Moyamoya Disease

Pial Synangiosis: Encephaloduroarteriosynangiosis–Encephalomyosynangiosis

Ronald T. Grondin, Edward R. Smith, and R. Michael Scott

Moyamoya syndrome is a vasculopathy characterized by chronic progressive stenosis to occlusion at the distal portions of the intracranial internal carotid arteries, including the proximal anterior cerebral arteries (ACAs) and middle cerebral arteries (MCAs). It is associated with ~6% of childhood strokes.1,2 As progressive stenosis occurs, characteristic arterial collateral vessels develop at the base of the brain. These collateral vessels, when visualized on angiography, have been likened to the appearance of “something hazy, like a puff of cigarette smoke drifting in the air,” which translates as moyamoya in Japanese.

Some authors have distinguished between moyamoya disease, the idiopathic form of moyamoya, and moyamoya syndrome, defined as the vasculopathy found in conjunction with systemic conditions such as heart disease, sickle cell disease, and Down syndrome.^3,4 In both moyamoya disease and moyamoya syndrome, treatment strategies are directed toward improving the cerebral blood supply. Medical management is an important adjunct in improving the outcomes of patients with moyamoya, but definitive treatment of the disease appears to require cerebral revascularization. Here, we review the diagnosis and management of moyamoya, with a particular focus on the utilization of a specific method of “indirect” (not directly anastomosing two vessels together) cerebral revascularization–pial synangiosis.

Clinical Presentation and Natural History

Adults with moyamoya often present with hemorrhage, leading to rapid diagnosis. In contrast, children usually present with recurrent transient ischemic attacks (TIAs), stroke, seizures, or headaches; only ~3% of pediatric patients in the Children’s Hospital, Boston series had an intracerebral hemorrhage as their first symptom.³

The natural history of moyamoya syndrome is variable, ranging from slow progression, with rare, intermittent events, to rapid progression with fulminant neurologic decline.^3,5 At the time of their initial presentation, almost all children have bilateral involvement by arteriography, and the majority of remaining patients presenting with unilateral disease will go on to develop disease in the contralateral hemisphere.³ It has also been estimated that up to 66% of patients with moyamoya have progression of the disease with poor outcomes if left untreated.^6–8 This number contrasts strikingly to an estimated rate of only 2.6% of symptomatic disease progression in a meta-analysis of 1156 surgically treated pediatric patients.⁹ A more recent review of asymptomatic patients reported an annual stroke rate of 3.2% and reported radiographic progression of disease in 80%.¹⁰ The experience of Children’s Hospital, Boston has been that ~67% of patients will demonstrate radiographic progression of disease within a 5-year period.

The overall prognosis of patients with moyamoya syndrome depends on the rapidity and extent of vascular occlusion, the patient’s ability to develop effective collateral circulation, the age at onset of symptoms, the severity of presenting neurologic deficits and degree of disability, and the extent of infarction seen on computed tomography (CT) or magnetic resonance imaging (MRI) studies at the time of initial presentation.¹¹ In general, neurologic status at the time of treatment, more so than the age of the patient, predicts long-term outcome.^3,12

Importantly, individual patients have an excellent prognosis if surgical revascularization is performed prior to disabling infarction, even if severe angiographic changes are already present.³ Even in asymptomatic patients, surgical revascularization has been reported to protect against infarction.¹⁰ However, if left untreated, both the angiographic process and the clinical syndrome invariably progress, producing clinical deterioration with potentially irreversible neurologic deficits over time.¹³

Diagnostic Investigations

Moyamoya syndrome should be considered and diagnostic evaluation begun in any child who presents with symptoms of cerebral ischemia (e.g., a TIA manifesting as episodes of hemiparesis, speech disturbance, sensory impairment, involuntary movement, and/or visual disturbance), especially if the symptoms are precipitated by physical exertion, hyperventilation, or crying. The diagnosis of moyamoya is confirmed by radiographic studies. Radiographic evaluation of a given patient suspected of having moyamoya usually proceeds through several studies.

On CT, small areas of hypodensity suggestive of stroke are commonly observed in cortical watershed zones, basal ganglia, deep white matter, or periventricular regions.14,15 Hemorrhage from moyamoya vessels can be readily diagnosed on head CT.

CT findings often lead to an MRI study, with acute infarcts seen using diffusion weighted imaging (DWI) and chronic infarcts visualized with T1 and T2 imaging. Ongoing cortical ischemia may be inferred from fluid attenuation inversion recovery (FLAIR) sequences that demonstrate linear high signal following a sulcal pattern, felt to represent slow flow in poorly perfused cortical circulation (the so-called ivy sign).^15,16 The most diagnostic MRI findings in moyamoya disease are diminished flow voids in the internal carotid and middle and anterior cerebral arteries coupled with prominent collateral flow voids in the basal ganglia and thalamus.^15,17–21

Cerebral angiography is the gold standard for the diagnosis of moyamoya disease. Angiographic studies should include selective injection of both internal and external carotid arteries and vertebral arteries. External carotid imaging is essential to identify preexisting collateral vessels, so that surgery, if performed, will not disrupt them. Aneurysms or arteriovenous malformations (AVMs), known to be associated with some cases of moyamoya, can also be best detected by conventional angiography.

