Direct Bypass Surgery Research Articles

Novel Indirect Revascularization Technique with Preservation of Temporal Muscle Function for Moyamoya Disease Encephalo-Duro-Fascio-Arterio-Pericranial-Synangiosis: A Case Series and Technical Note

Direct and/or indirect bypass surgery is the established approach for preventing stroke in patients with moyamoya disease. However, conventional indirect revascularization, including encephalo-myo-synangiosis, has some disadvantages associated with the mass effect of the temporal muscle under the bone flap and postsurgical depression in the temporal region. We devised a novel indirect revascularization method, using only the temporal fascia, to address the aforementioned disadvantages. A skin incision was performed along the superficial temporal artery. The temporal fascia was cut such that the base of the fascia flap was on the posterior side. The fascia and temporal muscles were dissected separately. After turning over the fascia, the muscle was cut such that the base of the muscle flap was on the anterior side. Craniotomy, direct bypass, and encephalo-duro-synangiosis were performed conventionally. Only the temporal fascia was used for indirect revascularization and duraplasty. The muscle was replaced in the anatomically correct position after replacing the bone flap. We performed the aforementioned surgery on 18 (13 women and 5 men) consecutive patients (21 cerebral hemispheres) enrolled between 2012 and 2016. The average age was 28.7 years. The mean follow-up period was 31.6 months. In 17 patients (94%), the symptoms and cerebral blood flow improved. Digital subtraction angiography showed satisfactory angiogenesis from the temporal fascia. Depression in the temporal region and atrophy of the temporal muscle were negligible. This surgical technique provides good clinical and cosmetic outcomes. It may also be one of the good surgical treatments available for symptomatic moyamoya disease.

Marked Changes in Blood-Brain Barrier Biomarkers After Direct Bypass Surgery for Moyamoya Angiopathy: Preliminary Study

The blood-brain barrier (BBB) of patients with moyamoya angiopathy (MMA) is unstable, which may contribute to transient neurologic symptoms (TNS) after direct bypass surgery. However, BBB-related proteins have never been investigated. The purpose of this study was to evaluate the perioperative serum levels of biomarkers representing BBB function in MMA patients based on the hypothesis that postoperative hemodynamic change may disrupt the BBB. A total of 12 hemispheres in 11 patients with MMA were prospectively examined. Direct revascularization surgery was performed for all cases. The serum levels of tight junction (occludin and claudin 5), adherens junction (vascular endothelial-cadherin) proteins, and matrix metalloproteinase (MMP)-2 and MMP-9 were measured quantitatively 1 day before surgery and on postoperative days 1, 4, and7. Successful patency of the direct bypass was achieved in all. The serum level of occludin was significantly increased on postoperative day 1, and the levels in 2 cases with TNS were markedly elevated over 10-fold higher than baseline. Furthermore, the postoperative MMP-9 levels were significantly elevated on each day. On the other hand, there was no significant fluctuation in claudin 5, vascular endothelial-cadherin, and MMP-2 level. Marked changes in biomarkers representing the tight junction of the BBB were observed. These preliminary results suggest that marked hemodynamic change and TNS in some patients are associated with disruption of the BBB after direct bypass surgery for MMA.

Predicting the Occurrence of Hemorrhagic Cerebral Hyperperfusion Syndrome Using Regional Cerebral Blood Flow After Direct Bypass Surgery in Patients with Moyamoya Disease

Superficial temporal artery-middle cerebral artery anastomosis is an established treatment for moyamoya disease. However, hemorrhagic cerebral hyperperfusion syndrome (CHS) leads to poor outcomes. This study aimed to identify predictors of hemorrhagic CHS based on regional cerebral blood flow (rCBF) in patients with moyamoya disease. The study included 251 hemispheres in 155 patients with moyamoya disease who underwent preoperative and postoperative rCBF measurements and superficial temporal artery-middle cerebral artery double anastomosis. We used rCBF increase rate for predicting hemorrhagic CHS. rCBF increase rate was calculated by 2 methods. In method 1, the rCBF value on the operated side was compared with the rCBF value on the nonoperated side. In method 2, the postoperative rCBF value on the operated side was compared with the preoperative rCBF value on the operated side. Patients were classified into 4 groups according to rCBF increase rate to predict risk of hemorrhagic CHS. Hemorrhagic CHS occurred in 7 (2.8%) hemispheres (no children). Severe hemorrhagic CHS occurred in only 1 (0.4%) hemisphere. Hemorrhagic CHS was observed in patients with ≥30% rCBF increase according to method 1 and ≥50% rCBF increase according to method 2 and was most frequently noted in ≥100% rCBF increase. Predictors for hemorrhagic CHS were ≥30% rCBF increase when using method 1 and ≥50% increase when using method2.

