterior circulation in moyamoya disease (MMD) are uncommon, and in such cases, endovascular treatment (EVT) is a good choice. A retrospective study was performed on 35 consecutive patients admitted to our hospital who were diagnosed with MMD and main trunk aneurysms in the residual anterior circulation and were treated with EVT. The 35 patients were aged 38-77years (mean, 56.1 ± 8.8years) and included 17 females (48.6%, 17/35). There were 29 cases (82.9%, 29/35) of hemorrhagic onset. In 35 patients, there were 38 main trunk aneurysms in the residual anterior circulation. Thirty-eight aneurysms underwent coiling; among them, coiling with stent assistance was used in the treatment of 6 (15.8%, 6/38) aneurysms. The immediate modified Raymond-Roy classification (MRRC) was grade I for all aneurysms. Among 35 patients, intraoperative bleeding occurred in 2 (5.7%, 2/35) patients. After EVT, immediate hemiplegia occurred in 4 (11.4%, 4/35) patients, and immediate coma occurred in 1 (2.9%, 1/35) patient. At discharge, in 35 patients, the Glasgow Outcome Scale (GOS) was five in 88.6% of them. Of 35 patients, 68.6% had follow-up data, GOS was five in 87.5% patients, and the MRRC was grade I for all aneurysms in the follow-up angiography. For main trunk aneurysms in the residual anterior circulation in MMD, although EVT was accompanied by potential ischemic and hemorrhagic complications, which should be considered, EVT can still offer an acceptable prognosis in more than 85% of patients.

Distribution of Intracranial Major Artery Stenosis/Occlusion According to RNF213 Polymorphisms.

Intracranial major artery stenosis/occlusion (ICASO) is the major cause of ischemic stroke. Recent studies have suggested that variants of RNF213, a susceptibility gene for moyamoya disease (MMD), are also related to non-MMD ICASO. Regarding the predominant involvement of steno-occlusion on anterior circulation in MMD, we hypothesized that the ICASO distribution pattern (anterior/posterior) in non-MMD may differ according to RNF213 variants. This study analyzed 1024 consecutive Korean subjects without MMD who underwent computed tomography angiography (CTA) or magnetic resonance angiography (MRA). We evaluated four single nucleotide polymorphisms (SNPs) in the exon region of RNF213: 4448G > A (rs148731719), 4810G > A (rs112735431), 4863G > A (rs760732823), and 4950G > A (rs371441113). Associations between RNF213 variants and anterior/posterior ICASO were examined using multivariate logistic regression analysis. Anterior ICASO was present in 23.0% of study subjects, and posterior ICASO was present in 8.2%. The GA genotype of RNF213 4810G > A (adjusted odds ratio (AOR) [95% confidence interval (CI)], 2.39 [1.14–4.87] compared to GG; p = 0.018) and GA genotype of RNF213 4950G > A (AOR [95% CI], 1.71 [1.11–2.63] compared to GG; p = 0.015) were more frequent in subjects with anterior ICASO. The genotype frequency of RNF213 4863G > A differed significantly according to the presence of posterior ICASO. Further investigations of the functional and biological roles of RNF213 will improve our understanding of the pathomechanisms of ICASO and cerebrovascular disease.

Comparative study of 4D CTA and DSA for vascular assessment in moyamoya disease

Purpose: To evaluate the vascular stenosis and collateral circulation in moyamoya disease using 4D CTA.Methods: Two neuroradiologists evaluated 4D CTA and DSA for 101 moyamoya patients. The performance of 4D CTA relative to DSA was determined using consistency checks (kappa values, 95% CI) and correlation analysis.Results: The kappa values were 0.714 (modified Suzuki score), 0.846 (Houkin score), 0.594 (basicranial moyamoya vessels), 0.435 (posterior circulation collaterals) and 0.591 (ECA collaterals). The correlation coefficients were 0.843, 0.872, 0.792, 0.635 and 0.797.Conclusions: 4D CTA showed strong consistency and correlation with DSA in the vascular stenosis score, but was insufficient in collateral circulation evaluation.

