Long-term Outcomes After Encephaloduroarteriosynangiosis in Adult Patients with Moyamoya Disease Presenting with Ischemia

doi:10.1016/j.wneu.2018.04.076

World Neurosurgery

Volume 115, July 2018, Pages e482-e489

https://doi.org/10.1016/j.wneu.2018.04.076 Get rights and content

Highlights

•
In adult moyamoya disease (MMD), controversy remains regarding the effectiveness of revascularization surgeries given the lack of randomized studies comparing the efficacy of surgical techniques.
•
There is ongoing controversy regarding the most appropriate surgical treatment for adult patients with MMD.
•
We report the clinical outcomes in a Chinese adult cohort with MMD following encephaloduroarteriosynangiosis and demonstrate the long-term efficacy of this indirect procedure in reducing rates of ischemic events and hemorrhages in adult patients with MMD presenting with ischemia.

Background

In adult Moyamoya disease (MMD), there remains controversy about the effectiveness of revascularization surgeries because randomized studies have not been performed to compare the efficacy of surgical techniques. This study was conducted to assess the most appropriate surgical treatment for adult patients with MMD.

Methods

Encephaloduroarteriosynangiosis (EDAS) was performed on 247 hemispheres in 145 patients. The clinical and demographic characteristics of patients were obtained via retrospective chart review. Clinical and angiographic states were evaluated retrospectively using quantitative methods. The mean duration of clinical follow up was 141.4 ± 19.5 months.

Results

A total of 247 EDAS procedures were performed in 145 patients, including 15 EDAS performed using the occipital artery as the donor vessel. The mortality rate was 0%, and the permanent morbidity rates were 1.2% per operation and 2.0% per person. The mean modified Rankin Scale score was 1.21 ± 1.31 postoperatively and 1.01 ± 1.39 at the last follow-up. Of the 109 hemispheres studied, 45% were classified as grade A, 34% as grade B, and 21% as grade C collateral circulation. The annual rates of stroke were calculated to be 0.73% per person-year. Overall, the 1-,5-, and 10-year actuarial stroke rates were 2.1±1.2%, 6.8±2.1%, and 8.9±2.4%, respectively. Bilateral involvement was a common significant factor in any, hemorrhagic, and ischemic strokes. Hypertension was a risk factor for ischemic strokes during follow-up.

Conclusions

EDAS is an effective procedure in a Chinese cohort of patients with MMD. EDAS resulted in satisfactory long-term improvement of clinical states and prevention of recurrent strokes.

Introduction

Moyamoya disease (MMD) is an idiopathic and progressively occlusive disease of the bilateral internal carotid arteries that presents characteristic abnormal vascular networks and afflicts patients worldwide.1, 2 Although the etiology of MMD remains unclear, recent studies have identified a genetic susceptibility factor,3, 4 the RNF213 gene, that may partially explain why the highest MMD incidence rates occur in East Asian countries, including Japan, Korea, China, and Taiwan.1, 2, 5, 6, 7, 8

Recent guidelines for the treatment of MMD published in Japan recommend surgical revascularization for MMD that manifest cerebral ischemic symptoms.⁹ Indirect revascularization surgeries, such as encephaloduroarteriosynangiosis (EDAS) and other variants, are generally accepted as standard treatment for pediatric MMD.10, 11, 12, 13, 14 In adult MMD, however, there remains controversy about the effectiveness of revascularization surgeries because randomized studies have not been performed to compare the efficacy of surgical techniques, and the retrospective studies that have been conducted implicate various age ranges, small numbers of patients, short-term follow-up, and no standardization of surgical techniques.12, 13, 15, 17, 18, 19, 20, 21, 22 In this study, we report the clinical outcomes in a Chinese adult cohort with MMD following EDAS and demonstrate the long-term efficacy of this indirect procedure in reducing rates of ischemic events and hemorrhages in adult patients with MMD presenting with ischemia.