Minimally invasive direct coronary bypass surgery via distal mini-sternotomy

Minimally invasive direct coronary artery bypass grafting (MIDCAB) was developed to decrease perioperative morbidity, some of which may be related to the use of cardiopulmonary bypass and to cross-clamping of the aorta. We report our initial experience with multivessel MIDCAB via distal mini-sternotomy (DIMS). DIMS is performed to gain access to the left and right internal thoracic arteries and to reach the left anterior descending coronary artery (LAD), diagonal branches, and right coronary artery (RCA). Between January 2016 and January 2017, 12patients with significant coronary artery disease of the LAD and the RCA underwent multivessel, all-arterial MIDCAB through adistal midline skin incision from the fourth intercostal space to the xyphoid process, with L‑ or T‑shaped division of the sternum. The mean age of the patients was 61.5 ± 5.2years (range: 52-71years). We performed all-arterial revascularization using the left internal mammary artery in 12patients, the radial artery in ten, and the right internal mammary artery in twopatients. The mean number of grafts per patient was 2.08 ± 0.4 (range: 2-3). The mean length of the skin incision was 8.5 ± 1.3 cm (range: 7-11 cm). There was no perioperative ischemia, postoperative bleeding, or arrhythmia events. No postoperative cognitive dysfunction occurred. The mean hospital stay was 5.6days. No major adverse cardiac events (MACE) occurred at the 12-month follow-up. At follow-up, all patients were in New York Heart Association classI and there were no wound complications. Although MIDCAB-DIMS is technically more demanding than conventional procedures and our experience is limited, we conclude that this technique can be used safely in selected patients, with promising 12-month follow-up results.

Long-term outcome in extracranial-intracranial bypass surgery for severe steno-occlusive disease of intracranial internal carotid or middle cerebral artery

ObjectivesWe report the long-term outcome and rates of recurrent cerebral ischemic events in our cohort of carefully selected patients after STA-MCA bypass for severe steno-occlusive disease of intracranial ICA or MCA with exhausted cerebral vasodilatory reserve. Patients and MethodsIn this retrospective study, we reviewed the hospital records for all patients who underwent direct superficial temporal artery-middle cerebral artery bypass surgery at our institution from January 2010 to August 2017. Patients were included in the study if they presented with transient ischemic attack or non-disabling stroke due to a severe steno-occlusive lesions of the intracranial internal carotid artery or middle cerebral artery with abnormal cerebral vasodilatory reserve on imaging. The overall event rate is defined as transient ischemic attack, acute ischemic stroke, peri-operative stroke or death. Results69 patients were included in the study. The median age of cohort was 57 years (inter-quartile range 36–78). Median follow up period in our study was 73 months (range 2–90 months). The overall event rate post-treatment during the follow up period is 20.2%. In contrast, previous studies have showed that patients who underwent best medical therapy had a higher recurrent ischemic stroke rate over a 2–3-year period. ConclusionThis study suggests that carefully selected patients with severe steno-occlusive disease and significantly abnormal cerebral hemodynamic reserve who undergo extracranial-intracranial bypass surgery, may benefit from long-term prevention of symptomatic cerebral ischemic events.

Intraoperative evaluation of local cerebral hemodynamic change by indocyanine green videoangiography: prediction of incidence and duration of postoperative transient neurological events in patients with moyamoya disease.

Transient neurological events (TNEs) occur frequently in the acute phase after direct bypass surgery for moyamoya disease (MMD), but there is currently no way to predict them. FlowInsight is a specialized software for analyzing indocyanine green (ICG) videoangiography taken with a surgical microscope. The purpose of this study was to investigate whether intraoperative evaluation of local hemodynamic changes around anastomotic sites using FlowInsight could predict the incidence and duration of TNEs. From patients who were diagnosed with MMD in our hospital between August 2014 and March 2017 and who underwent superficial temporal artery-middle cerebral artery bypass surgery, we investigated 25 hemispheres (in 22 patients) in which intraoperative ICG analysis was performed using FlowInsight. To evaluate the local cerebral hemodynamics before and after anastomosis, regions of interest were set at 3 locations on the brain surface around the anastomotic site, and the mean cerebral blood flow (CBF), mean gradation (Grad), mean transit time (MTT), and mean time to peak (TTP) were calculated from the 3 regions of interest. Furthermore, the change rate in CBF (ΔCBF [%]) was calculated using the formula (postanastomosis mean CBF - preanastomosis mean CBF)/preanastomosis mean CBF. ΔGrad (%), ΔMTT (%), and ΔTTP (%) were similarly calculated. Postoperative stroke without TNE occurred in 2 of the 25 hemispheres. These 2 hemispheres (in 2 patients) were excluded from the study, and data from the remaining 23 hemispheres (in 20 patients) were analyzed. For each parameter (ΔCBF, ΔGrad, ΔMTT, and ΔTTP) calculated by FlowInsight, the difference between the groups with and without TNEs was significant. The median values for ΔCBF and ΔGrad were significantly higher in the TNE group than in the no-TNE group (ΔCBF 30.13 vs 3.54, p = 0.0106; ΔGrad 62.05 vs 10.78, p = 0.00435), whereas the median values for ΔMTT and ΔTTP were significantly lower in the TNE group (ΔMTT -16.90 vs -7.393, p = 0.023; ΔTTP -29.07 vs -7.02, p = 0.00342). Comparison of the area under the curve (AUC) for each parameter showed that ΔTTP had the highest AUC and was the parameter with the highest diagnostic accuracy (AUC 0.857). The Youden index revealed that the optimal cutoff value of ΔTTP was -11.61 (sensitivity 77.8%, specificity 71.4%) as a predictor of TNEs. In addition, Spearman's rank correlation coefficients were calculated, and ΔCBF, ΔGrad, ΔMTT, and ΔTTP each showed a strong correlation with the duration of TNEs. The larger the change in each parameter, the longer the TNEs persisted. Intraoperative ICG videoangiography findings were correlated with the occurrence and duration of TNEs after direct bypass surgery for MMD. Screening for cases at high risk of TNEs can be achieved by ICG analysis using FlowInsight.

