Won-Sang Cho

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.

Clinical course of untreated cerebral cavernous malformations: a meta-analysis of individual patient data

Summary Background Cerebral cavernous malformations (CCMs) can cause symptomatic intracranial haemorrhage (ICH), but the estimated risks are imprecise and predictors remain uncertain. We aimed to obtain precise estimates and predictors of the risk of ICH during untreated follow-up in an individual patient data meta-analysis. Methods We invited investigators of published cohorts of people aged at least 16 years, identified by a systematic review of Ovid MEDLINE and Embase from inception to April 30, 2015, to provide individual patient data on clinical course from CCM diagnosis until first CCM treatment or last available follow-up. We used survival analysis to estimate the 5-year risk of symptomatic ICH due to CCMs (primary outcome), multivariable Cox regression to identify baseline predictors of outcome, and random-effects models to pool estimates in a meta-analysis. Findings Among 1620 people in seven cohorts from six studies, 204 experienced ICH during 5197 person-years of follow-up (Kaplan-Meier estimated 5-year risk 15·8%, 95% CI 13·7–17·9). The primary outcome of ICH within 5 years of CCM diagnosis was associated with clinical presentation with ICH or new focal neurological deficit (FND) without brain imaging evidence of recent haemorrhage versus other modes of presentation (hazard ratio 5·6, 95% CI 3·2–9·7) and with brainstem CCM location versus other locations (4·4, 2·3–8·6), but age, sex, and CCM multiplicity did not add independent prognostic information. The 5-year estimated risk of ICH during untreated follow-up was 3·8% (95% CI 2·1–5·5) for 718 people with non-brainstem CCM presenting without ICH or FND, 8·0% (0·1–15·9) for 80 people with brainstem CCM presenting without ICH or FND, 18·4% (13·3–23·5) for 327 people with non-brainstem CCM presenting with ICH or FND, and 30·8% (26·3–35·2) for 495 people with brainstem CCM presenting with ICH or FND. Interpretation Mode of clinical presentation and CCM location are independently associated with ICH within 5 years of CCM diagnosis. These findings can inform decisions about CCM treatment. Funding UK Medical Research Council, Chief Scientist Office of the Scottish Government, and UK Stroke Association.

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.

Post-laminectomy kyphosis in patients with cervical ossification of the posterior longitudinal ligament : does it cause neurological deterioration?

OBJECTIVE Total laminectomy (TL) is an effective surgical technique for the treatment of cervical ossification of the posterior longitudinal ligament (OPLL) along multiple levels. However, kyphosis and probable neurological deterioration have been frequently reported after laminectomy. We analyzed the changes in the cervical curvature after TL and subsequent changes in neurological status. METHODS We retrospectively reviewed the records of 14 patients who underwent TL for the treatment of cervical OPLL between Jan. 1998 and Dec. 2003. TL was selected according to the previously determined criteria. The curvature of the cervical spine was visualized on a lateral cervical spine X-ray and measured using Ishiharas Curvature Index (CI) before the operation and at the last follow-up examination. Perioperative neurological status was estimated using the modified Japanese Orthopedic Association score and the Improvement Rate (IR) at the same time as the images were evaluated. RESULTS The mean age of the patients was 57 years, the male/female ratio was 10:4, and the mean follow-up period was 41 months. The mean number of OPLL was 4.9, and the mean number of operated levels was also 4.9. The CI decreased after TL (p=0.002), which was indicative of a kyphotic change. However, this kyphotic change showed no correlation with the length of the follow-up period, number of operated levels and preoperative CI. Neurological examination at the last follow-up showed an improved neurological status in all patients (p=0.001). There was no neurological deterioration in any case during the follow-up period. Moreover, there was no correlation between IR and the degree of kyphotic change. Postoperative complications, such as C5 radiculopathy and epidural bleeding, resolved spontaneously without neurological sequelae. CONCLUSION Kyphotic change was observed in all but one patient who underwent TL for the treatment of cervical OPLL. However, we did not find any contributing factors to kyphosis or evidence of postoperative neurological deterioration.

The effectiveness of 3T time-of-flight magnetic resonance angiography for follow-up evaluations after the stent-assisted coil embolization of cerebral aneurysms

Background Artifacts introduced by stents limit the value of magnetic resonance (MR) imaging as a follow-up modality after the stent-assisted coil embolization of cerebral aneurysms. Purpose To investigate the usefulness of 3 Tesla (3T) time-of-flight (TOF) MR angiography (MRA) for the follow-up evaluation. Material and Methods Twenty-two aneurysms of 20 patients treated with stent-assisted coil embolization were followed up with 3T TOF MRA and digital subtraction angiography (DSA) with three-dimensional rotational angiography (3DRA). The status of coiled aneurysms was compared with 3T TOF MRA and DSA with 3DRA in terms of complete occlusion, residual neck, and residual aneurysm. TOF MRA at 3T was performed 1 day before DSA with 3DRA, with a mean follow-up period of 20.1 ± 10.8 months. Results Twenty (90.9%) of 22 cases were concordant between the two modalities. The degree of agreement and correlation between them were high (κ = 0.771, P < 0.001; r = 0.832 and P < 0.001). When evaluating the status of residual neck, the sensitivity was 80% (4/5 cases); specificity was not available because there were no cases of complete occlusion. For the status of residual aneurysm, the sensitivity and specificity were 94.1% (16/17 cases) and 100% (all 5 cases), respectively. Conclusion TOF MRA at 3T with source images could be useful as a non-invasive follow-up modality after the stent-assisted coil embolization of cerebral aneurysms. Further study with a larger patient sample is needed to confirm the effectiveness of 3T TOF MRA.

