Jae Seung Bang

Long-Term Outcomes After Combined Revascularization Surgery in Adult Moyamoya Disease

Background and Purpose— The surgical outcomes of adult moyamoya disease are rarely reported. We aimed to evaluate the long-term outcomes of combined revascularization surgery in patients with adult moyamoya disease. Methods— Combined revascularization surgery consisting of superficial temporal artery–middle cerebral artery anastomosis with encephalodurogaleosynangiosis was performed on 77 hemispheres in 60 patients. Clinical, angiographic, and hemodynamic states were evaluated retrospectively using quantitative methods preoperatively and postoperatively in the short-term (≈6 months) and long-term (≈5 years) periods. The mean clinical follow-up duration was 71.0±10.1 months (range, 60–104 months). Results— Clinical status improved until 6 months after surgery and remained stable thereafter, as assessed by the Karnofsky Performance Scale and modified Rankin Scale. The revascularization area relative to supratentorial area significantly increased in the long-term period compared with that in the short-term period (54.8% versus 44.2%; P<0.001). Cerebral blood flow in the territory of the middle cerebral artery improved in the short-term period compared with that in the preoperative period (68.7 versus 59.1; considering blood flow of the pons as 50; P<0.001) and thereafter became stable (65.5 in the long term; P=0.219). The annual risks of symptomatic hemorrhage and infarction were 0.4% and 0.2%, respectively, in the operated hemispheres. Conclusions— Combined revascularization surgery resulted in satisfactory long-term improvement in clinical, angiographic, and hemodynamic states and prevention of recurrent stroke.

Quantitative angiographic comparison with the OSIRIS program between the direct and indirect revascularization modalities in adult moyamoya disease.

BACKGROUND Up-to-date, quantitative angiographic measurement of revascularization extent after bypass surgery has not been reported. OBJECTIVE To measure the extent of angiographic revascularization quantitatively 6 months postoperatively with the OSIRIS program (University Hospital of Geneva, version 3.1). METHODS A total of 75 bypass procedures were performed in 65 consecutive adult moyamoya disease patients, and 71 bypass surgeries in 61 adult moyamoya disease patients were studied 6 months postoperatively with angiography. We performed 5 different types of bypass surgeries: encephaloduroarteriosynangiosis (EDAS), superficial temporal artery-middle cerebral artery anastomosis (SMA), SMA with encephalomyosynangiosis (EMS), SMA with EDAS, and SMA with encephaloduroarteriomyosynangiosis (EDAMS). We also investigated single-photon emission computed tomography (SPECT) results after 6 months postoperatively and compared the angiographic revascularization extent with the SPECT results. RESULTS The mean values for the extent of revascularization among 5 different bypass surgeries were as follows: 32.4% for EDAS only, 57.4% for SMA only, 58.4% for SMA with EMS, 66.1% for SMA with EDAS, and 70.8% for SMA with EDAMS. There was a statistically significant difference in the extent of revascularization among the 5 surgical modalities (P = .000) and between the EDAS-only group and various SMA groups (P = .000). Statistical analysis between angiographic revascularization extent and SPECT results demonstrated significant statistical correlation (P = .000). CONCLUSION The extent of angiographic revascularization in adult moyamoya disease patients was highest in the SMA with EDAMS group and lowest in the EDAS-only group. In addition, angiographic revascularization extent was well correlated with the change in SPECT.

A retrieval thrombectomy technique with the Solitaire stent in a large cerebral artery occlusion

BackgroundTo describe preliminary experiences and the procedural details of retrieval thrombectomy using a self-expanding and fully retrievable Solitaire stent (ev 3 Inc., CA, USA) in acute ischemic stroke (AIS) patients with large artery occlusions.MethodsEight patients with AIS were treated by mechanical thrombectomy using a self-expanding, fully retrievable stent (Solitaire, ev 3 Inc., CA, USA). The stent was deployed to cover the whole intra-arterial clot and then it was slowly retrieved while occluding the internal cerebral artery (ICA) with a balloon guiding catheter. Additionally, continuous negative pressure was applied through the balloon guiding catheter with a specially designed gun device. Occlusion sites were M1 in six cases including one combined supraclinoid ICA occlusion and the other combined M2 occlusion, M2 in 1 case and one basilar artery top.ResultsComplete recanalization was achieved in all patients. Procedure time was 45 min or less in seven cases and 70 min in one case. Distal emboli occurred in one case in which the balloon guide catheter was not used. Only in this case was intraarterial fibrinolytics infusion necessary. There was no post-operative intracranial hemorrhage.ConclusionsIn our experience, retrieval thrombectomy with the Solitaire stent was a simple and effective method for reopening large cerebral arteries in AIS patients.