Risk factors for and outcomes of postoperative complications in adult patients with moyamoya disease.

The risk factors and clinical significance of postoperative complications in moyamoya disease are still unclear. The aim of this study was to investigate the predictors of postoperative complications in moyamoya disease and examine the impact of complications on outcomes. The authors reviewed consecutive cases involving adult moyamoya disease patients who underwent indirect, direct, or combined bypass surgery in their hospital between 2009 and 2015. Preoperative clinical characteristics and radiographic features were recorded. Postoperative complications within 14 days after surgery were examined. Multivariate logistic regression analyses were performed to identify the risk factors for either postoperative ischemia or postoperative cerebral hyperperfusion. Outcome data, including recurrent strokes and neurological status (modified Rankin Scale [mRS]) during follow-up, were collected. Outcomes were compared between patients who had complications with those without complications, using propensity-score analysis to account for between-group differences in baseline characteristics. A total of 500 patients (610 hemispheres) were included in this study. Postoperative complications were observed in 74 operations (12.1%), including new postoperative ischemia in 30 cases (4.9%), hyperperfusion in 27 (4.4%), impaired wound healing in 12 (2.0%), and subdural effusion in 6 (1.0%). The complication rates for different surgery types were as follows: 12.6% (n = 25) for indirect bypass, 12.7% (n = 37) for direct bypass, and 10.0% (n = 12) for combined bypass (p = 0.726). Postoperative ischemic complications occurred in 30 hemispheres (4.9%) in 30 different patients, and postoperative symptomatic hyperperfusion occurred after 27 procedures (4.4%). Advanced Suzuki stage (OR 1.669, 95% CI 1.059-2.632, p = 0.027) and preoperative ischemic presentation (OR 5.845, 95% CI 1.654-20.653, p = 0.006) were significantly associated with postoperative ischemia. Preoperative ischemic presentation (OR 5.73, 95% CI 1.27-25.88, p = 0.023) and admission modified Rankin Scale (mRS) score (OR 1.81, 95% CI 1.06-3.10, p = 0.031) were significantly associated with symptomatic postoperative cerebral hyperperfusion syndrome (CHS). Compared with patients without postoperative complications, patients who experienced any postoperative complications had longer hospital stays and worse mRS scores at discharge (both p < 0.0001). At the final follow-up, no significant differences in functional disability (mRS score 3-6, 11.9% vs 4.5%, p = 0.116) and future stroke events (p = 0.513) between the 2 groups were detected. Advanced Suzuki stage and preoperative ischemic presentation were independent risk factors for postoperative ischemia; the mRS score on admission and preoperative ischemic presentation were independently associated with postoperative CHS. Although patients with postoperative complications had worse neurological status at discharge, postoperative complications had no associations with future stroke events or functional disability during follow-up.

