Quantitative Angiographic Hemodynamic Evaluation After Revascularization Surgery for Moyamoya Disease

Abstract

The corresponding hemodynamic changes of the internal carotid artery (ICA) after the revascularization surgery for moyamoya disease (MMD) remain unclear. The aim of this study was to analyze the hemodynamic changes of the ipsilateral ICA after the combined direct and indirect extracranial-intracranial (EC-IC) bypass. MMD patients undergoing combined EC-IC bypass were retrospectively reviewed. The mean transit time (MTT) of ICA was evaluated by color-coding angiography before revascularization and at follow-up. The MTT defined as the blood transit time between the end of cervical portion (C1) and the C7 segment of ICA. The clinical prognosis was assessed with Matsushima grading system, moyamoya vessel reduction system, and modified Rankin Scale (mRS). The correlation between hemodynamic parameter and prognosis was analyzed. Subgroup analysis was conducted between different presentations and different ages. Fifty-one patients were identified and the mean imaging follow-up interval was 5.5 months. The ICA-MTT was increased after the combined revascularization (P < 0.001) compared with contralateral ICA. Faster preoperative ICA-MTT was significantly associated with improved mRS in the ischemic group (P = 0.05). The increased ICA-MTT was significantly associated with favorable neoangiogenesis (P = 0.04), moyamoya vessel reduction (> 50%) (P = 0.023), and improved mRS score (P = 0.008). In subgroup analysis, the correlation in the ischemic subgroup and adult subgroup remained significant. In this cohort, the ICA-MTT increased after the combined EC-IC bypass, and there was a positive correlation between the increased blood transit time and favorable outcomes. Color-coding DSA proved to be useful as a quantitative and serial method to monitor postoperative courses after revascularization in MMD.

Keywords: Combined bypass; Hemodynamic change; Internal carotid artery; Moyamoya disease; Vessel remodeling.

Fig. 1

Color-coding digital subtraction angiography (DSA) for moyamoya disease (MMD) (sagittal position) and the measurement principle of hemodynamic parameter. Internal carotid artery-mean transit time (ICA-MTT) was defined as the difference of the region of interest (ROI) peak time intensity between the end of ICA C1 (Ref region, red line) and the C7 segment after the anterior choroidal artery originated from the ICA (No.2 region, green line) (a). Time-density curve showing MTT (b)

Fig. 2

Comparison of internal carotid artery-mean transit time (ICA-MTT) before the operation and follow-up: The ICA-MTT was significantly increased after surgery (a); In subgroup analysis, the prolongation was still existed in both the hemorrhagic and the ischemic group (b, c); The ΔICA-MTT in the hemorrhagic group also has no significant differences with the ischemic group (d). *P value indicates statistical significance

Fig. 3

The correlation between ΔICA-MTT and angiographic and clinical outcomes in the overall study population and subgroup: Longer ΔICA-MTT was associated with better neoangiogenesis (Matsushima grade A), more moyamoya vessel diminishment (grade 1), and improved mRS scores in the overall study population (a, b, c). This correlation remained obvious in the ischemic group (d, e, f). *P value indicates statistical significance (P < 0.05)

Fig. 4

Preoperative digital subtraction angiography (DSA) of the left hemisphere showed Suzuki stage III moyamoya disease (MMD) and large amount of moyamoya vessels (a). Cerebral blood flow (CBF) of computed tomography perfusion (CTP) showed poor perfusion in the left middle cerebral artery (MCA) territories, especially in the left frontal lobe (b). The preoperative blood flow in the internal carotid artery (ICA) was fast, and the ICA-MTT was 0 s (c, d). Six months later, the moyamoya vessels of the left hemisphere were significantly reduced (a vs e). Good angiogenesis was observed and evaluated as Matsushima grade A (anastomotic site: red arrow) (f). The postoperative blood flow in the ICA was significantly prolonged to 1.34 s (g, h)