Indirect Synangiosis Research Articles

Combined cerebral revascularization for moyamoya disease

Combined cerebral revascularization with direct and indirect components is recognized as the most appropriate method for treating patients with Moyamoya disease all over the world, however, large studies on its effectiveness in Russia have not yet been conducted. Was to evaluate the results of combined cerebral revascularization in patients with Moyamoya disease with an analysis of the clinical state and perfusion and angiographic features of neoangiogenesis. For the period from 2013 to 2020 in N.N. Burdenko National Medical Research Center of Neurosurgery 79 combined revascularizations were performed in 55 patients with Moyamoya disease. The average age was 13.9±10.11 years. All patients were examined according to a single protocol, including a comprehensive assessment of the clinical symptoms, the state of the brain tissue, the cerebral vascular system, and cerebral blood flow. The results of surgical treatment were evaluated in the early postoperative and long-term periods. The average follow-up period was 14.66±13.17 months. In the postoperative period, the dynamics of neurological status and cerebral blood flow were assessed and the features of neoangiogenesis from various components of revascularization were studied. In the early postoperative period, in 77.2% of cases, a good treatment result was observed, with no negative dynamics of the neurological status. Ischemic stroke in the operated hemisphere developed in 4 cases (5.1%). In the follow-up period, an improvement in neurological symptoms was observed in 76.6%. Improvement of cerebral blood flow was noted in 92.4% of cases, direct anastomoses functioned in 94.3%, and signs of neovascularization in the area of indirect synangiosis were observed in 80.0%. At the same time, a complementary influence of direct and indirect components of revascularization was revealed in ensuring good general angiographic and perfusion results. Combined revascularization is a highly effective method of surgical treatment of all patients with Moyamoya disease.

Abstract WP131: Repeat Bypass Surgery for Moyamoya Disease Refractory to Previous Surgery

Background and Purpose: Surgical revascularization is known to reduce subsequent incidence of ischemic and hemorrhagic stroke with low morbidity in moyamoya disease. However, repeat bypass surgery is required for a certain subgroup of patients, although the information on indication, surgical technique, and outcome is limited. Therefore, this study was aimed to precisely analyze clinical features, surgical technique, and long-term outcome of repeat bypass surgery for refractory moyamoya disease. Methods: This study included totally 20 surgeries for18 patients who underwent repeat bypass surgery because previous surgery was inadequate in 10 surgeries (Group A) or because the posterior cerebral artery was further involved after surgery in 10 (Group B). There were 7 males and 11 females. Their age ranged from one to 69 years. Precise radiological examinations were performed before surgery, using MRI, cerebral angiography, and SPECT. In Group A, all patients who previously underwent inadequate surgery repeated headache attack, TIA, or hemorrhagic stroke, and underwent repeat bypass surgery targeted to the non-revascularized area, using STA-MCA anastomosis and/or indirect synangiosis as appropriate. On the other hands, occipital artery to posterior cerebral artery (OA-PCA) anastomosis and/or indirect bypass was required in Group B who developed disease progression in the PCA. Results: All 18 patients successfully underwent repeat bypass surgery. Postoperative course was uneventful. Postoperative examinations revealed good revascularization in the operated hemispheres and the improvement of cerebral hemodynamics. Headache attack and TIA disappeared within 6 months at the latest after surgery. During follow-up periods, one (5.6% per person) of 18 patients died of recurrent hemorrhagic stroke two years after repeat bypass surgery. Conclusion: Repeat bypass surgery is feasible and effective to reduce further incidence of headache attack, TIA, and ischemic and hemorrhagic stroke. Through precise radiological analysis, surgical procedures should be planned to yield maximal therapeutic effects.

Berlin Grading System Can Stratify the Onset and Predict Perioperative Complications in Adult Moyamoya Disease.