Encephaloduroateriosynangiosis versus conservative treatment for patients with moyamoya disease at late Suzuki stage

The purpose of this study is to investigate the long-term outcomes after conservative and encephaloduroateriosynangiosis procedures for patients with moyamoya disease at late Suzuki stage. We retrospectively reviewed 64 patients (128 hemispheres) with moyamoya disease at late Suzuki Stage at Beijing Tiantan Hospital. Clinical features, radiologic findings, and outcomes were analyzed. The mean age at diagnosis was 29.0 ± 14.9 years. The distribution of the initial Suzuki stage of MMD was as follows: stage 4, n = 75; stage 5, n = 46; stage 6, n = 7, PCA involvement was observed in 4 (37.5%) hemispheres. The incidence of postoperative stroke was 6.7%. During the average follow-up of 46.9 ± 21.1 months, including postoperative and follow-up strokes, seven of 75 (9.3%) conservatively treated hemispheres and 10 of 87 (10.1%) surgically treated patients experienced a stroke event there was not statistically significant in the Kaplan-Meier curve of stroke incidence between the surgical group and conservative group (log-rank test, p = .848). However, the rate of perfusion improvement in indirect bypass surgically treated patients was higher than in those conservative treated patients 3 months after discharge (p < .05). Although indirect bypass surgery was shown to be effective in improving the cerebral perfusion in patients with MMD at late Suzuki stage, it failed to reduce the risk of recurrent stroke compared to conservative treatment. Further study is needed to determine whether direct bypass surgery is effective in MMD patients at late Suzuki stage.

Abstract TP405: Drastic Changes of Blood-brain Barrier Biomarkers After Direct Bypass Surgery for Moyamoya Angiopathy - A Preliminary Study -

Objective: Drastic hemodynamic change can be expected after direct bypass surgery for moyamoya angiopathy (MMA). However hemodynamic hyperperfusion could be observed presumably because of the increased permeability of blood-brain barrier (BBB). The assessment of BBB related molecular proteins has never been investigated. The purpose of this study was to evaluate the perioperative serum levels of biomarkers representing BBB function in MMA patients based on the hypothesis that postoperative hemodynamic change may cause the instability of BBB. Methods: A total of 13 hemispheres in 12 patients with MMA were prospectively investigated. A superficial temporal artery - middle cerebral artery direct bypass was performed in all cases. All patients had blood examinations before and postoperative day (POD) 1, 4 and 7, respectively. The serum levels of tight juction proteins (occludin [OCLN] and claudin 5 [CLDN5]) and an adherence junction protein (vascular endothelial [VE]-cadherin) were measured quantitatively using enzyme linked immunosorbent assay. The percent change of these proteins compared to preoperative was calculated. Results: Successful patency of the direct bypass was obtained in all cases. No apparent hemorrhagic or ischemic changes were observed on CT and MR image in this study. The mean percent changes of OCLN, CLDN5 and VE-Cadherin on POD 1 were 523.3 ± 598.0%, 108.7 ± 297.0% and -23.9 ± 25.5%, respectively. The following changes of OCLN and CLDN were decreased; -7.7 ± 63.8% and 80.0 ± 320.9% on POD 4 and -9.1 ± 54.2% and 36.3 ± 209.1% on POD 7, respectively. On the other hand, there was no remarkable fluctuation on those of VE-Cadherin in this series. The serum levels of OCLN and CLDN5 on POD 1 were markedly elevated over 10 folds higher than baseline in two patients, who had transient neurological symptoms within 13 days after the surgery. Conclusion: In patients with MMA undergone direct bypass surgery, drastic changes of biomarkers representing tight junction of BBB were observed. These preliminary results suggested that marked hemodynamic change and temporary neurological symptom in some patients might be associated with the instability of BBB after direct bypass surgery for MMA.

Postoperative Dilatation of Superficial Temporal Artery Associated with Transient Neurologic Symptoms After Direct Bypass Surgery for Moyamoya Angiopathy.

In moyamoya angiopathy, transient neurologic symptoms (TNS) are occasionally observed after superficial temporal artery (STA)-middle cerebral artery direct bypass surgery. The purpose of this study was to investigate the correlation between TNS and postoperative magnetic resonance imaging as well as perform a perfusion study. We reviewed 52 hemispheres in 33 consecutive patients with moyamoya angiopathy. TNS were defined as reversible neurologic dysfunction without any apparent intracranial infarction or hemorrhage. All patients underwent magnetic resonance imaging and single-photon emission computed tomography before and within 5 days after surgery. Maximum diameter of STA on time-of-flight magnetic resonance angiography and the dilatation ratio of STA were calculated. The presence of signal changes on fluid-attenuated inversion recovery images and regional cerebral blood flow were also evaluated. TNS were observed in 13 of 52 (25%) cases1-16 days after surgery. The mean preoperative STA dilatation, postoperative STA dilatation, and dilatation ratio of STA were 1.33 mm ± 0.27, 1.67 mm ± 0.30, and 29.31% ± 28.13%. Postoperative intraparenchymal cortical hyperintensity lesions and high-intensity signals in the cortex sulci (ivy sign) were detected in 24 (46.2%) cases and 29 (55.8%) cases, respectively. Univariate analyses demonstrated no association between TNS and postoperative signal change on fluid-attenuated inversion recovery images as well as cerebral blood flow. Only>1.5-fold dilatation of STA was significantly correlated with TNS (P < 0.0001). STA dilatation was correlated with TNS after direct bypass surgery for moyamoya angiopathy.

