Revascularization Techniques in Pediatric Cerebrovascular Disorders

This chapter focuses on brain revascularization techniques used for the treatment of pediatric cerebrovascular disease. Although a wide variety of clinical scenarios might warrant surgical revascularization of the brain, the three most commonly encountered by neurosurgeons include atherosclerotic carotid disease, intracranial aneurysms, and moyamoya syndrome. This chapter will focus primarily on surgical revascularization in the setting of treating children with moyamoya syndrome.

Moyamoya Syndrome

Moyamoya syndrome is an arteriopathy characterized by progressive stenosis of the distal internal carotid arteries as they enter the cranial vault. ^, Narrowing of the internal carotids causes reduced cerebral blood flow, the development of cerebral ischemia, and collateral blood vessel formation in the region of the carotid bifurcation, on the cortical surface, and from branches of the external carotid artery (ECA). This alternative blood supply—composed of recruitment of maximally dilated preexisting arteries and growth of new vessels—provides circulation to the region formerly supplied by the internal carotids. Although usually limited to the anterior circulation, this process may also involve the posterior circulation, including the basilar and posterior cerebral arteries. The appearance of this basal collateral network on angiography has been compared to a hazy cloud or puff of smoke: the disease defined by the Japanese word “moyamoya.” Due to the natural propensity for patients with moyamoya to develop collateral vessels from branches of the external carotid, and the fact that both the external carotid circulation and arteries on the surface of the brain are not involved in moyamoya arteriopathy, most of the surgical revascularization techniques in this condition aim to augment blood flow to the ischemic brain by utilizing the external carotid circulation as a donor source of new blood flow to arteries on the surface of the brain.

Evaluation

Moyamoya should be included in the differential diagnosis when cerebral ischemia is suspected in children, as moyamoya is associated with approximately 6% to 10% of non-perinatal pediatric strokes and transient ischemic attacks (TIA). ^, Evaluation should consist of (1) clinical assessment, including consideration of specific populations at increased risk of moyamoya ( Table 75.1 ); (2) radiographic studies, incorporating magnetic resonance imaging (MRI) and potentially digital subtraction angiography (DSA); and, if moyamoya is identified, (3) discussion of screening family members with imaging and genetic testing.

Table 75.1

Moyamoya Associations

Alagille syndrome
Asian ancestry
Autoimmune disease (DM I, thyroid disease)
Cranial radiation
Congenital structural cardiac disease
Down syndrome
MOPD (microcephalic osteodysplastic primordial dwarfism)
Neurofibromatosis type I (NF1)
PHACE syndrome (posterior fossa malformations–hemangiomas–arterial anomalies–cardiac defects–eye abnormalities–sternal cleft and supraumbilical raphe syndrome)
Robinow syndrome
Seckel syndrome
Sickle cell disease

Radiographic

The initial evaluation of moyamoya-related cerebral ischemia typically includes MRI. While protocols may be institution-specific, the general use of axial T1/T2 images to assess structural anatomy, diffusion-weighted imaging (DWI) to assess acute stroke, FLAIR images to assess chronic stroke burden and areas of slow flow (as evidenced by ivy sign, present in ∼80% of cases), and MR angiography (MRA) to visualize the circle of Willis are commonly available and useful sequences. ^, Advances in vessel wall imaging can help distinguish between vasculitis and moyamoya.

If moyamoya is identified on MRI, then DSA should be considered, as this modality has higher diagnostic sensitivity for moyamoya compared to MRI (including the ability to better differentiate vasculitis) and offers important data germane to preoperative planning. Specifically, transdural collaterals visualized on DSA are critical biomarkers of disease that can assess angiogenic potential (particularly in combination with proteomic assays), predict 1-year radiographic outcomes from surgery, and when incorporated into surgical planning, have been demonstrated to reduce perioperative stroke complications by greater than 40% (especially in the setting of previous cranial surgery or shunting). ^, ^, ^, The risk of DSA is generally low, with ∼1% complication rates at high-volume centers. ^, Contraindications include contrast allergies, aortic stenosis, and general medical instability precluding a sedated or anesthetized procedure.

Surgical Treatment of Moyamoya

Surgical revascularization is the primary treatment for moyamoya. ^, ^, ^, ^, Key points of surgical management include appropriate indications for surgery, timing of operation, selection of specific technique and expectation setting for expected outcomes following revascularization. Tenets of perioperative care include careful hydration (often with intravenous fluids at 1–1.25× maintenance), avoidance of hyperventilation-related cerebral vasoconstriction (often due to crying, pain, or emesis), and strict blood pressure control to avoid even brief hypotension and maintain cerebral perfusion.