The Collateral Circulation in Moyamoya Disease: A Single-Center Experience in 140 Pediatric Patients

BackgroundThe patterns and clinical significance of the presence of collaterals in moyamoya disease has not been elucidated thoroughly. We aimed to summarize the clinical features of collaterals in pediatric moyamoya disease. Basic proceduresWe reviewed consecutive pediatric patients with moyamoya vasculopathy who were admitted to our hospital from 2009 to 2015. Only pediatric moyamoya patients with digital subtraction angiography examinations were included in this study. We classified spontaneous collaterals into two groups by their origins, the internal carotid artery and vertebral artery (ICA-VA)-originated collaterals and the external carotid artery (ECA)-originated collaterals. Main findingsA total of 140 pediatric patients with moyamoya disease (mean age, 10.1 ± 3.7 years) were included in this study. We identified collaterals originated from ICA-VA in 122 (87.1%) pediatric patients (222 hemispheres). Patients in the ICA-VA collaterals group had similar Suzuki stages with patients without collaterals originated from ICA-VA (mean, 3.86 vs 3.50; P = 0.157). We identified collaterals originated from ECAs in 70 (50.0%) pediatric patients (106 hemispheres) with moyamoya disease. The infarctions were more common in patients with ECA-originated collaterals than in patients without ECA-originated collaterals (25 versus 12; P = 0.021). Principal conclusionsOur results demonstrate that collaterals originating from ECAs are associated with advanced Suzuki stages and infarction presentations in children with moyamoya disease.

Pathophysiological consideration of medullary streaks on FLAIR imaging in pediatric moyamoya disease.

OBJECTIVE Medullary streaks detected on fluid-attenuated inversion recovery (FLAIR) imaging have been considered to be reflected ischemic regions in pediatric moyamoya disease. The purpose of this study was to evaluate these medullary streaks both clinically and radiologically and to discuss associated pathophysiological concerns. METHODS The authors retrospectively reviewed data from 14 consecutive pediatric patients with moyamoya disease treated between April 2009 and June 2016. Clinical and radiological features and postoperative imaging changes were analyzed. In 4 patients, hyperintense medullary streaks on FLAIR imaging (HMSF) at the level of the centrum semiovale were detected. RESULTS The HMSF were coincident with hyperintense medullary streaks on a T2-weighted image, though they were not completely coincident with the vasculature on either a T2*-weighted image or contrast-enhanced CT. Analysis revealed significantly higher values in terms of MR angiography scores, number of flow voids of the basal ganglia, and the presence of the medullary artery in the group with HMSF than in those without. In contrast, the presence of white matter damage was significantly less frequent in the HMSF group. All HMSF disappeared after surgery, and the mean apparent diffusion coefficient at the same level was significantly reduced postoperatively. CONCLUSIONS Although HMSF should be associated with collateral circulation in moyamoya disease, other factors may be involved, including stagnated cerebrospinal fluid or vasogenic edema that is relevant to the impaired state of the white matter. Findings in this study provide insight into the pathophysiological basis of the perivascular space in moyamoya disease.

Reversible Changes of Posterior Cerebral Artery after Angioplasty for Moyamoya Disease: Report of a Case

Background: The changes of posterior cerebral arteries (PCAs) in Moyamoya disease (MMD) are often involved in the clinical setting. However, the changes of PCAs after recovering the hemodynamics of anterior circulation in MMD are not reported. Case Description: A 14-year-old patient was diagnosed as MMD with symptomatic stenosis in the right middle cerebral artery (MCA), asymptomatic stenosis in the left terminal internal carotid artery, and moyamoya-like vessels, stenotic lesion and an aneurysm were found in the right PCA, who was treated with balloon angioplasty in the right MCA. One month later, the patient suffered from transient ischemic attack in the right. DSA showed deteriorated severe stenosis in the left terminal portion of ICA and the proximal segment of MCA. The patient was performed angioplasty in the left ICA and MCA again. The follow-up angiography did not show any evidence of restenosis at the previous sites of stenosis after 18 months. Interestingly, the aneurysm and collateral vessels were disappeared as well as the stenotic vessel in the right PCA was recovered completely. Conclusion: Our findings indicated that the pathologic changes of PCA are reversible after recovering the hemodynamic of the anterior circulation in MMD. It is important to understand the pathophysiological changes of posterior circulation in MMD.

Posterior Cerebral Artery Insufficiency in Pediatric Moyamoya Disease.

