Moyamoya Syndrome

Moyamoya syndrome is an arteriopathy characterized by progressive stenosis of the distal internal carotid arteries as they enter the cranial vault.^1,2 With narrowing of the internal carotids, cerebral blood flow is reduced, cerebral ischemia develops, and collateral blood vessels develop in the region of the carotid bifurcation, on the cortical surface, and from branches of the external carotid artery (ECA). This alternative blood supply—comprised of maximally dilated pre-existing 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 involve the posterior circulation as well; 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.” Because of the natural propensity in patients with moyamoya for collateral vessels to the brain to develop from branches of the external carotid and because these arteries and those on the surface of the brain are not involved by the moyamoya arteriopathy, most of the surgical revascularization techniques in this condition utilize the external carotid circulation as a donor source of new blood flow to the ischemic brain.

Surgical Treatment of Moyamoya

Two general methods are employed: direct and indirect. 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 (dura, muscle, pedicles of the STA) and placing it in contact with the brain to promote in-growth of new vessels to the cortex.

Historically, direct procedures have been used in adults, with immediate increase of blood flow to the ischemic brain cited as a major benefit of the procedure. Augmentation of cerebral blood flow usually does not occur for several weeks with indirect techniques. However, direct bypass is often technically difficult to perform in children because of the small size of donor and recipient vessels; making indirect techniques appealing. Nonetheless, direct operations have been successful in children as have indirect procedures in adults.^3–5 Considerable debate exists regarding the relative merits and shortcomings of the two approaches; in fact, some centers advocate combinations of both approaches.^5–7

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; the combination of both, encephalo-myo-arterio-synangiosis (EMAS), a variant of EDAS in which the STA is sutured to the brain; pial synangiosis, described in detail below; and the drilling of multiple burr holes without vessel synangiosis.^8–14 Dural inversion, carrying out a craniotomy, opening the dura, and turning the dural flaps inward over the surface of the brain has also been described as a revascularization technique.¹³ Cervical sympathectomy and omental transposition or omental pedicle grafting have also been described.² We have found the technique of pial synangiosis particularly effective in the pediatric moyamoya population, and in a review of 143 patients treated with pial synangiosis, demonstrated marked reductions in stroke frequency following surgery.¹⁴ Regardless of the revascularization procedure utilized, the perioperative strategies for complication avoidance are relevant to all moyamoya patients, regardless of surgical technique employed.

Operative Approach

Prior to incision, intravenous antibiotics are given. The microscope is employed from the onset of the case. No infiltration of the scalp with local anesthetic or epinephrine is used in order to avoid injury to the vessel.

Vessel Dissection

Using high magnification, a #15 blade is used to score the dermis at the distal end of the STA. A thin, curved pediatric hemostat and toothed Adson pickups are used by the surgeon (with suction and a second pickup by the assistant) to identify the STA under the skin. Using a repeated technique of subcutaneous dissection with the hemostat over the STA followed by elevation of the skin by the hemostat and an incision over the hemostat by the assistant, the STA is dissected along its length down to the root of the zygoma. Care must be taken to avoid tearing the vessel; particularly at tortuous bends or side branches. Irrigating bipolar (usually set at 25 with fine tips) is employed for hemostasis of small scalp vessels. A 0.05 × 3 cm Cottonoid is often useful to cover the exposed vessel to gently tamponade scalp bleeding as proximal dissection continues; electrocautery is used sparingly to control bleeding points along the incision line. A longer length of STA dissection is preferable (10 cm is optimal, although not always possible, especially in smaller children) (Fig. 61-1).

FIGURE 61-1 These images demonstrate the initial steps in performing a pial synangiosis. A, Course of the parietal branch of the STA marked out following Doppler mapping. B, Distal incision with subcutaneous dissection using a fine curved hemostat. C, Completed dissection of the STA branch prior to freeing up an adventitial cuff. D, Elevation of the STA with an associated adventitial cuff, using the monopolar cautery. Note that all of the surgery occurs under the microscope.