The grading system for moyamoya disease is not established. To assess the usefulness of a recently proposed grading system for stratifying the clinical severity and predicting postoperative morbidity in adult moyamoya disease. We investigated 176 hemispheres from 89 adult patients who were diagnosed with moyamoya disease in Japan. Their data were analyzed using the Berlin grading system with minor modifications. After summarizing the numerical values for digital subtraction angiography (1-3 points), magnetic resonance imaging (0-1 points), and single-photon emission computed tomography (0-2 points), 3 grades of moyamoya disease were defined: mild (grade I) = 1 to 2 points, moderate (grade II) = 3 to 4 points, and severe (grade III) = 5 to 6 points. In total, 82 of 161 hemispheres underwent superficial temporal artery to middle cerebral artery anastomosis and indirect synangiosis. Postoperative neurological morbidity was included within 30 d after surgery. Preoperative examinations categorized 87 hemispheres as grade I, 39 as grade II, and 50 as grade III. There was a significant correlation between the Berlin grading system and clinical severity (P < .001). Perioperative complications occurred in 12 of 82 (14.6%) hemispheres, including transient ischemic attack in 3 hemispheres, ischemic stroke in 4 hemispheres, symptomatic hyperperfusion in 4 hemispheres, and intracerebral hemorrhage in 1 hemisphere. The Berlin grading system was related to their occurrence (P < .001). The Berlin grading system facilitates the stratification of clinical severity and predicting postoperative neurological morbidity in adult moyamoya disease, thereby suggesting its general usage in clinical practice.

Abstract 101: Repeat Bypass Surgery for Moyamoya Disease Refractory to Previous Surgery

Purpose: Surgical revascularization is known to reduce subsequent incidence of ischemic and hemorrhagic stroke with low morbidity in moyamoya disease. However, repeat bypass surgery is required for a certain subgroup of patients, although the information on indication, surgical technique, and outcome is limited. Therefore, this study was aimed to precisely analyze clinical features, surgical technique, and long-term outcome of repeat bypass surgery for refractory moyamoya disease. Methods: This study included 16 patients who underwent repeat bypass surgery because previous surgery was inadequate in 10 patients or because the posterior cerebral artery was further involved after surgery in 6. There were 7 males and 9 females. Their age ranged from one to 69 years. Precise radiological examinations were performed before surgery, using MRI, cerebral angiography, and SPECT. All 10 patients who previously underwent inadequate surgery repeated headache attack, TIA, or hemorrhagic stroke, and underwent repeat bypass surgery targeted to the non-revascularized area, using STA-MCA anastomosis and/or indirect synangiosis as appropriate. OA-PCA anastomosis and/or indirect bypass was required in 6 patients who developed disease progression in the PCA. Results: All 16 patients successfully underwent repeat bypass surgery. Postoperative course was uneventful. Postoperative examinations revealed good revascularization in the operated hemispheres and the improvement of cerebral hemodynamics. Headache attack and TIA disappeared within 6 months at the latest after surgery. During follow-up periods, one of 16 patients died of recurrent hemorrhagic stroke two years after repeat bypass surgery. Conclusion: Repeat bypass surgery is feasible and effective to reduce further incidence of headache attack, TIA, and ischemic and hemorrhagic stroke. Through precise radiological analysis, surgical procedures should be planned to yield maximal therapeutic effects.

Diagnosis and Treatment of Moyamoya Disease

Moyamoya disease is a cerebrovascular disease of unknown etiology, which is characterized by bilateral stenosis or occlusion at terminal portion of internal carotid artery and at proximal portion of anterior cerebral artery and /or middle cerebral artery and abnormal vascular network in the vicinity of the arterial occlusions. It occurs frequently in Asian countries, particularly in Korea and Japan, but is rare in Western countries. To establish the etiology of moyamoya disease, much about the pathology from autopsies, factors involved in its pathogenesis, and its genetics have been studied. It may occur at any age from childhood to adulthood and in general, initial manifestation is cerebral ischemic symptoms in children and intracranial hemorrhage symptoms in adults. Because it progress and cause recurrent stroke, early diagnosis and proper management has been recognized. Cerebral angiography is essential for definitive diagnosis and treatment plan. Magnetic resonance imaging/magnetic resonance angiography is useful for diagnosis and follow-up tools after revascularization. Evaluation of the cerebral hemodynamics by single photon emission computed tomography and positron emission tomography is useful for diagnosis and assessment of the severity of cerebral ischemia in moyamoya patients. Surgical revascularization is effective for moyamoya disease manifesting as ischemic symptoms, to prevent further ischemia and infarction. In hemorrhagic type moyamoya disease, revascularization can be considered. Direct bypass, indirect synangiosis and combined methods are used. Outcomes of revascularization are excellent in preventing transient ischemic attacks in most patients. (Ewha Med J 2013;36(1):9-17)