Cerebral Perfusion Studies and Follow-up Imaging

Cerebral blood flow studies can be helpful in the diagnostic evaluation of patients with moyamoya disease and assist in treatment decisions. Techniques include transcranial Doppler (TCD) ultrasonography, xenon-enhanced CT, positron emission tomography (PET), and single-photon emission computed tomography (SPECT) with acetazolamide challenge.

Although each of these studies has the potential to add information on the diagnosis and management of moyamoya, not all are routinely used in the United States. MRI/MR angiography (MRA) and conventional angiography are the standard diagnostic tools used for most patients with moyamoya. Following treatment, an angiogram and an MRI/MRA are often obtained 1 year after surgery and, depending on the age of the patient, yearly MRI thereafter.

Surgical Treatment

Once a major stroke or hemorrhage has occurred, children with moyamoya disease frequently are left with permanent neurologic impairment.^5,22 Therefore, early diagnosis and prompt treatment of this disorder are of utmost importance to prevent additional neurologic deficits. Despite this urgency, there is no agreed-upon method of treatment for patients with this chronic occlusive cerebrovascular disorder. There are reports of some patients who stabilize clinically without intervention, but this typically occurs after they have experienced significant, debilitating neurologic disability.

The majority of data available supports the use of surgical revascularization as a first-line therapy for the treatment of moyamoya syndrome, particularly for patients with recurrent or progressive symptoms.⁹ Some studies have suggested that there may be differences in the effectiveness of surgery for the treatment of moyamoya depending on the type of presentation of the patient—hemorrhagic or ischemic.⁶ These studies suggest that revascularization procedures prevent recurrent ischemic attacks, an important finding given that the majority of pediatric patients with moyamoya present with ischemic symptoms. Two relatively large studies with long-term follow-up have demonstrated a good safety profile for surgical treatment of moyamoya (4% risk of stroke within 30 days of surgery per hemisphere), with a 96% probability of remaining stroke-free over a 5-year follow-up period.^3,6 These data suggest that surgical therapy of moyamoya confers an effective, durable treatment for the disease.

Advantages and Disadvantages of Direct Revascularization Procedures Relative to Indirect Revascularization Procedures

Surgical treatments designed to increase perfusion of ischemic neural tissue in patients with moyamoya can be classified as direct, in which a healthy vessel is transected and anastomosed end to side to a cortical vessel distal to the site of moyamoya stenosis, or indirect, in which vascularized tissue, including muscle, dura, and scalp vessels, are put into contact with the brain and serve as a new source of collateral vessel development over time.

Direct anastomosis procedures, most commonly superficial temporal artery (STA)–to–MCA bypasses, may achieve instant improvement in focal cerebral perfusion, but these procedures are technically difficult to perform because pediatric patients often do not have a large enough donor scalp artery or recipient MCA to allow for an anastomosis large enough to supply a significant amount of additional collateral blood supply. Because of proximal stenoses, new blood supply provided to a single MCA branch may not allow wide redistribution of the newly available collateral. Temporary occlusion of a middle cerebral branch during the anastomosis may interfere with leptomeningeal collateral pathways already present and lead to an increased incidence of perioperative stroke. Furthermore, there is a paucity of reported series documenting the effectiveness of STA-MCA bypass in children in the United States. There is however, extensive evidence, including long-term follow-up, substantiating the efficacy of indirect revascularization procedures, such as pial synangiosis.3

Indirect Revascularization Procedures

A variety of indirect anastomotic procedures have been described: encephaloduroarteriosynangiosis (EDAS), whereby the STA is dissected free over a course of several inches and then sutured to the cut edges of the opened dura; encephalomyosynangiosis (EMS), in which the temporalis muscle is dissected and placed onto the surface of the brain to encourage collateral vessel development; and the combination of both, encephalomyoarteriosynangiosis (EMAS).^23–25 There are multiple variations of these procedures, including solely drilling bur holes, without vessel anastomosis,^26,27 and craniotomy with inversion of the dura in hopes of enhancing new dural revascularization of the brain.²⁸ Cervical sympathectomy,²⁹ omental transplantation,^30–32 and omental pedicle grafting^33–35 have also been described, although sympathectomy has largely been abandoned due to its ineffectiveness.³⁶ Finally, several groups have reported improved results in the use of combined direct and indirect anastomoses.^23,37–39 A modification of the EDAS procedure has been described to treat moyamoya syndrome in both children and adults, termed pial synangiosis (described below), which leads to the induction of new collateral vessels in the patient with chronic ischemia due to moyamoya. The efficacy and durability of this specific variant of indirect revascularization have been validated by the largest surgical series of children with moyamoya reported in North America.³

