Original ArticleChronologic Evaluation of Cerebral Hemodynamics by Dynamic Susceptibility Contrast Magnetic Resonance Imaging After Indirect Bypass Surgery for Moyamoya Disease
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
References (39)
- et al.
Effectiveness of burr holes for indirect revascularization in patients with moyamoya disease–a review of the literature
World Neurosurg
(2014) - et al.
Reliability of mean transit time obtained using perfusion-weighted MR imaging; comparison with positron emission tomography
Magn Reson Imaging
(2003) - et al.
Validation of the CBF, CBV, and MTT values by perfusion MRI in chronic occlusive cerebrovascular disease: a comparison with 15O-PET
Acad Radiol
(2004) - et al.
Ultrasonographic changes after indirect revascularization surgery in pediatric patients with moyamoya disease
Ultrasound Med Biol
(2016) - et al.
Insights on the revascularization mechanism for treatment of Moyamoya disease based on the histopathologic concept of angiogenesis and arteriogenesis
World Neurosurg
(2011) - et al.
Indirect revascularization for moyamoya disease: is there a beneficial effect for adult patients?
Surg Neurol
(1996) - et al.
Cerebrovascular “moyamoya” disease. Disease showing abnormal net-like vessels in base of brain
Arch Neurol
(1969) - et al.
Moyamoya disease–a review
Stroke
(1983) - et al.
Severe haemodynamic stress in selected subtypes of patients with moyamoya disease: a positron emission tomography study
J Neurol Neurosurg Psychiatry
(2005) - et al.
Surgically induced angiogenesis to compensate for hemodynamic cerebral ischemia
Stroke
(1994)
Direct versus indirect revascularization procedures for moyamoya disease: a comparative effectiveness study
J Neurosurg
Long-term follow-up of surgically treated juvenile patients with Moyamoya disease
J Neurosurg Pediatr
Clinical features, surgical treatment, and long-term outcome in adult patients with moyamoya disease. Clinical article
J Neurosurg
Practical clinical use of dynamic susceptibility contrast magnetic resonance imaging for the surgical treatment of moyamoya disease
Neurosurgery
Neovascularization (angiogenesis) after revascularization in moyamoya disease. Which technique is most useful for moyamoya disease?
Acta Neurochir (Wien)
Effects of surgical revascularization on outcome of patients with pediatric moyamoya disease
Stroke
Risk factors for neurologic deterioration after revascularization surgery in patients with moyamoya disease
Anesth Analg
How does angiogenesis develop in pediatric moyamoya disease after surgery? A prospective study with MR angiography
Childs Nerv Syst
Assessment of regional cerebral blood flow by dynamic susceptibility contrast MRI using different deconvolution techniques
Magn Reson Med
Cited by (26)
Imaging Pattern and the Mechanisms of Postoperative Infarction After Indirect Revascularization in Patients with Moyamoya Disease
2021, World NeurosurgeryCitation Excerpt :In all patients, an antiplatelet agent was administered 2 days after surgery; we mainly prescribed aspirin, but in some cases, we continued the same antiplatelet drugs (cilostazol or clopidogrel) that the patient took before surgery. Because indirect bypass surgery requires time to improve cerebral hemodynamic impairment, antiplatelet agents were used for several months after surgery until improvement in cerebral hemodynamics was confirmed by perfusion-weighted MRI.19 Anticoagulative agents, such as intravenous heparin, were rarely used and reserved only for some patients with progressive infarction and severe hemodynamic disturbances and those requiring additional treatment for the postoperative infarction.
Cerebral Hyperperfusion Syndrome After Revascularization Surgery in Patients with Moyamoya Disease: Systematic Review and Meta-Analysis
2020, World NeurosurgeryCitation Excerpt :In recent years, more methods such as indocyanine green videography, fluid-attenuated inversion recovery images, positron emission tomography, multi-inversion time arterial spin labeling, and technetium 99m hexamethylpropyleneamine oxime have been reported to be used in clinical examination of CBF after MMD.57-62 Moreover, some studies have proposed other indicators trying to replace CBF to indicate the cerebral perfusion status after surgery, such as cerebrovascular reactivity value and mean transit time.63-65 However, the effectiveness of these methods and indicators still needs more investigation.
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.