Section snippets

Patient Selection

We searched our electronic medical record archive to identify eligible patients who were seen at 307th Hospital of People's Liberation Army, between December 2002 and June 2007. Medical data were collected prospectively according to our protocol and reviewed retrospectively under approval by the Research Ethics Board of 307th Hospital of People's Liberation Army. Because this is a retrospective follow-up study, patients consent is not required. All patients who met the following criteria were

Clinicoradiologic Outcomes

The mean mRS scores at the initial and last follow-up period were 1.21 ± 1.31 and 1.01 ± 1.39, respectively, a statistically significant difference (t = 2.38; P = 0.019) (Figure 1). Clinical status continued to improve postoperatively and stabilized 6 months after surgery until the last follow-up. Comparing the clinical states of 145 patients between preoperative and last follow-up periods, 132 patients (91.0%) improved, 5 (3.4%) were unchanged, and 8 (5.5%) worsened. A significant reduction in

Discussion

At present, there is great interest in understanding the optimal surgical management for adult MMD. In a Japanese adult population of 16 patients, Mizoi et al.¹² posited that direct bypass procedures were the treatment of choice, because indirect bypass did not result in sufficient collateral vessel formation to functionally improve cerebral blood flow. Recently, Gross et al.²⁶ demonstrated in a North American adult cohort that revascularization via direct bypass (29 patients) significantly

Conclusions

EDAS proved to be an effective procedure in our cohort of Chinese patients with MMD, resulting in satisfactory long-term improvement of clinical states and prevention of recurrent strokes. Larger, randomized clinical studies with longer follow-up will be critical in further defining the natural history of adult MMD and in elucidating the optimal medical and surgical treatments.

References (54)

W. Miao et al.
Epidemiological and clinical features of Moyamoya disease in Nanjing, China
Clin Neurol Neurosurg
(2010)
K. Mizoi et al.
Indirect revascularization for moyamoya disease: is there a beneficial effect for adult patients?
Surg Neurol
(1996)
H. Nakashima et al.
Long-term results of surgically treated moyamoya disease
Clin Neurol Neurosurg
(1997)
D.S. Kim et al.
Combined direct anastomosis and encephaloduroarteriogaleosynangiosis using inverted superficial temporal artery-galeal flap and superficial temporal artery-galeal pedicle in adult moyamoya disease
Surg Neurol
(2006)
M. Fujimura et al.
Incidence and risk factors for symptomatic cerebral hyperperfusion after superficial temporal artery-middle cerebral artery anastomosis in patients with moyamoya disease
Surg Neurol
(2009)
K. Ueki et al.
Moyamoya disease: the disorder and surgical treatment
Mayo Clin Proc
(1994)
K. Fujii et al.
The efficacy of bypass surgery for the patients with hemorrhagic moyamoya disease
Clin Neurol Neurosurg
(1997)
H.J. Noh et al.
Long term outcome and predictors of ischemic stroke recurrence in adult moyamoya disease
J Neurol Sci
(2015)
Q. Zhang et al.
Clinical features and long-term outcomes of unilateral moyamoya disease
World Neurosurg
(2016)
N. Hirotsune et al.
Long-term follow-up study of patients with unilateral moyamoya disease
Clin Neurol Neurosurg
(1997)

Y. Goto et al.

Worldwide distribution of moyamoya disease

Neurol Med Chir (Tokyo)

(1992)

R.M. Scott et al.

Moyamoya disease and moyamoya syndrome

N Engl J Med

(2009)

F. Kamada et al.

A genome-wide association study identifies RNF213 as the first Moyamoya disease gene

J Hum Genet

(2011)

S. Miyatake et al.

Homozygous c.14576G>A variant of RNF213 predicts early-onset and severe form of moyamoya disease

Neurology

(2012)

T. Baba et al.

Novel epidemiological features of moyamoya disease

J Neurol Neurosurg Psychiatry

(2008)

D. Chiu et al.

Clinical features of moyamoya disease in the United States

Stroke

(1998)

L. Duan et al.

Moyamoya disease in China: its clinical features and outcomes

Stroke

(2012)

N. Hashimoto et al.

Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis)

Neurol Med Chir (Tokyo)

(2012)

X.Y. Bao et al.

