Elsevier

World Neurosurgery

Volume 108, December 2017, Pages 427-435
World Neurosurgery

Original Article
Chronologic Evaluation of Cerebral Hemodynamics by Dynamic Susceptibility Contrast Magnetic Resonance Imaging After Indirect Bypass Surgery for Moyamoya Disease

https://doi.org/10.1016/j.wneu.2017.09.001Get rights and content

Objective

Although indirect bypass surgery is an effective treatment option for patients with ischemic-onset moyamoya disease (MMD), the time point after surgery at which the patient's hemodynamic status starts to improve and the time point at which the improvement reaches a maximum have not been known. The objective of the present study is to evaluate the hemodynamic status time course after indirect bypass surgery for MMD, using dynamic susceptibility contrast–magnetic resonance imaging (DSC-MRI).

Methods

We retrospectively analyzed the cases of 25 patients with MMD (37 sides; mean age, 14.7 years; range, 3–36 years) who underwent indirect bypass surgery and repeated DSC-MRI measurement within 6 months after the operation. The difference in the mean transit time (MTT) between the target regions and the control region (cerebellum) was termed the MTT delay, and we measured the MTT delay's chronologic changes after surgery.

Results

The postoperative MTT delay was 1.81 ± 1.16 seconds within 1 week after surgery, 1.57 ± 1.01 at weeks 1–2, 1.55 ± 0.68 at weeks 2–4, 1.32 ± 0.68 at months 1–2, 0.95 ± 0.32 at months 2–3, and 0.77 ± 0.33 at months 3–6. Compared with the preoperative value (2.11 ± 0.98 seconds), the MTT delay decreased significantly from 2 to 4 weeks after surgery (P < 0.05).

Conclusions

The amelioration of cerebral hemodynamics by indirect bypass surgery began soon after surgery and gradually reached a maximum at 3 months after surgery. DSC-MRI detected small changes in hemodynamic improvement, which are suspected to be caused by the initiation of angiogenesis and arteriogenesis in the early postoperative period.

Introduction

Moyamoya disease (MMD) is a progressive occlusive cerebrovascular arteriopathy characterized by bilateral stenosis of the terminal portion of the internal carotid arteries and development of a compensatory dilatation of the collateral vessels known as moyamoya vessels.1, 2 Patients with MMD show a variety of clinical presentations such as hemorrhage, infarction, and transient ischemic attack. The hemodynamic state varies depending on the type of presentation.3

Indirect bypass surgery was developed as a specific treatment option for ischemic-onset MMD.4, 5, 6, 7, 8 This surgery can less invasively achieve an amelioration of the hemodynamic deficiency of MMD in both children and adults if the surgical indication is confirmed by a reliable radiologic technique.9 One of the drawbacks of indirect bypass surgery is that it takes a long time before the amelioration of hemodynamics is achieved, unlike direct bypass surgery.10, 11, 12 For example, when magnetic resonance angiography was used to analyze the development of collateral vessels after direct and indirect bypass surgeries, it took approximately 3 months before collateral vessels were detected from indirect bypass surgery.13 However, to our knowledge, the time course of the improvement in the cerebral hemodynamics of patients with moyamoya after indirect bypass surgery has not been investigated. Therefore, accurate chronologic data that show when the hemodynamic condition starts to improve and when it reaches the maximum have not been made available.

Dynamic susceptibility contrast–magnetic resonance imaging (DSC-MRI) shows several cerebral hemodynamic parameters, and the reliability of these parameters has been validated.14, 15, 16, 17, 18, 19, 20 The investigators of a study that compared the parameters acquired by DSC-MRI with those acquired by positron emission tomography (PET) in patients with MMD concluded that a DSC-MRI–measured delay in the mean transit time (MTT), with reference to the cerebellum as a control, is a highly sensitive and specific parameter for the detection of an abnormally increased regional oxygen extraction fraction (OEF), as measured by PET.21

Our objective in the present study was to clarify the time course of cerebral hemodynamic changes induced by the development of surgically induced collateral circulation after indirect bypass surgery in patients with MMD. The changes of cerebral hemodynamics were measured using repeated sessions of DSC-MRI after the bypass surgery.

Section snippets

Patients

The ethics committee of our institution granted ethics approval of this retrospective study and waived written informed consent. A total of 57 patients with MMD underwent indirect bypass surgery at our department in the approximately 4-year period from April 2005 to March 2009. The surgical techniques included encephaloduroarteriosynangiosis (EDAS), encephaloduroperiosteum synangiosis (EDPS), and multiple cranial burr-hole surgeries, either singly or in combination. We determined the surgical

Clinical Outcome of the Patients

The preoperative ischemic events disappeared in 22 patients (88%) by 1 year after surgery. The preoperative ischemic events were ameliorated, but still present, in 3 patients (12%) after surgery. Perioperative infarction occurred in 1 patient (4% of patients, 2.7% of operations) within 1 week after surgery (Table 1).

Correlation Between the Anterior MTT Delay and Postoperative Days

The relationship between the anterior MTT delay and the interval (days) from the operation was plotted (Figure 2A). The anterior MTT delay began to decrease gradually soon after the

Discussion

We examined the time course of postoperative cerebral hemodynamic changes after indirect bypass surgery for MMD. DSC-MRI was used to measure the MTT, and it provided several novel findings. First, we observed that hemodynamic changes in patients with MMD who underwent indirect bypass surgery began soon after the surgery, gradually progressed, and continued for approximately 3 months, rather than progressing rapidly over a particular period. Second, in the rolandic and parietal areas where

Conclusions

Our findings indicate that the amelioration of cerebral hemodynamics in patients with MMD who underwent indirect bypass surgery began as early as 2–4 weeks postoperatively, with gradual improvement occurring for approximately 3 months thereafter, in contrast to the conventional wisdom that it may take 3–4 months until angiographically detectable collateral flow develops after indirect bypass surgery. In light of previous reports and the present results, we suggest that the DSC-MRI method can

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    Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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