Angiosome Targeted PTA is More Important in Endovascular Revascularisation than in Surgical Revascularisation: Analysis of 545 Patients with Ischaemic Tissue Lesions

This study aimed to evaluate the impact of angiosome targeted (direct) revascularisation according to revascularisation method in patients with diabetes. This retrospective study cohort comprised 545 diabetic patients with critical limb ischaemia and tissue loss (Rutherford 5, 6). All patients underwent infrapopliteal endovascular (PTA) or open surgical revascularisation between January 2008 and December 2013. Differences in the outcome after direct revascularisation, bypass surgery, and PTA were investigated by means of Cox proportional hazards analysis. The endpoints were wound healing, leg salvage, and amputation free survival. Overall, 60.3% of the ischaemic wounds healed during 1 year of follow-up. The highest wound healing rate was achieved after direct bypass (77%) and the worst after indirect PTA (52%). The Cox proportional hazards analysis showed that the number of affected angiosomes <3 (HR 1.37, 95% CI 1.01–1.84) was associated with improved wound healing, whereas wound healing was poorest after indirect PTA (p = .001). When Cox proportional hazard analysis was adjusted for the number of affected angiosomes, direct bypass gave the best wound healing (p = 0.003). The overall amputation rate was 25.1% at 1 year of follow-up, and the Cox proportional hazards analysis indicated that haemodialysis compared with patients with no haemodialysis (HR 2.55, 95% CI 1.49–4.38), C-reactive protein ≥10 mg/dL (HR 2.05, 95% CI 1.45–2.90), atrial fibrillation (HR 1.54, 95% CI 1.05–2.26), and number of affected angiosomes >3 (HR 1.75, 95% CI 1.24–2.46) were significantly associated with poor leg salvage. Direct PTA was associated with a lower rate of major amputation compared with indirect PTA (HR 0.57 95% CI 0.37–0.89). In diabetics, indirect endovascular revascularisation leads to significantly worse wound healing and leg salvage rates compared with direct revascularisation. Therefore, endovascular procedures should be targeted according to the angiosome concept. In bypass surgery, however, the concept is of less value and the artery with the best runoff should be selected as the outflow artery.

Angiosome Targeted PTA is More Important in Endovascular Revascularisation than in Surgical Revascularisation: Analysis of 545 Patients with Ischaemic Tissue Lesions

This study aimed to evaluate the impact of angiosome targeted (direct) revascularisation according to revascularisation method in patients with diabetes. This retrospective study cohort comprised 545 diabetic patients with critical limb ischaemia and tissue loss (Rutherford 5, 6). All patients underwent infrapopliteal endovascular (PTA) or open surgical revascularisation between January 2008 and December 2013. Differences in the outcome after direct revascularisation, bypass surgery, and PTA were investigated by means of Cox proportional hazards analysis. The endpoints were wound healing, leg salvage, and amputation free survival. Overall, 60.3% of the ischaemic wounds healed during 1 year of follow-up. The highest wound healing rate was achieved after direct bypass (77%) and the worst after indirect PTA (52%). The Cox proportional hazards analysis showed that the number of affected angiosomes <3 (HR 1.37, 95% CI 1.01-1.84) was associated with improved wound healing, whereas wound healing was poorest after indirect PTA (p=.001). When Cox proportional hazard analysis was adjusted for the number of affected angiosomes, direct bypass gave the best wound healing (p=0.003). The overall amputation rate was 25.1% at 1 year of follow-up, and the Cox proportional hazards analysis indicated that haemodialysis compared with patients with no haemodialysis (HR 2.55, 95% CI 1.49-4.38), C-reactive protein ≥10mg/dL (HR 2.05, 95% CI 1.45-2.90), atrial fibrillation (HR 1.54, 95% CI 1.05-2.26), and number of affected angiosomes >3 (HR 1.75, 95% CI 1.24-2.46) were significantly associated with poor leg salvage. Direct PTA was associated with a lower rate of major amputation compared with indirect PTA (HR 0.57 95% CI 0.37-0.89). In diabetics, indirect endovascular revascularisation leads to significantly worse wound healing and leg salvage rates compared with direct revascularisation. Therefore, endovascular procedures should be targeted according to the angiosome concept. In bypass surgery, however, the concept is of less value and the artery with the best runoff should be selected as the outflow artery.

