Patient Data
This study was approved by the Ethics Committee of Beijing Tiantan Hospital, Capital Medical University. All consecutive inpatients with MMD at Beijing Tiantan Hospital, Capital Medical University from January 2010 through December 2018 were screened. The inclusion criteria were as follows:1) patients diagnosed with MMD based on DSA according to published guidelines set by the Research Committee on MMD in Japan [9]; 2) patients who initially presented with intracranial hemorrhage confirmed by CT scan; 3) patients who received only indirect bypass; and 4) patients who received postoperative DSA after surgical revascularization. The exclusion criteria included moyamoya syndrome caused by neurofibromatosis, Down syndrome, meningitis, and cranial irradiation [1]. Therefore, 64 patients (64 hemispheres) were included (Fig. 1). Information on the analysis variables, including age at operation, sex, history of risk factors, hypertension, smoking, alcohol use, hyperlipidemia, thyroid disease diabetes, types of hemorrhage, modified Rankin Scale (mRS), and surgical modalities, was collected at study onset.
Radiologic profiles
The preoperative radiologic profiles, including the site of hemorrhage, collateral circulation ,and the stages of the pre-stroke period were determined by two independent neurosurgeons who were blinded to clinical information. The site of hemorrhage was based on the classification criteria established by Takahashi et al [10]. An anterior hemorrhage is defined as being located in the putamen, caudate head, frontal lobe, anterior half of the temporal lobe, subependymal area of the anterior part of the lateral ventricle, or anterior half of the corpus callosum. A posterior hemorrhage is defined as being located in the thalamus, posterior half of the temporal lobe, parietal lobe, occipital lobe, subependymal area of the posterior part of the lateral ventricle including the atrium, or posterior half of the corpus callosum.
Collateral circulation was evaluated based on the classification criteria by Liu et al [11]. Posterior collateral circulation was evaluated as follows, based on lateral views of vertebrobasilar artery angiograms, the leptomeningeal collateral networks from the posterior cerebral artery (PCA) territory to the anterior cerebral artery (ACA) territory:1) 1 point: blood supply to the cortical border zone between the ACA and PCA territory; 2) 2 points: blood supply over the central sulcus via the posterior pericallosal artery. On the anteroposterior view vertebrobasilar artery angiograms, the leptomeningeal collateral networks from the PCA territory to the middle cerebral artery (MCA) territory: 1) 1 point: the anastomoses of the anterior temporal branches of the PCA and MCA or the parietooccipital PCA anastomoses to MCA; 2) points: blood supply extended into the sylvian fissure;3) 3 points: blood supply extended into the occlusion within the M1 or proximal M2 segments. Anterior collateral circulation was evaluated by using the Suzuki stage [12], and scores of 6 to 0 corresponded to Suzuki stages 0 to 6. The grading score was obtained based on the sum of the anterior and posterior collateral circulation and the stages of collateral circulation were made as follows: Grade I, a score of 0 to 4; Grade II, a score of 5 to 8; and Grade III, a score of 9 to12.
The cerebral hemodynamic status was assessed by computed tomography perfusion. The stages of pre-stroke period were evaluated as follows [13]: Stage I, time to peak (TTP) was delayed, mean transit time (MTT), regional cerebral blood flow (rCBF), and regional cerebral blood volume (rCBV) were normal; Stage II, TTP and MTT were delayed, rCBF was normal, and rCBV was normal or slightly increased; Stage III, TTP and MTT were delayed, rCBF was decreased, and rCBV was normal or slightly decreased; Stage IV, TTP and MTT were delayed, rCBF and rCBV were decreased.
Postoperative Collateral Formation
Direct or combined bypass is the first choice for the treatment of hemorrhagic MMD in our centre. However, direct bypass is difficult in young pediatric patients or adult patients with advanced MMD due to the small caliber of the recipient artery. Indirect bypass was performed unless there were inadequate recipient or donor artery grafts [14], and encephaloduroarteriosynangiosis (EDAS) was the prioritized technique. For patients with no available donor vessels, multiple burr hole (MBH) or encephalodurogaleo(periosteal)synangiosis (EDGS) was performed [15]. For EDAS, the branch of the superficial temporal artery (STA) and the surrounding galea connective tissue were placed on the brain surface after being dissected free, and EDGS was performed as a variant of EDAS. For MBH, five to fifteen burr holes were drilled over the hypoperfusion brain area; the dura was opened and separated. Postoperative collateral formation was evaluated by using the Matsushima scale on lateral views of external carotid angiograms [16]: A, more than 2/3 of the MCA distribution; B, between 2/3 and 1/3 of the MCA distribution; and C, slight or none (Fig. 2). The evaluations were carried out by two independent neurosurgeons who were not involved in the surgical procedures and who were blinded to the clinical information.
Statistical Analysis
The statistical analyses were performed using SPSS (Windows version 22.0, IBM). AnA or B score on the Matsushima scale was defined as good postoperative collateral formation, and a C score on the Matsushima was defined as poor postoperative collateral formation. A logistic regression analysis was performed to test which variables were associated with postoperative collateral formation. Clinical variables that achieved p< 0.10 in the univariate analysis were included in the multivariate analysis. A probability value < 0.05 was defined as statistical significance.