The majority of clinical studies on moyamoya disease (MMD) have focused on anterior circulation. The disease involvement of posterior circulation in MMD, mainly in the posterior cerebral artery (PCA), has been mentioned since the early 1980s, and it has been repeatedly emphasized as one of the most important factors related to poor prognosis in MMD. However, its clinical features and outcome have only been elucidated during the last few years. In this review, the angiographic definition of PCA stenosis is summarized. The clinical features are elucidated as being either early-onset or delayed-onset, according to the time of PCA stenosis diagnosis in reference to the anterior circulation revascularization surgeries. The surgical strategy and hypothesis on the mechanism of PCA stenosis is also briefly mentioned. It appears that some MMD patients may show PCA stenosis during the early or late course of the disease and that the presenting symptoms may vary. Because the hemodynamic compromise caused by PCA stenosis may respond well to surgical treatment, clinicians should be aware of the condition, especially during follow-up of MMD patients.

Posterior cerebral artery involvement in moyamoya disease: initial infarction and angle between PCA and basilar artery

Moyamoya disease (MMD) is a chronic cerebrovascular occlusive disease, and progressive involvement of the posterior cerebral artery (PCA) has been reported. However, majority of MMD articles are presenting classic anterior circulation related issues. This study investigates the preoperative factors related to the long-term outcome of posterior circulation in MMD. Retrospective review of 88 MMD patients (166 PCAs in either hemisphere) without symptomatic disease involvement of PCA at initial diagnosis was done. Data at initial diagnosis regarding age, presence of infarction, status of the PCA, type of posterior communicating artery, and the angle between PCA and basilar artery were reviewed. Progressive stenosis of PCA was evaluated by symptom or radiological imaging during follow up. During an average follow up of 8.3 years, 29 out of 166 (18 %) evaluated PCAs showed progressive disease involvement. The average time of progression from the initial operation was 4.9 years, with the latest onset at 10.8 years. The patients who showed progressive stenosis of the PCA tended to be younger, present with infarction, have smaller angle between PCA and basilar artery, and have asymptomatic stenosis of the PCA at initial presentation. However, multivariate analysis confirmed only the presence of initial infarction and a smaller angle between PCA and basilar artery to be significantly associated with progressive stenosis of PCA. Involvement of PCA in MMD may occur in a delayed fashion, years after the completion of revascularization of anterior circulation. Persistent long-term follow-up regarding the posterior circulation is recommended.

Effect of inhalational anesthesia on cerebral circulation in Moyamoya disease.

To clarify the effects of inhalational anesthesia on cerebral circulation in patients with Moyamoya disease, the authors measured regional cortical blood flow (CoBF), jugular bulb oxygen saturation (SjO2), and frontal regional oxygen saturation (rSO2) by near infra-red spectroscopy under total intravenous and inhalational anesthesia in 13 patients undergoing revascularization procedures. Cortical blood flow decreased in some regions under inhaled anesthesia in all cases, and the mean value decreased significantly (p<0.01). Patients' SjO2 levels rose during inhalational anesthesia in 10 of 11 cases (p<0.01). Frontal rSO2 declined in 9 of 11 cases. Regional CoBF levels may be decreased by inhaled anesthesia in patients with Moyamoya disease, and such anesthesia may provoke intracerebral steal. Total intravenous anesthesia, however, lacked these effects.

Effect of inhalational anesthesia on cerebral circulation in Moyamoya Disease

Effect of inhalational anesthesia on cerebral circulation in Moyamoya Disease

Evaluation of Surgically Formed Collateral Circulation in Moyamoya Disease with 3D-CT Angiography: Comparison with MR Angiography and X-Ray Angiography

Three patients with moyamoya disease who had undergone bypass surgery at which bilateral encephaloduro-arterio-synangiosis (EDAS) anastomoses were created were studied with three-dimensional spiral CT angiography (3D-CTA). In one patient, magnetic resonance angiography (MRA) clearly visualized the bilateral EDAS, and 3D-CTA also visualized these anastomoses in detail with extreme clarity. In the other two patients, MRA did not clearly demonstrate the right EDAS anastomosis, but 3D-CTA visualized both side surgical collaterals clearly. External carotid angiography confirmed these findings. 3D-CTA might have great value in the evaluation of surgical bypass patency and, in following the disease progression.

Posterior circulation in moyamoya disease: angiographic study.