もやもや病に対する血行再建術後の虚血合併症

Surgical revascularization for such conditions as superficial temporal artery (STA)-middle cerebral artery (MCA) anastomosis and/or indirect synangiosis using STA, dura mater, temporal muscle and pericranium has been commonly recognized as standard treatment for patients with moyamoya disease. However, various postoperative complications have been reported. Of these complications, postoperative ischemic stroke influence prognosis. We retrospectively reviewed patients with ischemic complications after revascularization, and assessed the incidence and mechanism of this ischemic complication. For this study, postoperative ischemic complication was defined as a newly developed infarction within two weeks after surgery, which was confirmed by follow-up imaging studies. This study included 84 hemispheres of 62 patients with moyamoya disease that underwent revascularization surgery between December 2006 and August 2011. Patients under four years of age were treated with indirect revascularization, from four to 39 of age with direct and indirect revascularization, and over 40 of age with direct revascularization. Ischemic complications were found in five patients (7.2%) of six hemispheres (6.4%). All patients were male. The age at the time of surgery ranged from three to 44 (mean 19.3 years). These infarctions were located in the cerebral hemisphere ipsilateral to the site of surgery in five, and contralateral in one. All of them occurred within four days after surgery. Preoperative angiograms revealed disappearance of the anterior cerebral artery (ACA) and middle cerebral artery (MCA) and marked development collateral vessels from posterior cerebral artery (PCA) in all patients, and stenosis of PCA in two patients. Two patients were two-year-old infants, who made rapid progress just before indirect revascularization surgery. In patients who exhibit dependence on PCA, careful postoperative management, such as control of blood pressure, is important to prevent these ischemic complications. It is also recommended that direct revascularization surgery be performed for any infants with rapid progression berore surgery.

Abstract 2413: Postoperative Cerebral Hyperperfusion after Superficial Temporal Artery-Middle Cerebral Artery Anastomosis and Indirect Synangiosis in Moyamoya Disease: PET and SPECT Study

Background Postoperative cerebral hyperperfusion is known to occur after superficial temporal artery to middle cerebral artery (STA-MCA) anastomosis and indirect synangiosis in moyamoya disease. However, the clinical features and pathophysiology still remain to be elucidated. Objective To clarify the incidence and pathogenesis of postoperative hyperperfusion after surgical revascularization for moyamoya disease. Methods This study included 41 consecutive patients (58 surgeries) who underwent STA-MCA anastomosis and indirect synangiosis for moyamoya disease. Their medical records were evaluated to identify clinical features of postoperative hyperperfusion. Using 15O-gas positron emission tomography (PET), cerebral hemodynamics and metabolism were determined before surgery in all patients. Using 123I-IMP single photon emission computed tomography (SPECT), cerebral blood flow was qualitatively measured on Day 0, 2, and 7 after surgery in all patients. A multivariate logistic regression analysis was conducted to identify the predictors for postoperative hyperperfusion. Results Postoperative hyperperfusion was observed in 29 (50.0%) of 58 operated sides. In pediatric patients, it was quite rare. Thus, symptomatic and asymptomatic hyperperfusion occurred in 1 (5%) and 3 (15%) of 20 sides, respectively. In adult cases, however, symptomatic and asymptomatic hyperperfusion were significantly more often (P=0.0037 and P=0.026, respectively) and were noted in 12 (31.5%) and 13 (34.2%) of 38 sides, respectively. A logistic regression analysis revealed that cerebral blood volume (CBV) increase before surgery was a significant predictors for symptomatic hyperperfusion in adults (P=0.036). Furthermore, hyperperfusion immediately after surgery was at significantly higher risk to be symptomatic (7/9=77.7%, P=0.033). Conclusions Postoperative hyperperfusion after STA-MCA anastomosis in adult moyamoya disease is not rare. Preoperative CBV increase was closely related to the occurrence of symptomatic hyperperfusion in adult cases. Hyperperfusion immediately after surgery may easily cause neurological deficits or other symptoms. Precise evaluation of cerebral hemodynamics and metabolism before and after surgery would be valuable to predict postoperative hyperperfusion and prevent perioperative complications.

