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Won-Sang Cho, Young Seob Chung, Jeong Eun Kim, Jin Pyeong Jeon, Young Je Son, Jae Seung Bang, Hyun-Seung Kang, Chul-Ho Sohn and Chang Wan Oh

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.

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Young-Hoon Kim, Young Jin Lee, Jung Ho Han, Soyeon Ahn, Jaebong Lee, Jae Hyoung Kim, Byung Se Choi, Jae Seung Bang, Chae-Yong Kim, Gyojun Hwang, O-Ki Kwon and Chang Wan Oh

OBJECT

The authors aimed to assess whether the prevalence of intracranial aneurysms in patients with intracranial meningiomas was higher than that in a healthy population.

METHODS

The authors performed a hospital-based case-control study of 300 patients with newly diagnosed intracranial meningiomas and 900 age- and sex-matched controls without a history of brain tumors to evaluate any associations between intracranial aneurysms and intracranial meningiomas. Unconditional multivariate logistic regression models were used for case-control comparisons.

RESULTS

Intracranial aneurysms were identified in 23 patients (7.7%) and 24 controls (2.7%; p < 0.001). There was a significant association between intracranial aneurysms and intracranial meningiomas (OR 2.913, 95% CI 1.613–5.261) and hypertension (OR 1.905, 95% CI 1.053–3.446). In a subgroup analysis of the patients with newly diagnosed intracranial meningiomas, there was a significant association between intracranial aneurysms and hypertension (OR 2.876, 95% CI 1.125–7.352) and tumor volume (OR 1.012, 95% CI 1.001–1.024). These patients were also more likely than controls to have other intracranial vascular diseases (p < 0.001), such as isolated occlusion of the intracranial vessels, excluding intracranial aneurysms.

CONCLUSIONS

The prevalence of intracranial aneurysms was higher in patients with intracranial meningiomas. Hypertension and tumor volume appear to be associated with the formation of intracranial aneurysms in these patients.

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Jin Pyeong Jeon, Jeong Eun Kim, Jun Hyong Ahn, Won-Sang Cho, Young Dae Cho, Young-Je Son, Jae Seung Bang, Hyun-Seung Kang, Chul-Ho Sohn, Hyun-Tai Chung, Chang Wan Oh and Dong Gyu Kim

OBJECT

Treatment strategies for venous-predominant arteriovenous malformation (vp-AVM) remain unclear due to the limited number of cases and a lack of long-term outcomes. The purpose of this study was to report the authors’ experience with treatment outcomes with a review of the pertinent literature in patients with vp-AVM.

METHODS

Medical and radiological data from 1998 to 2011 were retrospectively evaluated. The degree of the arteriovenous (AV) shunt was categorized into 2 groups, a high- and low-flow AV shunt based on the angiographic findings.

RESULTS

Sixteen patients with a mean age of 45.3 years (range 16–78 years) and a mean follow-up of 79.9 months (range 25–264 months) were examined. Symptomatic lesions were noted in 13 patients: intracranial hemorrhage (ICH) in 9, seizure in 1, and headache in 3. A high-flow shunt was observed on angiography in 13 patients. Among these 13 patients, 12 patients were symptomatic. Nine patients presenting with ICH underwent hematoma removal with additional Gamma Knife surgery (GKS; n = 4), GKS only (n = 2), or conservative treatment (n = 3). The 3 asymptomatic patients received conservative treatment, and 1 rebleeding episode was observed. Seven of 8 patients who underwent GKS as an initial or secondary treatment modality experienced a marked reduction in the AV shunt on follow-up angiography, but complete obliteration was not observed.

CONCLUSIONS

Poor lesion localization makes a vp-AVM challenging to treat. Symptomatic patients with a high-flow shunt are supposedly best treated with GKS, despite the fact that only 87.5% of the vp-AVMs treated this way showed a reduction in the malformation volume, and none were cured.

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Ji Hoon Phi, Jung Won Choi, Moon-Woo Seong, Tackeun Kim, Youn Joo Moon, Joongyub Lee, Eun Jung Koh, Seul Ki Ryu, Tae Hee Kang, Jae Seung Bang, Chang Wan Oh, Sung Sup Park, Ji Yeoun Lee, Kyu-Chang Wang and Seung-Ki Kim

OBJECTIVE

In a minority of patients with neurofibromatosis Type 1 (NF-1), cerebral vasculopathy reminiscent of moyamoya disease develops. This phenomenon is called moyamoya syndrome (MMS), but there are no known risk factors for the prediction of MMS in NF-1 patients. Polymorphism of the RNF213 gene has exhibited strong associations with familial and sporadic moyamoya disease and other cerebral vasculopathies. The aim of this study is to find whether the RNF213 c.14576G>A variant is associated with MMS development in the NF-1 population or not.

METHODS

The MMS group included 16 NF-1 patients with documented MMS. The control group consisted of 97 NF-1 patients without MMS. Genomic DNA samples were obtained from the saliva or blood of both groups, and the presence of the RNF213 c.14576G>A variant was assessed by Sanger sequencing.