Following dissection of the STA branch, the “Colorado needle” electrocautery device (at low settings, usually one half to one third of the standard skin setting) is used in conjunction with the bipolar and microscissors to divide the galea and soft tissue on either side of the STA down to the temporalis fascia; leaving 1 to 2 mm of cuff on either side of the vessel. Two self-retaining retractors are then placed: one proximal and one distal. Dissection often terminates at the take-off of the frontal branch which should be preserved, if possible. However, if the bifurcation is high enough to prohibit mobilization of the STA then the frontal branch of the STA often must be divided. The preoperative arteriogram will indicate whether the frontal branch provides any significant intracerebral collaterals that can be relevant to the decision to potentially sacrifice the branch. Following the dissection of the vessel, a vessel loop is placed under the distal end of the STA and used to elevate the dissected portion of the vessel from the temporalis muscle. Monopolar electrocautery is then used to free up connective tissue around and beneath the vascular pedicle.

Craniotomy

Once the STA is freed, the microscope is removed and scalp flaps are developed using the electrocautery to minimize bleeding: creating a subgaleal dissection plane anteriorly and posteriorly. The temporalis is then divided into quadrants with the electrocautery. The muscle is reflected from the bone (with use of the electrocautery) and held back with multiple Lone Star retractors (fish hooks). Two burr holes are made; one inferior and one superior, in the bony exposure at the proximal and distal sites of the STA over the exposed bone. Following dural dissection with a #3 Penfield, the footplate is then used to turn the widest possible craniotomy flap. Care must be taken to avoid injury to the vessel. This is usually best performed by the assistant protecting the vessel with retractor (Fig. 61-2).

FIGURE 61-2 Intraoperative photographs documenting the steps of the craniotomy for pial synangiosis. A, Initial dural opening with stellate flaps and course of the STA. B, Arachnoidal opening, usually performed over vessels first, followed by subsequent opening over the cortex, if possible. C, Technique for placing 10-0 nylon stitch through pia and STA adventitial cuff. D, Completed suture, demonstrating good pial apposition to the vessel.

Dural Opening

Review of the angiogram is helpful to attempt to avoid disrupting pre-existing dural collaterals. If the middle meningeal artery is providing an important source of collateral flow, it is kept intact and the dura is opened in two separate windows on either side. The dura is opened with a #15 blade; with the initial incision line along the axis of the donor vessel, with the opening extended into six leaves of dura, three per side, retracted with 4-0 sutures. Small pieces of Gelfoam are placed between the retracted dura and craniotomy edge for hemostasis. Care is taken to minimize use of the bipolar on the dura in order to maximize collateral vessel development; although hemostasis is paramount in these patients. We avoid the use of thrombin after the dura is opened because of its demonstrated tendency to induce vasospasm in this patient population and all hemostatic substances such Gelfoam are from this point on in the operation moistened with saline solutions only.

Microsurgical Arachnoid Opening and Pial Synangiosis

Under the microscope, the arachnoid is opened widely; using the arachnoid knife, van Ness scissors, and jeweler’s forceps. Bleeding is controlled with irrigation or small dots of Gelfoam. The donor vessel is laid on the brain surface in apposition to areas of open arachnoid. The adventitia of the donor vessel is sutured to the superficial pia of the subjacent cortex, using 10-0 nylon suture on a BV-75 needle using three knots per suture. Generally, at least three sutures are placed. Vasospasm, if seen, is treated with topical papaverine.

Closure

After synangiosis, the microscope is removed. The dural flaps are repositioned on the brain surface but not sutured. The entire craniotomy exposure is then covered with a large piece of Gelfoam soaked in saline. The burr holes on the bone flap are enlarged to facilitate entry and exit of the vessel (Fig. 61-3). The bone flap is replaced with small titanium plates (not over the burr holes) and the temporalis muscle is closed only vertically to prevent pressure on the entering and exiting STA. Galea is closed with interrupted 3-0 vicryls (4-0 in smaller patients), taking care to avoid injuring the STA. Finally, the skin is closed with a running 4-0 rapide or other absorbable suture. Occasionally, EEG slowing will be noted with replacement of the bone flap. These usually resolve by adjusting anesthetic management or occasionally by briefly lifting the bone flap, followed by replacement of the bone.

FIGURE 61-3 Images taken at the conclusion of pial synangiosis. A, Final view of syangiosis prior to folding dural flaps down and placing Gelfoam on site. Note the course of the artery, wide arachnoidal opening, and significant area of the brain exposed to facilitate collateral development. B, View following replacement of the craniotomy flap. It is important to leave tension-free entry and exit sites for the STA at the base and apex of the craniotomy.