Clinical features, surgical treatment, and long-term outcome in pediatric patients with moyamoya disease in China

Cerebrovasc Dis

(2015)

S.K. Kim et al.

Pediatric moyamoya disease: an analysis of 410 consecutive cases

Ann Neurol

(2010)

R.M. Scott et al.

Long-term outcome in children with moyamoya syndrome after cranial revascularization by pial synangiosis

J Neurosurg Pediatr

(2004)

J.S. Bang et al.

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

Neurosurgery

(2012)

X.Y. Bao et al.

Clinical features, surgical treatment and long-term outcome in adult patients with Moyamoya disease in China

Cerebrovasc Dis

(2012)

D.H. Han et al.

Moyamoya disease in adults: characteristics of clinical presentation and outcome after encephalo-duro-arterio-synangiosis

Clin Neurol Neurosurg

(1997)

K. Kazumata et al.

The frequency of postoperative stroke in moyamoya disease following combined revascularization: a single-university series and systematic review

J Neurosurg

(2014)

X. Liu et al.

Long term outcome after conservative and surgical treatment of haemorrhagic moyamoya disease

J Neurol Neurosurg Psychiatry

(2013)

R.M. Starke et al.

Clinical features, surgical treatment, and long-term outcome in adult patients with moyamoya disease. Clinical article

J Neurosurg

(2009)

Cited by (22)