RESULTS

In the MMS group, 3 patients had the RNF213 c.14576G>A variant (18.7%), whereas no patients with this genetic variation were observed in the control group (0%). There was a meaningful association between the RNF213 c.14576G>A variant and MMS development (p = 0.0024). The crude odds ratio was calculated as 50.57 (95% CI 1.57–1624.41). All 3 patients with MMS and the c.14576G>A variant were diagnosed with MMS at an early age and had bilateral involvement.

CONCLUSIONS

The RNF213 c.14576G>A variant is more common in NF-1 patients who develop MMS than in NF-1 patients without MMS. This variant might be a susceptibility gene for the NF-1–moyamoya connection.

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Tackeun Kim, Chang Wan Oh, O-Ki Kwon, Gyojun Hwang, Jeong Eun Kim, Hyun-Seung Kang, Won-Sang Cho and Jae Seung Bang

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.

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Jin Pyeong Jeon, Jeong Eun Kim, Won-Sang Cho, Jae Seung Bang, Young-Je Son and Chang Wan Oh

OBJECTIVE

The purpose of this study was to evaluate treatment outcomes of future stroke prevention, perioperative complications, and angiographic revascularization in adults with symptomatic moyamoya disease (MMD) according to treatment modalities and surgical techniques.

METHODS

A systemic literature review was performed based on searches of the PubMed, Embase, and Cochrane Central databases. A fixed-effects model was used in cases of heterogeneity less than 50%. Publication bias was determined by Begg’s funnel plot, Egger’s test of the intercept, and the Begg and Mazumdar rank correlation test.

RESULTS

Eleven articles were included in the meta-analysis. Bypass surgery significantly decreased the future stroke events compared with conservative treatments in adult MMD (odds ratio [OR] 0.301, p < 0.001). Direct bypass showed better future stroke prevention than indirect bypass (OR 0.494, p = 0.028). There was no meaningful difference in perioperative complications between direct and indirect bypass (OR 0.665, p = 0.176). Direct bypass was associated with better angiographic outcomes than indirect bypass (OR 6.832, p < 0.001).

CONCLUSIONS

Bypass surgery can be effective in preventing future stoke events in adults with MMD. Direct bypass seems to provide better risk reduction with respect to stroke than indirect bypass in these patients.

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Brian P. Walcott, Jae Seung Bang, Omar Choudhri, Sirin Gandhi, Halima Tabani, Arnau Benet and Michael T. Lawton

A 46-year-old male presented with an incidentally discovered left ventricular body arteriovenous malformation (AVM). It measured 2 cm in diameter and had drainage via an atrial vein into the internal cerebral vein (Spetzler-Martin Grade III, Supplementary Grade 4). Preoperative embolization of the posterior medial choroidal artery reduced nidus size by 50%. Subsequently, he underwent a right-sided craniotomy for a contralateral transcallosal approach to resect the AVM. This case demonstrates strategic circumferential disconnection of feeding arteries (FAs) to the nidus, the use of aneurysm clips to control large FAs, and the use of dynamic retraction and importance of a generous callosotomy. Postoperatively, he was neurologically intact, and angiogram confirmed complete resection.

The video can be found here: https://youtu.be/j0778LfS3MI.

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Tackeun Kim, O-Ki Kwon, Jae Seung Bang, Heeyoung Lee, Jeong Eun Kim, Hyun-Seung Kang, Won-Sang Cho and Chang Wan Oh

OBJECTIVE

Brain arteriovenous malformation (BAVM) is a rare cerebrovascular disease that causes intracranial hemorrhage. Although several reports have demonstrated the epidemiological features of BAVM in Western countries, no epidemiological investigations regarding BAVM have been reported in Korea. The authors aimed to investigate the national epidemiology of ruptured BAVM in a Korean population.

METHODS

The authors used data from the National Health Insurance Service–National Sample Cohort (NHIS-NSC). The original cohort included approximately 1 million individuals (2% of the Korean population) with 12-year claim data (2002–2013). To construct an initial cohort for investigation, the authors selected 1,016,820 registered individuals in 2005. Subjects with a history of cerebrovascular disease (code I6xx) and BAVM (Q282) between 2002 and 2004 were washed-out to identify incident cases. During the 9-year follow-up (2005–2013), the incidence of BAVM was calculated using the earliest date of diagnosis of ruptured or unruptured BAVM. Direct standardization was applied to the crude incidence. Mortality and disability were evaluated using registration data. Related diagnostic procedures were also analyzed.

RESULTS

A total of 8,802,696 person-years of observation were noted. During observation, 308 patients were diagnosed with a ruptured BAVM. The crude incidence of ruptured BAVM was 3.5 per 100,000 person-years. There was no sex difference in incidence. The mortality rate for patients with a ruptured BAVM 1 month after diagnosis was 12.7%. At 1-year and 5-year follow-up examinations, mortality rates were 17.2% and 22.1%, respectively. Severe disability–free survival rates of patients with ruptured AVMs were 75.3% and 69.8% at 1-year and 5-year follow-up, respectively.

CONCLUSIONS

The standardized incidence of ruptured BAVMs was 3.6 per 100,000 person-years in Korea. Ruptured BAVMs resulted in high mortality and disability rates.