Clinical features and surgical treatment of hemorrhagic type moyamoya disease

Objective To investigate the clinical characteristics of hemorrhagic type moyamoya disease and its outcomes after revascularization. Methods The data of 46 patients with hemorrhagic moyamoya disease, including clinical features and surgical outcomes, were retrospectively reviewed. Among them, 42 cases were treated at Beijing Tiantan Hospital from August 2007 to November 2011. The other 4 cases were managed at the People's Liberation Army (PLA) 174 Hospital from August 2011 to June 2014. In this series of 46 patients, the operation of revascularization was performed in 50 hemispheres. Among them, direct superficial temporal artery to middle cerebral artery (STA-MCA)bypass surgery was conducted in 28 hemispheres, the encephalo-duro-arterio-synangiosis (EDAS) was performed in 10 hemispheres, and 12 hemispheres underwent a combination of STA-MCA bypass surgery and EDAS. Results The mean follow-up period was 52.5±6.5 months with a range of 18 ~ 87 months. Among the 19 cases with preoperative neurological deficiency, the symptoms were improved in 11cases, remained unchanged in 6 cases and became worse in 2 cases due to rebleeding. Among the preoperatively asymptomatic 27 cases, good outcomes were observed in 24 cases and rebleeding occurred in the non-surgical hemispheres of the remaining 3 cases. Follow-up CT Perfusion (CTP) and/or SPECT were performed in 25 cases and demonstrated significant improvement of cerebral blood perfusion in 20 cases and no remarkable change in 5 cases. Follow-up (at least 3 months post operation) DSA in the 15 patients who underwent STA-MCA bypass showed complete patency of the anastomosis and diminishing of the moyamoya vessels. In addition, 2 concurrent microaneurysms was found to have disappeared after the direct bypass surgery. Rebleeding developed in 2 (4%) hemispheres (post EDAS) in the surgical group and 3 (7%) hemispheres in the nonsurgical group. There was no statistical difference in the rate of rebleeding rate between the 2 groups(P>0.05). Conclusion The surgery of revascularization could improve the symptoms and cerebral perfusion for the patients with hemorrhagic moyamoya disease. Key words: Moyamoya disease; Hemorrhage; Cerebral revascularization; Treatment outcome

Disruption of Cortical Arterial Network is Associated with the Severity of Transient Neurologic Events After Direct Bypass Surgery in Adult Moyamoya Disease.

Transient neurologic events (TNEs) frequently occur after revascularization in adult moyamoya disease (MMD). In the present study, we hypothesized that cortical arterial network disruption may be associated with TNE severity after bypass surgery. This retrospective study included 76 hemispheres in 45 consecutive adult patients with MMD whounderwent direct revascularization surgery at our institution. We classified cortical arterial network disruption grade (NDG) into the following 4 categories based on angiography: NDG 0, >90% of suprasylvian cortical branches of the middle cerebral artery showed anterograde filling; NDG 1, 50%-90%; NDG 2, <50%; and NDG 3, none. TNE severity was assigned 1 of 4 grades based on symptom duration and clinical features: grade 0, none; grade 1, mild; grade 2, moderate; and grade 3, severe. We evaluated multiple clinical characteristics, including NDG, to identify factors that have a significant association with TNE severity. Of the 73 hemispheres without perioperative ischemic or hemorrhagic complications, the following degrees of TNEs were developed: grade 0, 33%; grade 1, 30%; grade 2, 22%; and grade 3, 15%. We determined that NDG and left-side surgery were significantly associated with TNE severity (P < 0.01 and P= 0.04, respectively). The NDG had excellent interobserver reliability (weighted κvalue= 0.96). There were no significant correlations between TNE severity and other clinical backgrounds. NDG is useful for the prediction of severity of TNEs after revascularization. Disturbed bypass flow spreading may lead to the development of TNEs in adult MMD.

Indirect Bypass Surgery May Be More Beneficial for Symptomatic Patients with Moyamoya Disease at Early Suzuki Stage

Moyamoya disease is a progressive stenosis or occlusion of the internal carotid artery. Revascularization surgery is considered the standard treatment. We conducted a retrospective study in hopes of finding indications for electing different surgical methods. A total of 55 hemispheres in 49 patients who received revascularization surgery between January 2013 and December 2015 were included. Medical data such as age and sex were extracted and risk factor analysis for vascular anastomosis patency was conducted with multivariable logistic regression. In this study, direct or combined bypass surgery had a higher incidence of perioperative neurologic defects than did indirect surgery (30.3% vs. 4.5%; P= 0.046). The rates of postsurgery stroke (6.2% vs. 18.2%) and modified Rankin Scale improvement (39.4% vs. 18.2%) were better in the direct or combined bypass surgery group, but no significant difference was found. Moreover, longer operative time (209 ± 29.4 minutes vs. 101 ± 16.5 minutes; P < 0.01) and longer hospital stay (9.0 ± 3.11 days vs. 5.3 ± 2.03 days; P < 0.01) made direct or combined bypass surgery less advantageous. Multivariable binary logistic regression showed that the late Suzuki stage is a more favorable factor than the early Suzuki stage (odd ratio, 7.78; confidence interval, 1.059-57.155; P= 0.044). Because vascular anastomosis patency in symptomatic patients with moyamoya disease at early Suzuki stage is relatively lower, indirect bypass surgery may be more beneficial for these patients in view of shorter operative time and hospital stay.