Transient Crossed Cerebellar Diaschisis Due to Cerebral Hyperperfusion Following Surgical Revascularization for Moyamoya Disease

Crossed cerebellar diaschisis (CCD) often occurs after ischemic or hemorrhagic stroke that damages the cortico-ponto-cerebellar pathway. However, CCD due to cerebral hyperperfusion following cerebrovascular reconstruction is rare. A 61-year-old woman presented with transient CCD due to cerebral hyperperfusion following bypass surgery for adult moyamoya disease. She developed transient weakness of the right extremities and was diagnosed with moyamoya disease. First, she underwent superficial temporal artery to middle cerebral artery (STA-MCA) anastomosis with indirect synangiosis on the left. Postoperative course was uneventful. Subsequently, she underwent STA-MCA anastomosis with indirect synangiosis on the right. She complained of mild headache on the right, and single photon emission computed tomography (SPECT) performed on the 7th postoperative day demonstrated hyperperfusion in the right frontal and temporal lobes associated with hypoperfusion in the left cerebellum. Magnetic resonance (MR) imaging demonstrated no new lesions and MR angiography showed patent STA-MCA bypass. Subsequent SPECT showed disappearance of both hyperperfusion and CCD. This case strongly suggests that cerebral hyperperfusion after bypass surgery for moyamoya disease may cause transient CCD. Although the clinical significance is still obscure, this phenomenon indicates the cortico-ponto-cerebellar pathway is interrupted due to hyperperfusion, suggesting the development of hyperperfusion syndrome. Careful observation of cerebral hemodynamics after bypass surgery is warranted to avoid hyperperfusion-related complications.

Moyamoya disease presenting with subarachnoid hemorrhage localized over the frontal cortex: case report

Background In moyamoya disease, intracranial bleeding is known to occur because of the rupture of saccular aneurysms in the circle of Willis or because of the rupture of dilated, fragile moyamoya vessels. The former causes subarachnoid hemorrhage (SAH), and the latter causes intracerebral or intraventricular hemorrhage. Case description In this report, we describe the case of a 34-year-old woman with moyamoya disease who suddenly developed headache and jacksonian seizure. Plain computed tomographic scans on admission revealed SAH localized over the left frontal cortex. The patient was diagnosed with moyamoya disease on cerebral angiography. However, no aneurysm was found on cerebral angiography. Positron emission tomography showed the reduction of CBF and its reactivity to acetazolamide and the elevation of CBV in the left hemisphere. She underwent STA to MCA anastomosis and indirect synangiosis. Intraoperative observations revealed that the pial arterioles were markedly dilated on the brain surface. The CBF in the left hemisphere significantly improved after surgery. The patient has experienced no further episode of cerebral ischemia or intracranial bleeding. Conclusions Subarachnoid hemorrhage of unknown cause is quite rare in moyamoya disease. Based on the findings in the present case, the dilated collateral arteries on the brain surface may rupture and cause SAH over the cerebral cortex, which is the third cause of intracranial bleeding in patients with persistent cerebral ischemia due to moyamoya disease.

もやもや病の治療戦略と長期予後

We review clinical results after surgical revascularization in 164 patients with moyamoya disease. The surgical procedures include superficial temporal artery to middle cerebral artery (STA-MCA) anastomosis and indirect synangiosis using STA, dura mater, temporal muscle and pericranium. There were no significant differences in the incidence of perioperative morbidity among surgical procedures. Indirect synangiosis induced surgical collaterals in most of the pediatric patients, but in only 60% of adult patients. Postoperative angiography and SPECT/PET studies revealed that the development of surgical collaterals through indirect synangiosis depended on the operated areas. During follow-up periods, 10 of 164 patients (6.1%) experienced ischemic (n=3) or hemorrhagic stroke (n=7) after surgery. Completed stroke and “small craniotomy” surgery were significantly associated with poor intellectual outcome in pediatric patients.

Determinants of intellectual outcome after surgical revascularization in pediatric moyamoya disease: a multivariate analysis.

