Surgical Techniques in Moyamoya Vasculopathy. Peter Vajkoczy

Chapter 2. General Principles of Direct Bypass Surgery

Marcus Czabanka and Peter Vajkoczy


Bypass surgery for treating moyamoya vasculopathy (MMV) is often regarded as treatment of choice. In contrast to extraintracranial bypass surgery in atherosclerotic disease, different revascularization techniques are proposed for the treatment of MMV which may be differentiated into direct, indirect, and combined bypass procedures. The superiority of direct bypass surgery in comparison to indirect strategies includes immediate additional blood flow to the ischemic brain leading to reduction of stroke risk in these patients. The following chapter focuses on the general principles of bypass surgery for the treatment of MMV, focusing on general ideas and surgical concepts which are important for indication and planning of the surgical strategy.

Keywords: chronic hemodynamic impairment, indirect revascularization, direct revascularization, indication and management of cerebral revascularization in Moyamoya patients

2.1 History and Initial Description

After the first description of an arterial end-to-end anastomosis using suture by the French surgeon Alexis Carrel in 1902 it took another 70 years until Yasargil described the most influential direct revascularization technique with the introduction of the superficial temporal artery to middle cerebral artery (STA-MCA) bypass for internal carotid artery occlusion and moyamoya vasculopathy (MMV).1 In contrast, indirect revascularization techniques had been performed already in the 1940s representing the first attempts to revascularize the ischemic brain. Since the introduction of both revascularization strategies there remains significant debate about the superiority of indirect versus direct revascularization techniques in MMV.2 Current treatment protocols recommend direct revascularization techniques aiming at immediate supply of additional blood flow to the brain for adult patients as the anatomic difficulties encountered especially in MMV (small and fragile donor and recipient vessels that impose difficulties for the microsurgical anastomosis) are less pronounced in adult patients compared to pediatric MMV patients.3-5 Consequently, in pediatric MMV patients indirect revascularization techniques have been described to be very effective for treating ischemic symptoms and restoring cerebrovascular reserve capacity.3'Therefore, in adult MMV patients, direct STA-MCA bypass has become the workhorse for revascularizing the ischemic brain, in pediatric patients indirect procedures are regarded as equivalent revascularization strategy often resulting in a combination of both procedures.7

2.2 Analysis of Hemodynamic Compromise for Direct Bypass Surgery

The most important aim of direct bypass surgery represents correction of hemodynamic compromise and reduction of stroke risk. Hemodynamic compromise is assessed using PET measurements of cerebral blood flow with/without acetacolamide stimulation analyzing cerebrovascular reserve capacity and calculating oxygen extraction fraction (OEF). There are currently different tracers used including C15O PET for cerebral blood volume assessment, H215O for cerebral blood flow, and 15O2 to measure OEF and cerebral metabolic rate of oxygen.Using positron emission tomography (PET) analysis MMV patients have been characterized as patients with high cerebral blood volume due to maximal vasodilation and reduced OEF as a sign of hemodynamic compromise. Single-photon emission computed tomography (SPECT) analysis allows detection of hemodynamic compromise using nonquantitative, relative measurements comparing the healthy hemisphere with the diseased one, which imposes methodological limitations to a bilateral disease as MMV. Even though it remains to be determined whether PET analysis is superior to other imaging modalities analyzing cerebrovascular reserve capacity, our experience comparing SPECT and H215O PET for detecting hemodynamic compromise indicate improved sensitivity and specificity for PET techniques in this regard9 (Fig. 2.1).

Another highly reliable tool is Xenon-CT measurement of cerebrovascular reserve capacity. Xenon-enhanced CT has been shown to correlate with increased risk of ischemic stroke in the presence of reduced cerebrovascular reserve capacity and therefore represents a gold standard for detecting hemodynamic compromise.10,11 Correspondingly, direct bypass surgery significantly improves cerebrovascular reserve capacity in MMV patients.12 However, significantly reduced availability of this technique due to approval restrictions avoid a broad application of Xenon-CT for detecting hemodynamic compromise in MMV patients. Novel MRI techniques may contribute to the hemodynamic assessment preoperatively. Dynamic susceptibility contrast-weighted bolus-tracking MRI, arterial spin labeling MRI, and blood oxygen level-dependent MRI have been shown to potentially identify tissue at risk for cerebral ischemia, hemodynamic compromise, and restoration of hemodynamic compromise after direct revascularization.13

Moreover, novel data imply that quantitative analysis of cerebral blood flow or OEF may not yet represent the only decisive indicator for future stroke in MMV as Zipfel et al demonstrate a 10% stroke risk for MMV patients with normal OEF in PET studies.14 Therefore, other factors must be included in the surgical decision-making process. These include the potential progressive character of MMV and the extraordinarily high risk of ischemic stroke if both hemispheres are affected by the disease (>80% stroke risk in 5 years).15 Following the Berlin moyamoya grading system, MMV may be graded according to angiography, presence of ischemic lesions in MRI, and the associated hemodynamic compromised into three different grades that correlate with the presence of ischemic symptoms and the associated risk for cerebral revascularization16,17 (Fig. 2.2).