Moyamoya Disease: Treatment and Outcomes

Although the pathogenesis of moyamoya disease (MMD) has not been fully elucidated, the effectiveness of surgical revascularization in preventing stroke has been addressed by many studies. The main mechanism of surgical revascularization is augmenting the intracranial blood flow using an external carotid system by either direct bypass or pial synangiosis. This can improve resting cerebral blood flow as well as vascular reserve capacity. For direct revascularization, the superficial temporal artery is used as the donor artery in most cases, although the occipital artery may be used in limited cases. Usually, the cortical branch of the middle cerebral artery is selected as the recipient of direct anastomosis. As for indirect revascularization, various techniques using different kinds of connective tissues have been introduced. In some cases, reinforcing the anterior cerebral artery and the posterior cerebral artery territories can be considered. The effectiveness of surgical revascularization for preventing ischemic stroke had been generally accepted by many studies. However, for preventing hemorrhagic stroke, new evidence has been added by a recent randomized controlled trial. The incidence of peri-operative complications such as stroke and hyperperfusion syndrome seems to be high due to the nature of the disease and technical demands for treatment. Preventing and adequately managing these complications are essential for ensuring the benefits of surgery.

Stroke prevention by direct revascularization for patients with adult-onset moyamoya disease presenting with ischemia

OBJECT Moyamoya disease (MMD) is a progressive disease that can cause recurrent stroke. The authors undertook this retrospective case-control study with a large sample size in an attempt to assess the efficacy of direct or combined revascularization surgery for ischemia in adults with MMD. METHODS The authors investigated cases involving patients with moyamoya disease presenting with ischemia who visited Seoul National University Bundang Hospital and Seoul National University Hospital between 2000 and 2014. Among 441 eligible patients, 301 underwent revascularization surgery and 140 were treated conservatively. Variables evaluated included age at diagnosis, sex, surgical record, Suzuki stage, and occurrence of stroke. Patients were stratified into 2 groups based on whether or not they had undergone revascularization surgery. Actuarial 1-, 5-, and 10-year stroke rates were calculated using the life table method. Risk factor analysis for 5-year stroke occurrence was conducted with multivariate regression. RESULTS Of the 441 patients, 301 had been surgically treated (revascularization group) and 140 had not (control group). The mean follow-up durations were 45 and 77 months, respectively. The actuarial 10-year cumulative incidence rate for any kind of stroke was significantly lower in the revascularization group (9.4%) than in the control group (19.6%) (p = 0.041); the relative risk reduction (RRR) was also superior (52.0%) in the revascularization group, and the number needed to treat was 10. The 10-year rate of ischemic stroke was greater (13.3%) in the control group than in the revascularization group (3.9%) (p = 0.019). The RRR for ischemic stroke in the revascularization group was 70.7%, and the number needed to treat was 11. However, the actuarial 1- and 5-year rates of ischemic stroke did not significantly differently between the groups. Overall, revascularization surgery was shown to be an independent protective factor, as revealed by multivariate analysis. CONCLUSIONS Direct or combined revascularization for patients with adult-onset moyamoya disease presenting with ischemia can prevent further stroke.

Superficial Temporal Artery to Middle Cerebral Artery Bypass in Acute Ischemic Stroke and Stroke in Progress