To clarify the angiographic findings of the posterior circulation in patients with moyamoya disease. Seventy-six patients with idiopathic moyamoya disease were studied with conventional angiography. The angiographic findings were reviewed for steno-occlusive lesions, collateral vessels, and aneurysms and compared with the finding of parenchymal lesions on computed tomographic and magnetic resonance images. Of 152 posterior cerebral arteries (PCAs), 66 (43%) had a stenotic or occluded lesion. The frequency of PCA lesions statistically significantly increased with the extent of the internal carotid artery (ICA) bifurcation steno-occlusive lesion. As the severity of ICA stenosis increased, basal cerebral moyamoya vessels and transdural collateral vessels similarly increased in number, but leptomeningeal collateral vessels decreased owing to the progressive development of more PCA lesions. Cerebral infarctions, ventricular dilatation, and cerebral atrophy were found to increase in frequency in patients with steno-occlusive PCA lesions. Steno-occlusive lesions of the PCA increase in frequency proportionally with severity of ICA bifurcation steno-occlusive lesions, so that cerebral infarctions increase in frequency with the extent of the PCA lesions.

Cerebral circulation in moyamoya disease: A clinical study using transcranial doppler sonography

Transcranial Doppler sonography was performed on eight patients diagnosed as Moyamoya disease. Angiographically, the patients-four adults (mean age 42) and four children (mean age 7.7)-underwent a complete six- or five-vessel angiographic study. The results showed the following: (1) Despite the presence of stenosis, all middle cerebral arteries showed very low-flow velocity compared to their ipsilateral distal internal carotid arteries. In adult cases, the difference was very significant ( p < 0.02). (2) Relatively high-flow velocity was observed in the posterior cerebral arteries of children, and in the ophthalmic arteries of adult cases. (3) In several occasions, very low-flow velocity values were still detected despite the fact that with angiography, the respective arterial segments were hardly opacified. The relation and discrepancy between these results and the angiographic findings, and the potential application of transcranial doppler in assessing and grading the severity of moyamoya disease are discussed.

Study of the posterior circulation in moyamoya disease. Part 2: Visual disturbances and surgical treatment.

The involvement of the posterior circulation in moyamoya disease was studied in 178 patients. Forty-three had several types of disturbance such as visual field defect, decreased visual acuity, episodes of blindness, and scintillating scotomata. Most of these symptoms were attributed to occlusive lesions in the posterior circulation. Visual disturbances were seen more often in patients with a juvenile onset than in cases of adult onset. Superficial temporal artery (STA) to middle cerebral artery (MCA) anastomosis and encephalomyosynangiosis (EMS) improved the cerebral perfusion both in the anterior and posterior circulation by redistribution of blood. In most cases, the visual symptoms subsided or were stabilized after STA-MCA anastomosis and EMS. These surgical procedures did not, however, lead to direct revascularization in cases of ischemia in the visual cortex. In five patients with impending blindness, transplantation of the omentum to the occipital lobe led to improved vision.

Angiographic feature and clinical evaluation of the anterior falx artery (author's transl)

The anterior falx artery which is a small meningeal branch of the anterior ethmoidal artery from the ophthalmic artery was described by Kuru (1967). Shiga(1968), Pollock and Newton (1968) reported the anatomy, angiographic features and some clinical evaluations of this artery. In this report, we shall demonstrate the angiographic findings and clinical evaluation of the anterior faix artery, based on a thousand patients, or 1254 serial angiograms which were taken between July, 1973 and June, 1978. All these angiograms were of good quality. Through the analysis of these material, the following results were obtained: The anterior falx artery was visualized in 21% of 217 normal cases and in 35% of pathologic cases (Table 1). This artery was visualized in 33.2% of left carotid angiograms, but only in 18.2% of right carotid angiograms. We also noticed that this artery is opacified more frequently in the pathologic side than the other side (Table 2). Bilateral carotid angiograms were taken in 221 patients and 94(42%)showed anterior falx arteries. In eight cases, two different anterior falx arteries were demonstrated. Anterior falx artery is important for collateral circulation in moyamoya disease and cerebral thrombosis. This artery sometimes supplies the meningioma, the arterio-venous malformation and other tumors invading into the dura. In addition, it could be stressed that there was dilatation of this artery in many patients with chronic subdural hematoma, subacute meningitis or malignant leptomeningeal dissemination. These dilatations may be due to compression of bridging vein and/or to circulatory change. Another important feature is the change of visualization of this artery in the same patient. In 15 of 28 patients in whom carotid angiographies were repeated, the visualization of the anterior faix arteries varied following clinical course from one examination to another. These differences were demonstrated between preoperative and postoperative angiograms in cases of subdural hematoma, cerebral tumor and acute head injury. These observations have convinced us that the anterior faix artery often has important clinical significance.