Especially, high-grade MMV patients impose a higher ischemia risk during cerebral revascularization than low- grade MMV patients, indicating that early revascularization may be reasonable in these patients avoiding a high complication profile while resulting in a significant reduction of stroke risk16. Moreover, the risk for cerebral hemorrhage must be included as STA-MCA bypass significantly reduces the risk for cerebral hemorrhage.18 The ethnic background of the patient and the risk for cerebral hemorrhage, that varies among MMV populations with a higher incidence of hemorrhagic MMV in Asia as compared to the predominantly ischemic populations in North America and Europe,2,19-21 in combination with the presence of fragile collateral vessels and microaneurysms further factors that should be considered in the surgical decision-making process for direct revascularization surgery.

2.3 Key Principles of Direct Revascularization Surgery

2.3.1 Graft Choice

In MMV, the STA is usually used as a donor vessel because standard STA-MCA bypass is regarded as the treatment of choice for direct revascularization procedures. High- flow bypass procedures are associated with a high-risk profile for hyperperfusion syndrome and therefore represent only rescue strategies in cases of failed low-flow anastomosis and/or failed indirect procedures.22 In this regard, bypass flow in STA-MCA bypass has been described to range between 10 and 60mL/min while flows above 30mL/min are associated with increased risk for hemorrhage and stroke.23 Other direct anastomosis techniques including STA-ACA bypass, occipital artery-posterior cerebral artery (OA-PCA) anastomosis, multiple insertion procedures, and the use of the auricular artery as donor vessel have been described by different bypass-experienced groups, yet all of these procedures do not display superiority to regular STA-MCA anastomosis and they are often associated with distinct disadvantages. Therefore, they play a minor role in direct revascularization of MMV patients and predominantly serve as rescue strategies in cases for failed primary revascularization procedures.

2.3.2 Recipient Artery

For direct STA-MCA anastomosis, an M4 segment of the MCA is usually selected as the recipient vessel. In cases of a missing suitable recipient, the sylvian fissure may be opened to select an M3 or M2 segment as recipient. However, in these cases microanastomosis may be technically more demanding and the risk of ischemia during temporary occlusion is unknown. In order to reduce the risk of a nonsuitable recipient vessel craniotomy may be placed above the “target point” at the end of the sylvian fissure.24 In this area, the risk for a nonsuitable recipient vessel is extremely low as the end of the sylvian fissure is characterized by numerous vessels entering the cerebral cortex.

2.3.3 Standardized Strategies versus Targeted Bypass Procedures

There remain debates about the use of a standardized surgical approach (e.g., using the target point as general localization for microanastomosis) versus performing targeted bypass procedures (e.g., using STA-ACA anstomosis in cases of predominantly hemodynamic compromise in the ACA vascular territory). Direct STA-MCA bypass at the target point has been shown to restore cerebrovascular reserve capacity independent from the most prominently compromised vascular territory, which is probably the result of suitable intracerebral collateralization path- ways.12 Especially, MMV patients are characterized by intensive leptomeningeal anastomosis, pericallosal anastomosis, and increased cortical microvascularization supporting the benefits of a standardized surgical approach in order to restore cerebrovascular reserve capacity.25 Moreover, temporary occlusion of an M4 segment may be performed without the risk of occlusion-induced cerebral ischemia, which may not be the case for more proximal anastomosis.26 Targeted bypass procedures have been described by different groups,27 yet targeted bypass procedures rely on definite localization of tissue at risk for ischemia, which still presents a major challenge for imaging modalities. Moreover, surgical techniques are more difficult as multiple insertion strategies with longer donor vessels and larger as well as diverse craniotomies are often required, leading to prolonged surgical time and a higher risk for intraoperative ischemia. Despite these difficulties, several moyamoya groups have reported good surgical outcomes for targeted bypass procedures especially in pediatric patients.27 For lack of a randomized clinical trial, it depends on the surgeons’ expertise and experience which direct revascularization strategy is performed without additional guidelines from the current body of literature.

2.3.4 Peri- and Intraoperative Management and Neuroprotection

General anesthesia is recommended for direct revascularization surgery. The most important goal during the peri- and intraoperative period is to maintain conditions that optimize cerebral blood flow and minimize the risk of ischemic or hyperemic injury.2 During preoperative preparation normocarbia should be achieved especially in the induction of general anesthesia while maintaining blood pressure baseline values. Baseline blood pressure is assessed in the days before surgery with the patient in a normal state of activity. Intraoperative blood pressure management in our institution aims at the patients’ baseline blood pressure level plus additional 10% in order to maintain high cerebral perfusion pressure. Maintaining oxygenation, normocarbia, stable arterial blood pressure, and an adequate depth of anesthesia is critical during the intraoperative period. In the case of hypertonic medications avoidance of hypotension after diuresis is another important aspect. During the time period of anastomosis, which requires temporary occlusion of a cortical vessel, oxygenation fraction is increased to 100% in order to further minimize the risk of occlusion-induced ischemia. Moreover, intraoperative monitoring of somatosensory- evoked potentials, motor-evoked potentials, and EEG monitoring may be used to detect phases of critical hypo- or hypertension.8 Early postoperative extubation is the goal in order to enable early and serial neurologic examinations after direct revascularization surgery. During the postoperative phase, maintenance of blood pressure is achieved aiming at the patients’ baseline blood pressure values in addition to adequate pain control and sufficient antiplatelet therapy.