The aim of this study was to clarify predictors for poor intellectual outcome in pediatric moyamoya disease. Fifty-two pediatric patients were included. Clinical diagnosis was transient ischemic attacks (TIA) in 35 and completed stroke in 17. Ten patients underwent indirect synangiosis through "small craniotomy," whereas the other 42 underwent superficial temporal artery (STA)-middle cerebral artery (MCA) anastomosis and indirect synangiosis through "large craniotomy." Full-scale IQ (FSIQ) was measured using the Wechsler intelligence scale for children (WISC) after surgery. Multivariate logistic regression models were applied to test the effect of clinical factors on intellectual outcome. Eight patients revealed mentally impaired status (FSIQ<70). Multivariate analysis revealed that completed stroke and "small craniotomy" surgery were significantly associated with poor intellectual outcome. Odds ratios of each factor were 33.4 (95% CI, 2.4-474) and 19.6 (95% CI, 1.8-215) respectively. Early diagnosis and the revascularization procedure over as wide an area as possible may be essential to improve their intellectual outcome.

小児および成人もやもや病に対する脳血行再建術の長期効果

We analyzed overall outcome after surgical revascularization in 149 patients with moyamoya disease. Of 61 childhood patients, 58 (95.1%) have not experienced further ischemic episode during follow-up periods. Postoperative angiograms showed well-developed collaterals via STA-MCA anastomosis and indirect synangiosis. Total IQs were significantly lower in childhood patients who had cerebral infarction at onset. Of 40 adult patients with ischemic-type moyamoya disease, 35 (87.5%) have not experienced further episodes of stroke. However, 3 (7.5%) patients had cerebral infarction in the contralateral side or in the vertebrobasilar territory, and 2 (5.0%) suffered intracranial bleeding during follow-up periods. Of 34 adults who underwent bypass surgery for hemorrhagic-type moyamoya disease, 7 (20.6%) developed rebleeding. Statistical analysis revealed that STA-MCA anastomosis combined with indirect synangiosis may significantly reduce the risk for rebleeding. Clinical strategies should be decided for adult patients with asymptomatic moyamoya disease.

Regional cerebral hemodynamics in childhood moyamoya disease

Regional cerebral blood flow (rCBF) and its reactivity to acetazolamide were analyzed in a series of 15 cases of childhood moyamoya disease, using the xenon-133 inhalation method and single photon emission CT (SPECT). Most of the patients had normal mean hemispheric cerebral blood flow (mCBF), comparable to that of age-matched healthy children. However, they had abnormal rCBF distribution and disturbed reactivity to acetazolamide in the territory of the internal carotid artery, especially in the frontal lobe. Surgical revascularization for the anterior circulation, which consisted of STA-MCA anastomosis and indirect synangiosis, dramatically improved these cerebral hemodynamics in the anterior circulation, including the frontal lobe, and reactivity to acetazolamide in the whole brain. These results suggest that surgical revascularization for the anterior circulation should be carried out in order to improve cerebral hemodynamics as widely as possible, especially in the frontal lobe, and may improve cerebral perfusion reserve in the posterior circulation.

Hemodynamic Evaluation of Vascular Reconstructive Surgery for Childhood Moyamoya Disease Using Single Photon Emission Computed Tomography

To evaluate the efficacy of vascular reconstructive surgery for childhood moyamoya disease, the cerebral blood flow (CBF) in 31 hemispheres of 16 patients was examined by single photon emission computed tomography (SPECT) using the 133Xe inhalation method. Results were divided into two groups; 17 hemispheres with superficial temporal artery-middle cerebral artery (STA-MCA) anastomosis [A(+) group] and 14 hemispheres without anastomosis [A(-) group]. The mean hemispheric CBF (mCBF) and regional CBF (rCBF) in the frontal, temporal, occipital, and basal ganglia regions were calculated. Pre- and postoperative SPECT on the 10 hemispheres of the A(+) group showed an increase in mCBF in 6 hemispheres, the disappearance of the low perfusion area (LPA) in all 5 hemispheres where LPA was present before surgery, and an improvement in rCBF distribution (an increase in rCBF in the frontal and temporal lobes and a decrease in the basal ganglia). This suggests that vascular reconstruction is greatly effective in treating this disease. A comparison between the A(+) group and the A(-) group by postoperative SPECT, as well as the clinical outcomes and the postoperative findings of electroencephalography and angiography, revealed that the A(+) group was superior to the A(-) group in the frequency of LPA (12% and 43%, respectively) and rCBF in the frontal region where STA-MCA anastomosis was usually performed. These results indicate that STA-MCA anastomosis with indirect synangiosis is the most effective treatment of childhood moyamoya disease.