Recognition of the Effect of Indirect Revascularization for Moyamoya Disease: The Balance Between the Stage Progression and Neoangiogenesis

Xiang-Yang Bao; Qian-Nan Wang; Xiao-Peng Wang; Ri-Miao Yang; Zheng-Xing Zou; Qian Zhang; De-Sheng Li; Lian Duan

doi:10.3389/fneur.2022.861187

Recognition of the Effect of Indirect Revascularization for Moyamoya Disease: The Balance Between the Stage Progression and Neoangiogenesis

Front Neurol. 2022 May 6:13:861187. doi: 10.3389/fneur.2022.861187. eCollection 2022.

Authors

Xiang-Yang Bao¹, Qian-Nan Wang², Xiao-Peng Wang^{1

3}, Ri-Miao Yang¹, Zheng-Xing Zou¹, Qian Zhang¹, De-Sheng Li¹, Lian Duan^{1

3}

Affiliations

¹ Department of Neurosurgery, Chinese PLA General Hospital (Former Department of Neurosurgery, The Fifth Medical Center of Chinese PLA General Hospital), Beijing, China.
² Department of Neurosurgery, Chinese PLA General Hospital (Former Department of Neurosurgery, The Eighth Medical Center of Chinese PLA General Hospital), Beijing, China.
³ Department of Neurosurgery, 307th Hospital of People's Liberation Army, 307 Clinical College, Anhui Medical University, Hefei, China.

Abstract

Objective: To explore the long-term progression of neoangiogenesis after indirect revascularization for moyamoya disease (MMD).

Methods: We enrolled patients who were diagnosed with MMD and treated by encephaloduroarteriosynangiosis (EDAS) surgery at our center from December 2002 through September 2009. A comparative study between short-term (6-12 months) and long-term (duration ≥ 8 years) follow-up angiographies was performed. The development of collateral circulation through EDAS was graded according to the system described by the Matsushima grade system.

Results: A total of 78 patients who received indirect EDAS were enrolled in the study. The mean age at the first operation was 26.9 ± 15.0 years. The Matsushima grades of the same hemisphere were higher at the long-term follow-up compared with the short-term follow-up. Importantly, no attenuation was observed in any hemisphere during the long-term follow-up. In total, 51 hemispheres (32.7%) and 26 hemispheres (16.6%) had progression during the short-term and the long-term follow-up, respectively. The ipsilateral Suzuki stage showed a significant negative correlation with progression pace. Furthermore, higher Suzuki stages were significantly correlated with the postsurgical Matsushima grade at both time points. A total of nine strokes (11.5%) occurred in 78 patients was reported at the long-term follow-up. The annual incidence rate of recurrent strokes was higher for the stage progression group than for the stable group.

Conclusion: For patients with MMD, postsurgical neoangiogenesis after indirect bypass continuously improved with time. The short-term progression of the internal carotid artery (ICA) might be attributed to cerebral revascularization, while the long-term progression should be attributed to the natural progression of the disease.

Keywords: Matsushima grade; encephaloduroarteriosynangiosis; long-term; moyamoya; neoangiogenesis.