Exploring the Influence of Dual Revascularization Techniques on Preoperative Middle Meningeal Artery Collateral Networks in Moyamoya Angiopathy

Introduction: Moyamoya disease is characterized by spontaneous and progressive occlusion of the intracranial carotid arteries and their most proximal branches. One of the current treatments involves a combined surgical revascularization technique: direct revascularization with a superficial temporal artery to middle cerebral artery (STA-MCA) bypass, along with indirect revascularization using encephaloduroarteriosynangiosis (EDAS). Despite some direct STA-MCA bypasses occluding over time, cerebral perfusion and clinical status surprisingly remain unaffected. Given that the middle meningeal artery (MMA) is a major branch of the external carotid artery (ECA), which could serve as a direct donor, we hypothesize that MMA collaterals compete with the direct bypass for flow, while overall cerebral perfusion remains largely unchanged.

Methods: This retrospective, single-center, single-surgeon case series included 36 eligible patients with ischemic Moyamoya disease who underwent exclusively a “combined” surgical revascularization. Preoperative and postoperative cerebral angiograms were analyzed for the presence of MMA collateral networks, and postoperative angiograms at long term were assessed for direct bypass patency. Pre- and postoperative NOVA-MRA data from 29 patients were examined. Total hemispheric blood flow was defined as the sum of ICA, ACA, MCA, and PCA flow in the respective hemisphere, with direct bypass flow added for postoperative measurements.

Results: All 36 patients who underwent combined revascularization had patent bypasses postoperatively. Cerebral angiography after 13-month (median follow-up) showed 24 (66.6%) direct bypasses remained robustly patent, while 12 were regressed. Preoperative MMA collaterals were identified in 12 patients (33.3%), increasing to 23 (64%) post-revascularization. In the patent bypass group, MMA collaterals were present in 54% of cases, compared with 83% in the diminished bypass group. Three patients suffered from minor strokes during the follow-up period: two patients with patent direct bypasses and MMA collaterals (6 and 13 weeks post-surgery) and one in a patient with occluded direct bypass (19 months postsurgery). Postoperative NOVA-MRA showed 9 patients with improved total hemispheric blood flow, while 20 worsened. Overall, postoperative total hemispheric blood flow decreased by an average of 36 mL/min among the 29 patients analyzed. Of the three patients with new strokes, only one had a reduced total hemispheric flow (−101 mL/min), while the other two showed increased flow (+33 mL/min and +65 mL/min).

Conclusion: Long-term regression of direct bypasses is associated with increased MMA collateral networks, suggesting that while direct bypasses immediately enhance cerebral perfusion, MMA collaterals restore cerebral perfusion in the long term, allowing for regression of the direct bypass in ⅓ of cases. This phenomenon is not associated with an increased stroke rate. NOVA data reveal chronic disease progression in Moyamoya patients with reduced postoperative hemispheric blood flow. MMA collaterals, although not robustly detected in NOVA analysis, may be crucial for asymptomatic patients despite worsened total hemispheric flow. Future NOVA protocols for Moyamoya patients should include ECA flow, as postoperative increases may reflect enhanced MMA collaterals.

Publication History

Article published online:
07 February 2025