Low flow velocity in the middle cerebral artery predicting infarction after bypass surgery in adult moyamoya disease.

OBJECTIVE Direct and indirect bypass surgeries are recognized as the most effective treatments for preventing further stroke in adults with moyamoya disease (MMD). However, the risk factors for postoperative infarction after bypass surgery for MMD are not well established. Therefore, the objective of this study was to investigate the risk factors for postoperative infarction. In particular, the authors sought to determine whether transcranial Doppler (TCD) ultrasonography measurements of mean flow velocity (MFV) in the middle cerebral artery (MCA) could predict postrevascularization infarction. METHODS The medical records of patients with MMD who underwent direct bypass surgery at the authors' institution between July 2012 and April 2015 were reviewed. The MFV in the MCA was measured with TCD ultrasonography and categorized as high (> 80 cm/sec), medium (40-80 cm/sec), and low (< 40 cm/sec). Postoperative MRI, including diffusion-weighted imaging, was performed for all patients within a week of their surgery. Angiographic findings were classified according to the Suzuki scale. Postrevascularization infarction was defined as any diffusion restriction on postoperative MRI scans. Postoperative neurological status was assessed through a clinical chart review, and the modified Rankin Scale was used to evaluate clinical outcomes. RESULTS Of 43 hemispheres in which bypass surgery for MMD was performed, 11 showed postrevascularization infarction. Ten of these hemispheres had low MFV and 1 had medium MFV in the ipsilateral MCA. In both univariate and multivariate analyses, a low MFV was associated with postrevascularization infarction (adjusted OR 109.2, 95% CI 1.9-6245.3). A low MFV was also statistically significantly associated with more advanced MMD stage (p = 0.02). CONCLUSIONS A low MFV in the ipsilateral MCA may predict postrevascularization infarction. Bypass surgery for MMD appears to be safe in early-stage MMD. Results of TCD ultrasonography provide clinical data on the hemodynamics in MMD patients before and after revascularization.

Long-term follow-up of pediatric moyamoya disease treated by combined direct-indirect revascularization surgery: single institute experience with surgical and perioperative management.

Moyamoya disease (MMD) is a rare occlusive cerebrovascular disease that mainly presents in children as cerebral ischemia. Prompt treatment with either a direct or indirect revascularization procedure is necessary for children with MMD in order to prevent repeated ischemic events. We herein present our experience with combined direct and indirect bypass surgery for the treatment of pediatric MMD as well as our uniquely designed perioperative protocol. Twenty-three patients with MMD, aged between 2 and 16years old (mean 9.36), underwent 38 combined bypass procedures between 2008 and 2015. All patients underwent single superficial temporal artery-middle cerebral artery (STA-MCA) anastomosis combined with encephalo-duro-myo-synangiosis (EDMS). The perioperative management protocol was stratified into two unique eras: the first era with normotensive care and the second era with strict blood pressure control (systolic 100-130mmHg) and routine aspirin administration. Patients were followed after surgery for a period ranging between 3 and 131months (mean 77months) in yearly clinical and radiological follow-ups. Three postoperative complications were observed: two cases of cerebral hyperperfusion (2/38, 5.3%) and one case of perioperative minor stroke (1/38, 2.6%), two of which were in the first era. No strokes, either ischemic or hemorrhagic, were observed in the follow-up period, and the activity of daily living as shown by the modified Rankin Scale improved in 20 patients, with no deterioration being observed in any of our patients. STA-MCA bypass with EDMS is safe and effective for the management of pediatric MMD and provides long-term favorable outcomes. Perioperative care with blood pressure control combined with the administration of aspirin may reduce the potential risk of surgical complications.

Clinical implications of the cortical hyperintensity belt sign in fluid-attenuated inversion recovery images after bypass surgery for moyamoya disease.