Encephalo-Duro-Pericranio-Synangiosis for the Treatment of Moyamoya Disease with Posterior Cerebral Artery Lesions
2023, World Neurosurgery
We describe our experience performing encephalo-duro-pericranio synangiosis for the parieto-occipital region (EDPS-p) as a treatment for moyamoya disease (MMD) with hemodynamic disturbances caused by lesions of the posterior cerebral artery.
From 2004 to 2020, 60 hemispheres of 50 patients with MMD (38/50 females, age 1–55 years) underwent EDPS-p as a treatment for hemodynamic disturbances in the parieto-occipital region. A skin incision was made on the parieto-occipital area to avoid the major skin arteries, and the pedicle flap was created by attaching the pericranium to the dura mater under the craniotomy with multiple small incisions. The surgical outcome was assessed on the basis of the following points: perioperative complications, postoperative improvement of clinical symptoms, subsequent novel ischemic events, qualitative assessment of the development of collateral vessels by magnetic resonance arteriography, quantitative assessment of postoperative perfusion improvement based on the mean transit time, and cerebral blood volume on dynamic susceptibility contrast imaging.
Perioperative infarction occurred in 7/60 hemispheres (11.7%). The transient ischemic symptoms observed preoperatively disappeared in 39/41 hemispheres (95.1%) during the follow-up period (12–187 months), and none of the patients experienced novel ischemic events. Collateral vessels supplied from the occipital arteries, middle meningeal arteries, and posterior auricular arteries developed postoperatively in 56/60 hemispheres (93.3%). Postoperative mean transit time and cerebral blood volume showed significant improvement in the occipital, parietal, and temporal areas (P < 0.001), as well as the frontal area (P = 0.01).
EDPS-p seems to be an effective surgical treatment for patients with MMD who suffer hemodynamic disturbances caused by posterior cerebral artery lesions.
Postoperative vascular event prediction using angiography and ultrasonography in patients with Moyamoya disease
2022, Journal of the Neurological Sciences
Indirect revascularization surgery reduce the risk of recurrent vascular events in patients with moyamoya disease (MMD), but the roles of postoperative angiography and ultrasonography in predicting these events remain unclear.
This prospective study enrolled patients with MMD who would undergo their first unilateral indirect revascularization surgery. They received preoperative and postoperative ultrasound examination at 1, 3, and 6 months and conventional cerebral angiography. On ultrasonography, postoperative emerging flow (PEF) in an intracranial artery was defined as emerging flow postoperatively with absence of flow preoperatively. Predictors of vascular event frequency reduction were identified from angiographic and ultrasonographic parameters.
In total, 52 patients (including 24 pediatric and 24 male patients), who underwent 52 preoperative and 82 postoperative ultrasound examinations, were enrolled. Significant postoperative changes were noted in all the ultrasonographic parameters of ipsilateral superficial temporal artery (STA) and the end-diastolic velocity and flow volume in contralateral STA. During a median follow-up of 5.3 years, indirect revascularization surgery significantly reduced the occurrence of ipsilateral vascular events. Predictors of vascular event frequency reduction included Matsushima grade A or B on the ipsilateral side on angiography (odds ratio [OR] = 22.00, P = 0.002) and lower resistance index (RI) in ipsilateral STA (OR = 0.0001, P = 0.012) but no PEF pattern in ipsilateral middle cerebral artery (OR = 0.14, P = 0.029) on ultrasonography performed within 6 months.
Reduction of long-term vascular event frequency probably can be predicted through postoperative angiography and ultrasonography within 6 months after indirect revascularization surgery.
Long-term outcomes of moyamoya disease following indirect revascularization in middle adulthood: A prospective, quantitative study
2022, Journal of the Formosan Medical Association
Citation Excerpt :
Thus, indirect revascularization can be considered for adult moyamoya patients in selected condition. Though increasing studies have reported the effectiveness of indirect revascularization in adult moyamoya patients,4–14 patient's age is always considered a factor limiting its use in adult patients. The effectiveness of indirect revascularization for moyamoya patients in middle adulthood has never been prospectively studied.
Our previous study demonstrated that indirect revascularization is effective in the treatment of adult moyamoya patients. This prospective study aims to evaluate the long-term effectiveness of indirect revascularization in moyamoya patients in middle adulthood.
From January 2013 to June 2019, moyamoya patients more than 40 years of age underwent indirect revascularizations were studied. The hypoperfusion area of brains was revascularized. The cerebral angiography and time-to-peak (TTP) scoring (ranged 0–14) of the magnetic resonance perfusion study were used to evaluate the revascularization effect.
During the study period, 50 consecutive adult moyamoya patients underwent indirect revascularization. Seventeen patients (27 cerebral hemispheres) more than 40 years of age were included. The mean age was 47.9 ± 6.4 years, and 13 patients were female. The pre-operative Suzuki stages were I, II, III, IV, V, and VI in 1, 1, 9, 13, 0, and 3 hemispheres, respectively. After a mean follow-up period of 52.5 ± 20.6 months, all patients had improvement or stabilization of their clinical conditions. Available post-operative angiography demonstrated Matsushima grading A in 18 of 20 hemispheres. The mean TTP score of all 27 hemispheres improved from 5.0 ± 3.3 pre-operatively to 12.0 ± 2.1 after surgery (p < 0.001). The post-operative mean TTP score of the 7 hemispheres without angiographic follow-up was 10.4 ± 1.8. One patient had persistent mild motor weakness after 56-month follow-up. Transient complications with full recovery occurred in 3 patients.
Indirect revascularization is a safe method with satisfactory long-term results in moyamoya patient in middle adulthood.
Combined STA-MCA Bypass and Encephalodurosynangiosis Versus Encephalodurosynangiosis Alone in Adult Hemorrhagic Moyamoya Disease: A 5 -Year Outcome Study
2020, Journal of Stroke and Cerebrovascular Diseases
Citation Excerpt :
This finding was supported later by the Japan Adult Moyamoya trial, providing evidence that the risk of rebleeding in adult patients can be reduced by direct bypass surgery.5 Studies by Bao et al6,15 also showed that a satisfactory long-term improvement of clinical states and prevention of recurrent stroke is achieved after EDAS. However, both the ischemic and hemorrhagic type were included in their patient population.
Aim: The purpose of this study was to compare the 5-year prognosis of combined superficial temporal artery- middle cerebral artery (STA-MCA) bypass and Encephalodurosynangiosis (EDAS) and EDAS alone in hemorrhagic moyamoya disease (MMD). Methods: This study included 123 adult patients admitted to Beijing Tiantan Hospital with hemorrhagic MMD between 2010 and 2015. The surgical procedures included combined revascularization of STA-MCA anastomosis with EDAS (n = 79) or EDAS alone (n = 44). We recorded basic demographic data as well as several risks factors, and used multivariate regression analysis to evaluate the predictive factor of overall survival and rebleeding-free survival. Results: Of the 123 patients with hemorrhagic MMD, the mean age was 37.97 ± 11.04 years old and the mean follow-up period was 65.9 months (ranging from 12 to 100 months). A total of 21 rebleeding events occurred in 19 patients, yielding an annual incidence of rebleeding of 3.1%. Of the 19 patients with rebleeding, 11 (57.8%) patients died of rebleeding and one patient experience 3 rebleeding events. In the combined revascularization group, 9 (11.3%) patients experienced rebleeding, of which 5 (6.3%) died. This incidence was lower than in the indirect group, where 22.7% of patients experienced rebleeding events and 13.6% died. However, no significant difference was found between these 2 groups. In Kaplan-Meier survival analysis, the combined revascularization group had a better prognosis than the EDAS alone group, and multivariate regression analysis revealed that the combined revascularization procedure was associated with a better outcome. Conclusions: Both combined revascularization and EDAS alone can reduce the risk of rebleeding in hemorrhagic MMD. Combined revascularization was found to be superior to EDAS alone in terms of preventing rebleeding events.
Isolated anterior cerebral artery occlusion: an atypical form of moyamoya disease
2024, Stroke and Vascular Neurology
Chinese expert consensus on the treatment of MMD
2023, Chinese Neurosurgical Journal

