Direct Bypass Surgery Vs. Combined Bypass Surgery for Hemorrhagic Moyamoya Disease: A Comparison of Angiographic Outcomes

Abstract

Objective: Extracranial-intracranial bypass is currently recognized as the optimal treatment for hemorrhagic-type moyamoya disease (MMD) which reduces incidence of rebleeding. Recent studies have reported the advantage of combined bypass over direct bypass for the general MMD patients. However, the effect of direct bypass and combined bypass surgery specifically for hemorrhagic-type MMD had not been investigated yet. Methods: Hemorrhagic-type MMD patients who underwent direct and combined bypass surgery with complete clinical and radiological documentation from a multicenter cohort between 2009 and 2017 were retrospectively included. Surgical methods included superficial temporal artery-middle cerebral artery (STA-MCA) anastomosis (direct bypass), combined STA-MCA bypass with encephalodurosynangiosis (EDS), and combined STA-MCA bypass with encephaloduroarteriosynangiosis (EDAS). Matsushima standard on follow-up catheter angiography was used to assess surgical outcome. Modified Rankin Scale, incidence of rebleeding and ischemia during follow-up were recorded. Rebleeding-free survival rates between direct and combined bypass were compared by Kaplan-Meier analysis. Results: Sixty eight hemorrhagic-onset MMD patients were included in this study, among which 71 hemispheres were treated with surgery (direct bypass: 17; bypass+EDS: 24; bypass+EDAS: 30). Forty six (64.8%) hemispheres had satisfactory revascularization (Matsushima level 2-3) and 26 (36.6%) had poor neoangiogenesis. Matsushima level was not significantly different between surgical groups (P = 0.258). Good neoangiogenesis from dural grafts was achieved in 26 (36.6%) hemispheres, and good neoangiogenesis from STA grafts was only seen in 4 (out of 30, 12.5%) hemispheres. Multivariate analysis showed bypass patency [P < 0.001, OR (95%CI): 13.41 (3.28-54.80)] and dural neoangiogenesis [P < 0.001, OR (95%CI): 13.18 (3.26-53.36)] both independently contributed to good angiographic outcome. During follow-up, incidences of rebleeding or ischemic events, and re-bleeding free survival rate were not significantly different between surgical groups (P = 0.433, P = 0.559, and P = 0.997). However, patients who underwent combined bypass surgery had significantly lower mRS at follow-up comparing to patients who underwent direct bypass (P = 0.006). Conclusion: Combined bypass surgery and direct bypass surgery offered similar revascularization for hemorrhagic MMD. Bypass patency and dural angiogenesis both contributed to revascularization independently. The potential of indirect bypass to grow new vessels in hemorrhagic-MMD patients was generally limited, but dural leaflets offered better neoangiogenesis than STA grafts and was therefore recommended for surgical revascularization of hemorrhagic MMD.

Keywords: angiographic outcome; combined bypass; direct bypass; hemorrhagic-type; moyamoya disease; surgical outcome; surgical revascularization.

Figure 1

Illustration of combined direct bypass and EDAS technique. Both branches of STA were exposed and separated. (A) Dura were cut in a radial fashion (black arrow). (B) Anterior branch of STA were anastomosed with M4-branch of MCA (black arrowhead). Posterior branch of STA was attached to cortical surface (white arrowhead). Dural leaflets were inverted underneath bone edge (black arrow).

Figure 2

Evaluation of STA-MCA bypass patency with DSA. (A) occluded: complete proximal occlusion of STA and disappearance of MCA branches; (B) stenosed: thin, stenosed STA with a few visible MCA branches; (C) patent: patent or dilated STA with patent or even dilated MCA branches (red triangles point to the anastomosis).

Figure 3

Evaluation of neoangiogenesis from dural grafts and STA grafts with DSA on a scale of three levels. “None”: completely no growth of new vessels; “Minimal': Few, localized new vessels; “Good”: Abundant new vessels covering considerable area and reaching deep into brain cortex. (A,B) Preoperative and follow-up DSA showed “none” dural neoangiogenesis and “none” STA neoangiogenesis. (C,D) Preoperative and follow-up DSA showed “minimal” neoangiogenesis from STA. (E,F) Preoperative and follow-up DSA showed “minimal” neoangiogenesis from dural grafts and “good” neoangiogenesis from STA grafts. (G,H) Preoperative and follow-up DSA showed “good” neoangiogenesis from dural grafts (red triangles point to the STA neoangiogenesis and black arrows point to dural neoangiogenesis).

Figure 4

Evaluation of AchA-PcoA dilation [by Liu et al. (29)]. (A) grade 0: normal AchA and PcoA without dilation. (B) grade 1: dilation of the AChA within the choroidal fissure and/or dilation of the PCoA without abnormally extensive branches. (C) grade 2: dilation and extension of the AChA beyond the choroidal fissure and/or dilation of the PCoA with abnormally extensive branches (posterior pericallosal arteries and/or leptomeningeal collateral vessels supplying the anterior cerebral circulation). (D) grade 3: disappearance of AChA-PCoA due to occlusion of ICA.

Figure 5

Kaplan-Meier plot showing freedom from rebleeding per hemisphere treated with direct and combined bypass surgery. Tick marks indicate time points after which data were censored for a particular patient-hemisphere in the group (point of last follow-up). No significant difference was found between the two surgical groups (P = 0.997, Log-Rank test).

Figure 6

Illustrated case 1. A 48-years-old male patient presented with intraventricular hemorrhage who underwent combined STA-MCA bypass and EDAS surgery. (A) Preoperative ICA angiography (Suzuki V). (B) Preoperative angiography showing STA and its branches. (C,D) Postoperative angiography showing satisfying revascularization. Direct bypass of anterior branch of STA to MCA was almost occluded (black arrow), with dural neoangiogenesis supplying MCA territory (white arrow). Little neoangiogenesis had grown from posterior branch of STA (black arrow head). (E–H) Preoperative CTP images, respectively showing increased time to peak (TTP), increased mean transit time (MTT), decreased cerebral blood flow (CBF), and decreased cerebral blood volume (CBV) on the right hemisphere. (I–L) Postoperative CTP showing improved TTP, MTT, CBF, CBV at left temporal region. This patient had improved symptoms during follow-up.

Figure 7

Illustrated case 2. A 50-years-old female patient presented with intraventricular hemorrhage (IVH) who underwent direct bypass surgery. (A,B) Preoperative DSA images showed Suzuki stage VI ICA and external carotid artery. (C,D) Postoperative DSA showed patent direct bypass supply most of MCA territory. Dural neoangiogenesis was very limited. This patient had a recurrent IVH during follow-up.