Contralateral Side

If the EEG is stable and the contralateral side is affected, then the wound is dressed. The patient is repositioned and the same operation is performed on the contralateral side. Loss of CSF from the first operation may make arachnoid opening more difficult on the second side. As previously discussed, the dominant or most symptomatic side is generally done first so that if there are intraoperative events that preclude continuing with the second side; the most important hemisphere has been treated.

Complication Avoidance

The most significant postoperative complication in our series has been stroke, which in a series of 143 patients occurred at about 4% per operated hemisphere. Patients at the greatest risk appear to be those with neurologic instability around the time of surgery, those who have suffered a stroke within 1 month of the operation, or those with certain angiographic risk factors such as moyamoya disease in the posterior circulation. There have been two perioperative deaths related to ischemic stroke: one in a 5-year-old child operated on in the midst of a crescendo of strokes preoperatively and one in a 15-year-old boy with unusually fulminant disease with pre-existing basilar artery occlusion whose internal carotid artery—the sole supply of his posterior circulation—thrombosed following a unilateral operation. Other complications include four subdural hematomas requiring evacuation and two spinal fluid leaks.

Preoperative

As discussed in the preoperative section, careful management of moyamoya patients before they get to the OR can have a significant influence on complication avoidance. Patients, ideally, should be neurologically stable prior to surgery and at least 1 month out from any significant stroke. Patients must be medically optimized for surgery including prehydration, as described in our protocol (Table 61-1). Preoperative imaging is critical to planning vessel selection (the parietal branch of the STA may be small or absent, necessitating utilization of a frontal or retroauricular branch).

Intraoperative

Avoid hyperventilation and hypotension at all times, and remain aware of EEG slowing. Anesthetic efforts to restore normal physiology often improve EEG changes. Throughout the case, meticulous hemostasis is vital to prevent postoperative hemorrhage in the setting of ASA. Careful dissection of the STA is critical to avoid tears or avulsion of side branches. Cautery of side branches further out from the donor vessel helps to minimize risk of inadvertently injuring the graft. Attentive detail to the closure reduces the likelihood of a CSF leak.

Postoperative

Continue IV fluids at 1.5× maintenance for 48 to 72 hours until clearly taking enough liquids orally. Aggressive pain control is important to minimize blood pressure fluctuations and hyperventilation. Frequent and detailed neurologic examinations by nursing staff and physicians are critical to identify possible postoperative ischemia such that interventions can be instituted in an attempt to avoid progressing to a completed stroke.

Follow-Up

Careful follow-up of patients with moyamoya is warranted to monitor for disease progression and for response to therapy.^16,17 We routinely obtain MRI and MRA studies 6 months after surgery. Postoperative angiograms are usually obtained 12 months after surgery and typically demonstrate excellent MCA collateralization from both the donor STA and the meningeal arteries. A repeat MRI and MRA is done for comparison purposes and for a new baseline. For high-risk patients, MRI/A may be obtained in lieu of an angiogram if contrast from the angiogram presents a substantial risk to the kidneys. Generally, annual MRIs are obtained in all patients for 3 to 5 years after the initial 1-year angiogram and then spaced out subsequent to the 5-year time point. Particular attention must be paid to patients with unilateral moyamoya as the opposite side can progress in up to one third of patients, especially in children.¹⁸ Patients are maintained on lifelong ASA therapy.

A review of 143 children with moyamoya syndrome treated with pial synangiosis had marked reductions in their stroke frequency after surgery especially after the first year postoperatively. In this group, 67% had strokes preoperatively and only 3.2% had strokes after at least 1 year of follow-up. The long-term results are excellent with a stroke rate of 4.3% (2 patients in 46) in patients with a minimum of 5 years of follow-up.¹⁹ This work supports the premise that pial synangiosis provides a significant protective effect against new strokes in this patient population.

Conclusions

Moyamoya syndrome is an increasingly recognized entity associated with cerebral ischemia. Diagnosis is made on the basis of clinical and radiographic findings, including a characteristic stenosis of the internal carotid arteries in conjunction with abundant collateral vessel development. Treatment is predicated on revascularization of the ischemic brain which can be direct (STA-MCA bypass) or indirect (including pial synangiosis). The use of pial synangiosis is a safe, effective, and durable method of cerebral revascularization in moyamoya syndrome and should be considered as a primary treatment for moyamoya, especially in the pediatric population.