BACKGROUND:Surgical reperfusion may be beneficial in patients with acute ischemic stroke who are ineligible for thrombolysis. OBJECTIVE:To evaluate the outcome of superficial temporal artery to middle cerebral artery (STA-MCA) bypass in acute stroke and stroke in progress. METHODS:The clinical and radiological data of 9 patients treated by STA-MCA bypass requiring urgent reperfusion but ineligible for intra-arterial thrombolysis (IAT) were reviewed. Pooled analysis was performed of published literature concerning STA-MCA bypass in acute stroke (21 cases in 2 articles). RESULTS:Of the 9 patients enrolled, symptom aggravation occurred during medical treatment in 4 patients and after IAT in 2. Three patients were ineligible for IAT despite being within 8 hours of symptom onset. Bypass significantly improved National Institutes of Health Stroke Scale scores (preoperatively, 12.4 ± 4.88; 3 days postoperatively, 8.6 ± 6.39, P = .046; discharge, 5.4 ± 5.15, P = .008; 3 mo postoperatively 3.7 ± 4.82, P = .008) without significant infarction growth by diffusion weighted imaging (preoperatively, 15.0 ± 8.87 mL; 7 days postoperatively, 15.2 ± 8.28 mL; P = .110). Abnormal perfusion regions (mean transit time >145% of contralateral side value) were reduced in all cases (2.63 ± 0.93 mL). Good outcomes (modified Rankin scale ≤2) were achieved by 6 patients. Pooled analysis with our patients showed a significant neurological improvement (P < .001) and a good outcome in 25 (83.3%) patients without hemorrhage or complication. CONCLUSION:STA-MCA bypass may be beneficial to patients with acute stroke or stroke in progress who are ineligible for IAT. Furthermore, it appears safe when the infarction is small. These findings indicate that STA-MCA bypass could be considered as a treatment option in selected patients with acute stroke or stroke in progress.

A retrospective analysis on the natural history of incidental small paraclinoid unruptured aneurysm

Objective The optimal consensus concerning treatment of incidental small paraclinoid unruptured intracranial aneurysms (UIAs) remains controversial. The aim of this retrospective study was to reveal the natural history of small paraclinoid UIAs with the goal of informing the treatment plan. Methods 524 patients harbouring 568 paraclinoid UIAs (≤5 mm) were retrospectively evaluated during the mean follow-up of 35.4 months. The aneurysms were divided into two groups with respect to arterial branch: related (ophthalmic and superior hypophyseal artery), and non-related. Medical records were reviewed concerning multiple variables, such as sex, age, hypertension (HTN), diabetes mellitus, smoking and aneurysmal factors (size, arterial relationship, multiplicity and the occurrence of rupture and growth). The cumulative risk and the risk factors of aneurysmal rupture and growth were analysed. Results Two aneurysmal (0.35%) ruptures and 17 growths (3.0%) were observed during the follow-up of 1675.5 aneurysm-years with an annual rupture of 0.12% and an annual growth of 1.01%. The cumulative survival without aneurysmal growth reached a significant difference in aneurysms ≥4 mm (p=0.001), HTN (p=0.002), and arterial branch-related location (p=0.001). Multivariate analysis disclosed that aneurysm ≥4 mm (HR, 4.41; p=0.003), HTN (HR, 5.74; p=0.003), arterial branch-related location (HR, 6.04; p=0.002), and multiplicity (HR, 0.27; p=0.042) were significant predictive factors for aneurysm growth. Conclusions Although incidental small paraclinoid UIAs have a relatively lower rupture and growth risk, patients with high-risk factors, including aneurysm ≥4 mm, HTN, arterial branch-related aneurysms, and multiple aneurysms must be monitored closely. The limitation of the retrospective nature of this study should be taken into consideration.

The natural clinical course of hemodynamically stable adult moyamoya disease.