OBJECTIVE Transient neurological symptoms are frequently observed during the early postoperative period after direct bypass surgery for moyamoya disease. Abnormal signal changes in the cerebral cortex can be seen in postoperative MR images. The purpose of this study was to reveal the radiological features of the "cortical hyperintensity belt (CHB) sign" in postoperative FLAIR images and to verify its relationship to transient neurological events (TNEs) and regional cerebral blood flow (rCBF). METHODS A total of 141 hemispheres in 107 consecutive patients with moyamoya disease who had undergone direct bypass surgery were analyzed. In all cases, FLAIR images were obtained during postoperative days (PODs) 1-3 and during the chronic period (3.2 ± 1.13 months after surgery). The CHB sign was defined as an intraparenchymal high-intensity signal within the cortex of the surgically treated hemisphere with no infarction or hemorrhage present. The territory of the middle cerebral artery was divided into anterior and posterior parts, with the extent of the CHB sign in each part scored as 0 for none; 1 for presence in less than half of the part; and 2 for presence in more than half of the part. The sum of these scores provided the CHB score (0-4). TNEs were defined as reversible neurological deficits detected both objectively and subjectively. The rCBF was measured with SPECT using N-isopropyl-p-[123I]iodoamphetamine before surgery and during PODs 1-3. The rCBF increase ratio was calculated by comparing the pre- and postoperative count activity. RESULTS Cortical hyperintensity belt signs were detected in 112 cases (79.4%) and all disappeared during the chronic period. Although all bypass grafts were anastomosed to the anterior part of the middle cerebral artery territory, CHB signs were much more pronounced in the posterior part (p < 0.0001). TNEs were observed in 86 cases (61.0%). Patients with TNEs showed significantly higher CHB scores than those without (2.31 ± 0.13 vs 1.24 ± 0.16, p < 0.0001). The CHB score, on the other hand, showed no relationship with the rCBF increase ratio (p = 0.775). In addition, the rCBF increase ratio did not differ between those patients with TNEs and those without (1.15 ± 0.033 vs 1.16 ± 0.037, p = 0.978). CONCLUSIONS The findings strongly suggest that the presence of the CHB sign during PODs 1-3 can be a predictor of TNEs after bypass surgery for moyamoya disease. On the other hand, presence of this sign appears to have no direct relationship with the postoperative local hyperperfusion phenomenon. Vasogenic edema can be hypothesized as the pathophysiology of the CHB sign, because the sign was transient and never accompanied by infarction in the present series.

Hemorrhagic Adult Unilateral Moyamoya Disease with Multiple Unruptured Intracranial Aneurysms: A Case Report

Adult unilateral moyamoya disease with intracranial aneurysm is frequently reported in the literature, but there is much variation in its treatment. In this case report, we describe the time course and treatment regimen of a patient with moyamoya disease and review the literature regarding moyamoya disease with intracranial aneurysm. A 64-year-old man had untreated intracranial aneurysm and unilateral moyamoya disease for 10 years. He presented with sudden-onset right hemiparesis and aphasia due to a subcortical hemorrhage. He was admitted to the local neurosurgical unit, and upon resolution of symptoms, he was admitted to our hospital. A cerebral angiogram revealed the champagne bottleneck sign of the left carotid artery and obliteration of the top of the left intracranial carotid artery with a moyamoya phenomenon. Two unruptured intracranial aneurysms were identified in the anterior communicating artery(Acom A) and the right intracranial carotid artery(C3). We performed superficial temporal artery-middle cerebral artery anastomosis followed by aneurysmal neck clipping of the Acom A aneurysm. Postoperative imaging showed no new ischemic damage and improved cerebral blood flow. Although the patient experienced temporal worsening of aphasia, his function recovered a few months later and he was able to resume his normal daily life activities. The combination of direct bypass surgery and aneurysmal neck clipping might be a therapeutic option for hemorrhagic unilateral moyamoya disease with unruptured intracranial aneurysm.

The Efficacy of Surgical Treatment for the Secondary Prevention of Stroke in Symptomatic Moyamoya Disease: A Meta-Analysis.

The treatment of moyamoya disease (MMD) is controversial and often depends on the doctor's experience. In addition, the choice of surgical procedure to treat MMD can differ in many ways. In this study, we performed a meta-analysis to determine whether surgical treatment of MMD is superior to conservative treatment and to provide evidence for the selection of an appropriate surgical treatment.The human case–control studies regarding the association of MMD treatment were systematically identified through online databases (PubMed, Web of Science, Elsevier Science Direct, and Springer Link). Inclusion and exclusion criteria were defined for the eligible studies. The fixed-effects model was performed when homogeneity was indicated. Alternatively, the random-effects model was utilized.This meta-analysis included 16 studies. Surgical treatment significantly reduced the risk of stroke (odds ratio (OR) of 0.17, 95% confidence interval (CI), 0.12–0.26, P < 0.01). A subgroup analysis showed that surgical treatment was more beneficial to hemorrhagic MMD (OR of 0.23, 95% CI, 0.15–0.38, P < 0.01), but there was no significant difference between surgical treatment and conservative treatment on ischemic MMD treatment (OR of 0.45, 95% CI, 0.15–1.29, P = 0.14). Further analysis indicated that compared to direct bypass surgery, indirect bypass surgery had a lower efficacy on secondary stroke risk reduction (OR of 1.79, 95% CI, 1.14–2.82, P = 0.01), while no significant difference was detected for perioperative complications.Surgery is an effective treatment for symptomatic MMD patients, and direct bypass surgery may bring more benefits for these patients.