Direct versus Indirect Procedures

One major consideration in the treatment of patients with moyamoya is the decision of which surgical technique to employ. A meta-analysis of 1156 pediatric patients treated with surgery concluded that 87% (1003 patients) derived symptomatic benefit from surgical revascularization (complete disappearance or reduction in symptomatic cerebral ischemia), but that there was no significant difference between the indirect and direct/combined groups.⁹Guidelines from Japan’s Ministry of Health and Welfare regarding indications for the surgical treatment of moyamoya syndrome (in both children and adults) discuss only direct bypass surgery for revascularization, a technique that is often not feasible in young children due to the small caliber of their vessels.⁴⁰ A review of pediatric patients with moyamoya has proposed that children under the age of 8 years should all receive indirect revascularization surgery, whereas older children could potentially receive both direct and indirect revascularization (if feasible).³⁹ The Children’s Hospital, Boston series strongly supports the utilization and long-term effectiveness of indirect revascularization with pial synangiosis in children of all ages. Although proponents of direct surgery often cite the primary benefit of immediate increases in perfusion, there is substantial evidence supporting the premise that indirect procedures, such as pial synangiosis, provide similar or improved long-term outcomes when compared with direct procedures in children. In addition, pial synangiosis is technically less demanding than direct bypass procedures, is less likely to fail, and does not present the risk of hyperperfusion injury.

Surgical Technique of Pial Synangiosis

The posterior (parietal) branch of the STA is identified by a pencil Doppler probe, and the artery is traced from its base above the zygomatic arch to the parietal convexity. Its course is accurately marked on the skin with an 18- or 21-gauge needle. We attempt to mark out at least 10 cm of vessel in most patients, but in young children, often only 6 to 7 cm can be identified. Although the parietal branch of the STA is most frequently used because the skin incision can be kept behind the hairline and the majority of the MCA circulation lies beneath that branch of the artery, the frontal branch can be used if necessary. Prior to draping, bilateral electroencephalography (EEG) electrodes are applied to the scalp so that continuous EEG monitoring can be performed throughout the case. Standard skin prep and draping can then be performed.

Skin Incision

We use the microscope right from the beginning of the artery dissection, finding it particularly helpful in very young children because of the fragility and small size of the STA and in young adults because of the frequent tortuosity of the vessel and its branches. A small skin incision down to subcutaneous tissue is made directly over the vessel at its most distal marked point with a no. 15 scalpel. The artery is identified by scalp retraction with toothed forceps and dissected using a delicate curved pediatric hemostat. A linear incision following the course of the artery is then performed, using the hemostat to dissect and then protect the STA as the assistant incises the skin overlying it. The skin edges rarely require coagulation, and most scalp edge bleeding will stop spontaneously, despite preoperative daily aspirin therapy, which is maintained throughout the peri- and postoperative period.

Synangiosis Procedure

After the artery is exposed, we use a needle-tip cautery (“Colorado needle”) at a low setting to separate the artery with its subjacent galea strip from the galea on either side. The artery pedicle is then encircled with a vessel loop distally and elevated and separated from the underlying periosteum and temporalis fascia using standard monopolar cautery, attempting to preserve as much adventitia and loose areolar tissue beneath the vessel as possible.

Anterior and posterior scalp flaps are then developed with electrocautery dissection to minimize bleeding, and disposable fishhook-type retractors are used to maintain scalp retraction. The artery pedicle is retracted out of the field as needed using the vessel loop, and the temporalis muscle is incised with the electrocautery into four equal quadrants, which are retracted widely using the previously placed skin hooks. Generous bur holes are drilled inferiorly and superiorly in the exposure, and as large a craniotomy as possible is turned using power equipment. The dura is then opened vertically along the exposure and cut into six separate flaps that are retracted on sutures; care is taken to preserve any significant middle meningeal collateral observed on the preoperative arteriogram, and the dura is opened around or between such vessels. Under high-power microscope, the arachnoid is incised linearly over the exposed cortex using a disposable arachnoid knife and jeweler’s forceps, beginning inferiorly over the temporal lobe in a sulcus and when possible laterally toward the crown of the adjacent gyri. Vannas ophthalmic scissors are helpful in making long, continuous arachnoid openings over MCA branches in certain patients. The pial vasculature will be profuse and tortuous in patients with advanced disease, and these areas of the pia should be avoided when the arachnoid is opened. Bleeding that occurs from the pial surface or from small vessels within the sulci usually stops after a few moments of irrigation with a microirrigator or the application of a minuscule pledget of Gelfoam soaked in saline. After completion of the arachnoid opening through as much of the length of the exposure as possible, the STA with its galea investiture is brought down onto the surface of the brain, placing the vessel over areas of opened arachnoid. Using jeweler’s forceps and a Castroviejo needle holder, the vessel is fixed to the cortical surface by placing three to six interrupted 10–0 nylon sutures through the vessel adventitia and the outermost layer of the pial-cortical surface (Fig. 14.1). At the completion of the pial synangiosis, the donor vessel is affixed to the cortical surface (Fig. 14.2). This tight pial approximation leads to a more satisfactory postoperative result then simply placing the vessel on the brain or suturing the vessel into the dura.

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