2.3.5 Intraoperative Flow Assessment

Intraoperative application of indocyanine green (ICG) videoangiography nowadays allows immediate assessment of bypass patency, which should be performed routinely after microanastomosis.28 Yet ICG videoangiography does not provide quantitative information regarding bypass flow due to limitations of flow assessment using fluorescence probes.29 Only intraoperative assessment of bypass flow using microflow probes allow quantitative assessment of flow characteristics before and after anastomosis and may therefore provide information about bypass capacity and bypass efficiency after anastomosis by assessing the cut flow index.23 Usually a cut flow index of above 0.5 is regarded as sufficient bypass function and indicates good bypass efficiency. In cases of a cut flow index below 0.5, analysis of potential confounders inflicting with bypass function should be performed focusing on problems with the microanastomosis or the recipient artery.23 In these cases bypass revision or even selection of another recipient may be performed to improve bypass function. Therefore, direct intraoperative flow assessment strategies provide information about potential drawbacks during bypass surgery and may help in the decision-making process in the case of bypass failure or poor bypass function. Additionally, massively increased flow in the MCA after direct anastomosis has been described to predict perioperative ischemia and hemorrhage.30 Intraoperative detection of this risk factor allows fine adjustment of postoperative management regarding blood pressure control and may therefore help in the complex perioperative management of MMV patients.

In order to monitor bypass induced changes to cortical perfusion, intraoperative laser speckle imaging allows pseudoquantitative assessment of cortical perfusion before and after STA-MCA microanastomosis and may therefore allow conclusions about immediate global effects of bypass surgery on brain perfusion and distribution of additional blood flow in cerebral cortex.31 Other strategies have been applied including a thermal diffusion flow probe to analyze regional cerebral blood flow before and after anastomosis, a light spectroscopy system for detection of oxygen saturation as well as infrared brain surface blood flow monitoring. All of the above named procedures share the fact that they are applied exclusively in an academic setting without a broad generalized application of these systems.

Intraoperative digital subtraction angiography provides detailed information about bypass flow and filling of cortical arteries via the bypass; however, intraoperative digital subtraction angiography is rarely available and is associated with prolonged surgical time.

2.4 General Complications and Risk Stratification

Rates of postoperative ischemia for direct revascularization in the treatment of MMV have been described to range between 3 and 8%, depending on the applied surgical strategy.2,21 Accepting this risk profile for perioperative ischemia the 5-year stroke risk is reduced to 5.5% with more than 90% of MMV patients being free of recurrent transient ischemic attacks in the case of successful revascularization.2,21

A major confounding problem in perioperative management of MMV patients is the phenomenon of hyperperfusion syndrome. This has been reported to occur in up to 38% of MMV patients after direct revascularization even though the exact risk profile remains unknown as surgical series in North America and Europe demonstrate significantly lower risk profiles for hyperperfusion syn- drome.32,33 Hyperperfusion may be associated with significant clinical neurological deficits as dysarthria, paresis, aphasia, and sensorimotor loss. These patients do not present signs of cerebral ischemia in postoperative MRI but rather demonstrate hyperperfusion aspects in postoperative perfusion studies as SPECT or MR/CT perfusion. The most important clinical aspect is to recognize this phenomenon as it requires a totally different treatment decision as postoperative ischemia (which requires an increase or at least maintenance in blood pressure). In hyperperfusion syndrome lowering of blood pressure is mandatory to treat neurological deficits. Especially patients presenting with highly frequent transient ischemic attacks are significantly associated with postoperative hyperperfusion syndrome.

In order to predict risk profiles of MMV patients, a novel grading scale of MMV allows differentiation between three MMV patient profiles.16 Applying this grading protocol demonstrates that MMV patient with a mild form are characterized by extremely low-risk profile for perioperative ischemia (0%) whereas patients with a severe form of MMV may face a risk profile of up to 16% in the case of one-staged bilateral revascularization.17 As this risk profile has been confirmed by other surgical groups with different surgical strategies, it becomes clear that revascularization surgery should be performed during an early phase of the disease. Not only to treat ischemic symptoms as early as possible and to avoid manifest cerebral infarctions, but also because the perioperative risk profile is lower during an early phase of the disease when hemodynamic compromise is less severe.

In this regard, many postoperative ischemic events do not occur in the hemisphere that underwent revascularization surgery. Competing flow between native collaterals and the bypass, distinct features of peri-, intra-, and postoperative blood pressure management and the associated hemodynamic fragility of MMV may be responsible for these ischemic events highlighting the importance of an experienced and sensitive interdisciplinary environment during the surgical treatment of patients.


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