OBJECT Moyamoya disease (MMD) is a rare cerebrovascular disease and its natural history is still unclear. The authors aimed to investigate the natural course of hemodynamically stable cases of adult MMD, with the analysis of stroke risk factors. METHODS Two hundred forty-one patients were included in this retrospective study. One hundred sixty-six (68.9%) were female, and mean age (± SD) at first visit was 41.3 ± 12.0 years (range 18-69 years). Unilateral involvement was identified in 33 patients, and 19 patients (7.9%) had a family history of MMD. According to the clinical presentations, patients were classified into hemorrhagic (n = 62, 25.7%), ischemic (n = 144, 59.8%), and asymptomatic (n = 35, 14.5%) groups. The mean duration of follow-up was 82.5 ± 62.9 months (range 7.3-347.0 months). RESULTS The annual stroke risk was 4.5%, and the annual risks of rebleeding in the hemorrhagic group and recurrent ischemic events in the ischemic group were 4.3% and 3.0%, respectively. There was no significant difference in cumulative stroke risk between the 3 groups (p = 0.461). Risk factors included thyroid disease for overall strokes (HR 2.56, 95% CI 1.16-5.67), initial hemorrhagic presentation for hemorrhagic strokes (HR 2.53, 95% CI 1.24-5.17), and initial ischemic presentation for ischemic strokes (HR 2.69, 95% CI 1.15-6.27). Familial MMD was a common risk factor for all types of stroke. Among the 3 clinical groups, the hemorrhagic group showed the worst clinical status at discharge and at most recent follow-up. Twenty-three patients (9.5%) eventually underwent revascularization surgery. CONCLUSIONS There was no statistically significant difference in the incidence of stroke in the different clinical groups; clinical status, however, was most severe in patients with hemorrhagic presentation. In patients who experienced stroke during the follow-up period, the stroke type tended to correspond to their initial presentation. Close follow-up is needed in patients with thyroid disease and a family history of MMD.

Epidemiology of Moyamoya Disease in Korea: Based on National Health Insurance Service Data

There have been a few studies reporting the epidemiology of moyamoya disease in Korea. Previous studies revealed relatively high prevalence and incidence of moyamoya disease in Korea and Japan. This study was designed to provide the latest epidemiologic information of moyamoya disease in Korea. We analyzed a database comprising of 50 million people covered in Korea by the National Health Insurance Service to calculate the prevalence. The incidence was estimated by eliminating the duplicated records of previous 3 years. We summarized the prevalence and incidence according to age, sex, and local distribution. In addition, the chronological changes were demonstrated with direct standardization using the 2010 population structure information. The standardized prevalence was 6.5 per 100000 persons in 2005, which was increased to 18.1 in 2013. In the same period, standardized incidence was increased from 2.7 to 4.3 per 100000 persons. The prevalence for men was 4.9 and 8.3 for women in 2005. In 2013, the prevalence had increased for men and women to 13.8 and 25.3, respectively. The incidence for men and women was 2.2 and 3.2, respectively, in 2005. It had increased to 3.5 and 5.7, respectively. The mean age of patients was 33.5 in 2005 and increased to 42.5 in 2013. The peak prevalent age group had shifted slightly to the older age groups, with chronologically consistent female predominance. The prevalence was highest in Jeollabuk province and lowest in Ulsan city.

Expression of cellular retinoic acid-binding protein-I (CRABP-I) in the cerebrospinal fluid of adult onset moyamoya disease and its association with clinical presentation and postoperative haemodynamic change

Objective The elevation of cellular retinoic acid-binding protein-I (CRABP-I) has been suggested as a candidate in the pathogenesis of paediatric moyamoya disease (MMD). However, few studies have addressed CRABP-I in adult onset MMD. The aim of this study was to examine the expression of CRABP-I in the cerebrospinal fluid (CSF) of adult onset MMD, and to evaluate its association with clinical presentation and postoperative haemodynamic change. Methods This study examined the CSF from 103 patients: bilateral MMD, n=58 (56.3%); unilateral MMD, n=19 (18.4%); atherosclerotic cerebrovascular disease (ACVD), n=21 (20.4%); and control group, n=5 (4.9%). The intensity of CRABP-I was confirmed by western blotting and expressed as the median (25th–75th percentile). The differences in CRABP-I expression according to disease entity (unilateral MMD vs bilateral MMD vs ACVD), initial presenting symptoms (haemorrhage vs ischaemia) and postoperative haemodynamic change (vascular reserve in single photon emission CT and basal collateral vessels in digital subtraction angiography) were analysed. Results CRABP-I intensities in bilateral MMD (1.45(0.86–2.52)) were significantly higher than in unilateral MMD (0.91(0.78–1.20)) (p=0.044) or ACVD (0.85(0.66–1.11)) (p=0.004). No significant differences were noted based on the initial presenting symptoms (p=0.687). CRABP-I was not associated with improvement in vascular reserve (p=0.327), but with decrease in basal collateral vessels (p=0.023) postoperatively. Conclusions Higher CRABP-I in the CSF can be associated with typical bilateral MMD pathogenesis in adults. Additionally, postoperative basal collateral change may be related to the degree of CRABP-I expression.