There are two main categories of surgical revascularization: direct (which involves transecting a donor vessel and anastomosing it directly to a single recipient cortical vessel) and indirect (which utilizes some vascularized tissue such as a vessel, muscle, or pericranium to stimulate the growth of a new vascular network when placed in contact with the brain). In direct revascularization, a branch of the ECA (usually the superficial temporal artery [STA]) is anastomosed end to side to a cortical artery (usually a distal branch of the middle cerebral artery [MCA]), the so-called “STA-MCA bypass.” In contrast, indirect techniques involve mobilizing vascularized tissue supplied by the ECA (including dura, muscle, and/or pedicles of the STA) and placing it in contact with the brain to promote the in-growth of new vessels to the cortex.

Both are effective in reducing the stroke rate in moyamoya patients, but direct procedures may not be technically possible in younger children. Historically, direct revascularization procedures have been favored in adults, with resultant immediate increase of blood flow to the ischemic brain cited as a major benefit of the procedure. In contrast, augmentation of cerebral blood flow usually does not occur for several weeks with indirect techniques. Despite this anticipated benefit over indirect revascularization, direct bypass is often technically difficult to perform in children because of their small caliber donor and recipient vessels, making indirect procedures appealing. Nonetheless, direct operations have been successful in children as have indirect procedures in adults. Considerable debate exists regarding the relative merits and shortcomings of the two approaches; in fact, some centers advocate combinations of both approaches. In addition, recent analyses support the premise that indirect operations are more durable with better long-term results in the pediatric population.

Numerous indirect revascularization 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; encephalo-myo-arterio-synangiosis (EMAS), which combines EDAS and EMS; pial synangiosis , a variant of EDAS described in detail as follows, in which the STA is sutured to the brain; the drilling of multiple burr holes without vessel synangiosis; and dural inversion , involving a craniotomy, opening of the dura, and turning the dural flaps inward over the surface of the brain. Cervical sympathectomy and omental transposition or omental pedicle grafting have also been described. We have found the technique of pial synangiosis particularly effective in the pediatric moyamoya population and, upon review of 143 patients treated with pial synangiosis, demonstrated marked reductions in stroke frequency following surgery. Regardless of the revascularization procedure employed, the perioperative strategies for complication avoidance are relevant to all moyamoya patients.

There is abundant evidence that surgical revascularization improves a wide range of outcome metrics in patients with moyamoya. Radiographically, revascularization reverses white matter changes, improves measures of cerebral oxygenation and increases cerebral blood flow, and stabilizes stroke burden despite progressive arteriopathy. ^, Clinically, surgery decreases ischemic symptoms, headache, risk of hemorrhage, and markedly reduces stroke rates (without surgery, stroke risk is 32% at 1 year and 66% to 90% at 5 years; after surgery, stroke risk drops to <5% for most populations at both 1 and 5 year time points), while concomitantly improving functional and cognitive outcomes. ^, ^, ^, ^,

Pial Synangiosis

We have recently published a specific perioperative protocol for patients with moyamoya (see Table 75.1 ). This protocol has been adapted from our practice for all patients with moyamoya and highlights general strategies we have found useful in the surgical management of this condition.

Indications for Surgery

Indications include radiographic evidence of moyamoya, coupled with ongoing ischemic symptoms and/or evidence of compromised blood flow or cerebral perfusion reserve. This latter criterion stems from data suggesting that clinically asymptomatic patients who have radiographic or functional evidence of impaired cerebral perfusion should also be considered as operative candidates. Relative contraindications include very early stage arteriopathy with normal perfusion and/or patients with profound medical or neurological compromise. ^, ^, ^, Of note, the scant existing data describing moyamoya surgical revascularization in patients harboring a mutation in the ACTA2 gene (encoding the smooth muscle-specific isoform of alpha-actin) suggest that this population is at very high risk for perioperative stroke.

The timing of surgery should generally minimize the duration between diagnosis and revascularization, although delays of several weeks may be appropriate to coordinate skilled anesthetic and operating room staffing, or to allow swelling from an acute stroke to abate. If possible, performing bilateral surgery (if indicated) under a single anesthetic may help reduce perioperative complications and the vulnerable period before both sides grow surgical collaterals, particularly in very young patients.

Overall, we generally advocate surgical treatment for patients with radiographically confirmed moyamoya, even if asymptomatic, as the preponderance of evidence suggests that moyamoya is a relentless, progressive process in children. Surgical treatment, both direct and indirect, has been shown to be safe when performed by experienced surgeons and confers long-lasting, durable protection from stroke relative to medical therapy alone.

It is increasingly clear that one of the most important predictors of surgical outcome is whether the patient is treated at a high-volume center with a dedicated cerebrovascular team. Recent data from national database analysis reveals that high-volume centers (averaging >30 procedures annually) had shorter lengths of stay (32%), lower costs (57%), an 8-fold higher likelihood of discharge to home (vs. rehabilitation), and a 15-fold lower rate of death. These data support the regionalization of care with centers of excellence for subspecialized moyamoya treatment.

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