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.

Clinical features and treatment outcomes of the spinal arteriovenous fistulas and malformations

OBJECT Spinal vascular diseases, such as spinal dural arteriovenous fistulas (DAVFs), perimedullary arteriovenous fistulas (AVFs), and spinal arteriovenous malformations (AVMs), are very rare. The authors analyzed the features and treatment outcomes of these conditions. METHODS Data from 64 patients were retrospectively reviewed. There were 33 spinal DAVFs (1 patient had 2 lesions), 20 perimedullary AVFs, and 12 spinal AVMs. Clinical features, radiological findings, treatment results, and clinical outcomes were evaluated according to the diseases, subtypes, and treatment modalities. The median duration of follow-up was 20, 42, and 56 months for spinal DAVFs, perimedullary AVFs, and spinal AVMs, respectively. RESULTS Spinal DAVFs showed faster progression of symptoms (median 5, 12, and 36 months for spinal DAVFs, perimedullary AVFs, and spinal AVMs, respectively) and worse neurological status at diagnosis (poor neurological status in 56%, 65%, and 33%, respectively). On MRI, signal voids were demonstrated in all except 1 spinal DAVF. At the last follow-up, 94% of spinal DAVFs, 68% of perimedullary AVFs, and 50% of spinal AVMs were completely obliterated. Favorable clinical outcomes were achieved in 91%, 95%, and 58%, respectively. In detail, the majority (78%) of spinal DAVFs were embolized, resulting in complete obliteration in 92% and favorable clinical outcomes in 92%. Most Type IVa and IVb perimedullary AVFs were surgically treated (71% and 88%), with complete obliterations of 86% and 71%, and favorable clinical outcomes in 100% and 86%, respectively. All Type IVc lesions were embolized with a low cure rate of 40%; however, clinical outcomes were satisfactory. Spinal AVMs were generally embolized (67%), and only glomus-type lesions attained a satisfactory cure rate (80%) and clinical outcome (100%). CONCLUSIONS Embolization produced satisfactory outcomes in spinal DAVFs and glomus-type spinal AVMs. Surgery is advantageous in Type IVa and IVb perimedullary AVFs. Palliative embolization can be effective in Type IVc perimedullary AVFs and juvenile spinal AVMs.

Endovascular Treatment of Ophthalmic Artery Aneurysms: Assessing Balloon Test Occlusion and Preservation of Vision in Coil Embolization

BACKGROUND AND PURPOSE: ICA–ophthalmic artery aneurysms have unique configurations corresponding to relative risks of ophthalmologic morbidities. Presented herein are clinical and radiologic outcomes of coil embolization in ophthalmic artery aneurysms. MATERIALS AND METHODS: From January 2003 to September 2013, endovascular coiling was performed in 43 consecutive patients with ophthalmic artery aneurysms, each classified by the degree to which the ophthalmic artery was incorporated by the aneurysm and the contiguity between the ophthalmic artery entry and parent ICA. Clinical and radiologic outcomes of this approach were investigated, including the technical aspects of treatment and the efficacy of balloon test occlusion. RESULTS: Among 14 patients (32.6%, all ophthalmic artery types) undergoing balloon test occlusion before endovascular coiling, patent collaterals between the external carotid artery and ophthalmic artery were demonstrated in 12 (85.7%) and complete compromise of the ophthalmic artery (without affecting vision) occurred in 4 patients during coiling. Steam-shaped S-configured (67.9%) or straight microcatheters (17.8%) facilitated aneurysm selection in most of the superiorly directed ophthalmic artery aneurysms (n = 28), and steam-shaped pigtail microcatheters (85.7%) were useful in medially directed aneurysms (n = 14). Balloon protection (n = 22) was generally used to facilitate coiling, or a stent (n = 9) was alternatively deployed. Satisfactory aneurysmal occlusion was achieved through coil embolization in 37 lesions (86.1%). During follow-up of 35 patients (mean interval, 12.9 ± 9.4 months), only 1 instance (2.9%) of major recanalization was observed. CONCLUSIONS: If one tailors technical strategies, ophthalmic artery aneurysms are amenable to safe and effective endovascular coil embolization, which tends to be stable in follow-up. Balloon test occlusion may be helpful in devising treatment strategies to preserve vision when coiling ophthalmic artery aneurysms (especially those incorporating an ophthalmic artery origin) is done.

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.