View all citing articles on Scopus

: This study was supported by the National Nature Science Foundation of China (Grant 81571136) and the Beijing Municipal Science and Technology Commission (Grant Z171100001017144). The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

: Xiang-Yang Bao, Yong Zhang, and Qian-Nan Wang contributed equally to this work and should be considered co–first authors.

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Original ArticleLong-term Outcomes After Encephaloduroarteriosynangiosis in Adult Patients with Moyamoya Disease Presenting with Ischemia

Highlights

Background

Methods

Results

Conclusions

Introduction

Section snippets

Patient Selection

Clinicoradiologic Outcomes

Discussion

Conclusions

Clin Neurol Neurosurg

Surg Neurol

Clin Neurol Neurosurg

Surg Neurol

Surg Neurol

Mayo Clin Proc

Clin Neurol Neurosurg

J Neurol Sci

World Neurosurg

Clin Neurol Neurosurg

Worldwide distribution of moyamoya disease

Neurol Med Chir (Tokyo)

Moyamoya disease and moyamoya syndrome

N Engl J Med

A genome-wide association study identifies RNF213 as the first Moyamoya disease gene

J Hum Genet

Homozygous c.14576G>A variant of RNF213 predicts early-onset and severe form of moyamoya disease

Neurology

Novel epidemiological features of moyamoya disease

J Neurol Neurosurg Psychiatry

Clinical features of moyamoya disease in the United States

Stroke

Moyamoya disease in China: its clinical features and outcomes

Stroke

Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis)

Neurol Med Chir (Tokyo)

Clinical features, surgical treatment, and long-term outcome in pediatric patients with moyamoya disease in China

Cerebrovasc Dis

Pediatric moyamoya disease: an analysis of 410 consecutive cases

Ann Neurol

Long-term outcome in children with moyamoya syndrome after cranial revascularization by pial synangiosis

J Neurosurg Pediatr

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

Neurosurgery

Clinical features, surgical treatment and long-term outcome in adult patients with Moyamoya disease in China

Cerebrovasc Dis

Moyamoya disease in adults: characteristics of clinical presentation and outcome after encephalo-duro-arterio-synangiosis

Clin Neurol Neurosurg

The frequency of postoperative stroke in moyamoya disease following combined revascularization: a single-university series and systematic review

J Neurosurg

Long term outcome after conservative and surgical treatment of haemorrhagic moyamoya disease

J Neurol Neurosurg Psychiatry

Clinical features, surgical treatment, and long-term outcome in adult patients with moyamoya disease. Clinical article

J Neurosurg

Original Article
Long-term Outcomes After Encephaloduroarteriosynangiosis in Adult Patients with Moyamoya Disease Presenting with Ischemia