Direct, Indirect, and Combined Extracranial-to-Intracranial Bypass for Adult Moyamoya Disease: An Updated Systematic Review and Meta-Analysis

Abstract

BACKGROUND: Moyamoya disease is a chronic, progressive cerebrovascular disease involving occlusion or stenosis of the terminal portion of the internal carotid artery. We conducted an updated systematic review and meta-analysis to investigate clinical and angiographic outcomes comparing direct, combined, and indirect bypass for the treatment of moyamoya disease in adults. METHODS: Two independent authors performed Preferred Reporting Items for Systematic reviews and Meta-Analyses guided literature searches in December 2021 to identify articles reporting clinical/angiographic outcomes in adult moyamoya disease patients undergoing bypass. Primary end points used were ischemic and hemorrhagic strokes, clinical outcomes, and angiographic revascularization. Study quality was evaluated with Newcastle-Ottawa and the Oxford Center for Evidence-Based Medicine scales. RESULTS: Four thousand four hundred fifty seven articles were identified in the initial search; 143 articles were analyzed. There were 3827 direct, 3826 indirect, and 3801 combined bypasses. Average length of follow-up was 3.59±2.93 years. Pooled analysis significantly favored direct (odds ratio [OR], 0.62 [0.48–0.79]; P <0.0001; OR, 0.44 [0.32–0.59]; P <0.0001; OR, 0.56 [0.42–0.74]; P <0.0001; OR, 3.1 [2.5–3.8]; P =0.0001) and combined (OR, 0.53 [0.41–0.69]; P <0.0001; OR, 0.28 [0.2–0.41]; P <0.0001; OR, 0.41 [0.3–0.56]; P <0.0001; OR, 3.1 [2.8–4.3]; P =0.0001) over indirect bypass for early stroke, late stroke, late intracerebral hemorrhage, and favorable outcomes, respectively. Indirect bypass was favored over combined (OR, 3.1 [1.7–5.6]; P <0.0001) and direct (OR, 4.12 [2.34–7.25]; P <0.0001) for early intracerebral hemorrhage. The meta-analysis significantly favored direct (OR, 0.37 [0.23–0.60]; P <0.001; OR, 0.49 [0.31–0.77]; P =0.002) and combined (OR, 0.23 [0.12–0.43]; P <0.00001; OR, 0.30 [0.18–0.49]; P <0.00001) bypass over indirect bypass for late stroke and late hemorrhage, respectively. Combined bypass was favored over indirect bypass for favorable outcomes (OR, 2.06 [1.18–3.58]; P =0.01). CONCLUSIONS: Based on combined meta-analysis (43 articles) and pooled analysis (143 articles), the existing literature indicates that combined and direct bypasses have significant benefits for patients suffering from late stroke and hemorrhage versus indirect bypass. Combined bypass was favored over indirect bypass for favorable outcomes. This is a strong recommendation based on low-quality evidence when utilizing the Grades of Recommendation, Assessment, Development, and Evaluation system. These findings have important implications for bypass strategy selection.

Indirect revascularization vs. non-surgical treatment for Moyamoya disease and Moyamoya syndrome: A comparative effectiveness study

“…But it's important to note that this study also had a high rate of bypass occlusion (10%). Another meta-analysis noted that although both direct bypass and combined bypass were superior to indirect bypass in the treatment of early stroke, late stroke and late intracerebral hemorrhage, indirect bypass was significantly superior to both direct and combined bypass in the treatment of early intracerebral hemorrhage ( 23 ). Sam et al ( 24 ) evaluated the improvement of cerebral blood flow in MMD and steno-occlusive disease patients before and after cerebrovascular revascularization by blood-oxygen-level-dependent cerebrovascular reactivity MRI and computerized prospective targeting of CO 2 , and they found that unilateral revascularization not only reversed gray matter thinning and cognitive loss in the affected hemisphere but also significantly improved in the unaffected hemisphere, however, this study included both direct and indirect bypass surgery, so it cannot be directly stated which surgery method is more effective.…”

Adult Moyamoya Disease and Syndrome: Current Perspectives and Future Directions: A Scientific Statement From the American Heart Association/American Stroke Association

“…90,91 There is a lack of randomized data regarding revascularization strategy in ischemic moyamoya. Most metaanalyses 70,73,74,[92][93][94] and their source studies have several limitations, including nonrandomized allocation of treatment, heterogeneity in age and clinical presentation of cohorts, unblinded outcome assessment, variable length of follow-up, and redundancy in the included cohorts. Although some data may suggest that the direct bypass or combined approach has advantages over the indirect approach for stroke prevention 73,74,[92][93][94] and angiographic outcomes, 70,73,92,93 without differences in perioperative complications, 70,73,74 such studies have major limitations, and no strong conclusions can be made.…”

Surgical revascularizations for pediatric moyamoya: a systematic review, meta-analysis, and meta-regression analysis

“…In a recent meta-analysis comparing the three bypass techniques in adults, Nguyen et al [69] found that DB/CB conferred benefits in terms of late stroke recurrence versus IB, with no dissimilarities in terms of perioperative outcomes. Notably, while cerebral hyperperfusion is an undesirable complication of DB in adult patients, this phenomenon is much less frequently observed in pediatric patients and so the conclusions of this study should not constitute a reason to avoid DB in children.…”