Surgical Techniques in Moyamoya Vasculopathy. Peter Vajkoczy

Chapter 16. Combined Direct (STA-MCA) and Indirect (EDAS) EC-IC Bypass

Erez Nossek, Annick Kronenburg, and David J. Langer


We espouse utilization of both the frontal and parietal branches of the superficial temporal artery (STA) when anatomically appropriate to treat symptomatic moyamoya disease (MMD) and syndrome (MMS). The frontal branch is used as the direct donor by performing an anastomosis with a cortical middle cerebral artery (MCA) artery, while the parietal branch is combined with dural reflections to create a large surface area of vascularized tissue for indirect revascularization. Patients are treated when they present with clear symptoms of ischemia or hemorrhage. Ischemic patients are exclusively treated when hemispheric blood flow testing demonstrates clear hypoperfusion. Asymptomatic hemispheres are only considered for treatment following successful treatment of a symptomatic contralateral hemisphere. MMD and MMS represent an uncommon but increasingly recognized cause of stroke in young and middle-aged adults in North America. Excellent outcome of treatment can be achieved by carefully selecting patients and maintaining a technical proficiency in the creation of both direct STA-MCA as well as indirect grafts for cerebral revascularization.

Keywords: moyamoya vasculopathy, cerebral revascularization, stroke, bypass

16.1 History and Initial Description

Extracranial-intracranial (EC-IC) bypass for the treatment of the symptomatic hypoperfused hemisphere in intracranial steno-occlusive diseases, secondary to atherosclerotic disease or moyamoya vasculopathy (MMV), is currently the treatment of choice.1,2 The use of a combined direct superficial temporal artery to middle cerebral artery (STA-MCA) and indirect encephalo-duro- arterio-synangiosis (EDAS), by performing an STA onlay with flipped dural flaps, is advocated as an optimal treatment option as it allows immediate augmentation of blood flow in the postoperative period, while providing the brain to acquire additional indirect flow in the long term.3 Dual placement of direct and indirect bypasses within the same hemisphere has been demonstrated by formal diagnostic angiogram, regardless of patients’ age and the hemodynamic status, to be of benefit with the indirect graft serving as an adjunct to a direct bypass in order to maximize revascularization.3 Quantitative magnetic resonance imaging (QMRI) studies have shown a reciprocal relationship between the direct and the indirect bypasses after combined bypass surgery, thus providing complementary revascularization.4

The STA is the terminal branch of the external carotid artery (ECA). It supplies the anterolateral part of the scalp. This artery usually (in 71.4-95.7% of the vessels) bifurcates above the level of the superior margin of the zygomatic arch. The mean inner diameter of the STA at the level of the zygomatic arch is approximately 2.2 to 2.7 ± 0.5 mm.5,6 The STA commonly bifurcates into an anterior frontal branch that courses anterosuperiorly and a posterior parietal branch that courses posterosuperiorly. The vessel however can be highly irregular in its anatomy and therefore its course must be studied angiographically preoperatively to insure adequate mapping of its trajectory (Fig. 16.1). The inner diameter of the frontal and parietal branches is approximately 1.4 to 2.1 and 1.4 to 1.8 at 7 cm respectively, distal to the zygomatic arch.6,7

16.2 Indications

The operative benefits of combined cerebral revascularization have been previously demonstrated with combined hemispheric revascularization shown to decrease rates of both ischemic and hemorrhagic stroke.8'9 Increased attention has also been directed at cognitive function, an important determinant of the quality of life, in patients with MMD. Cognition in MMD has been shown to be affected,10 possibly due to occult strokes, although it has also been shown in patients without stroke.11 Definitive benefits on cognition following revascularization have yet to be fully characterized. A recent systematic review concluded that combined cerebral revascularization was superior in producing favorable long-term clinical outcome.12 However, combining both techniques at the same procedure may be challenging and its nuances are critical for a good surgical and long-term outcome. In our previously published case series of patients treated with neurosurgical revascularization, the number of peri- and postoperative complications was acceptable, supporting evidence for the safety of these procedures in selected groups of patients.13 To favor optimal cerebral revascularization of the affected hemisphere, combined direct and indirect bypass therapy should become a standard treatment modality among vascular neurosurgeons when treating symptomatic MMV. Although little is known about the optimal timing of surgical intervention, we prefer not to perform revascularization surgery in the acute phase, which is in accordance with common practice.14 Patients presenting with hemorrhage are initially managed conservatively, with surgical consideration and radiographic workup performed following at least 2 to 3 months after recovery. Patients with transient ischemic attacks or those with small watershed ischemic infarction can be treated earlier following their full workup. Patients with larger recent infarctions are treated in more of a delayed fashion but usually within a month of their stroke, depending upon their neurological condition. We consider treating asymptomatic hemispheres in patients with bilateral MMV who have been revascularized on their symptomatic side, when there is evidence of hypoperfusion on cerebral hemodynamic studies.

16.3 Key Principles

The bypass procedure consists of (1) distal to proximal donor vessel preparation of the frontal STA branch (STAfb) for direct and the parietal STA branch (STApb) for indirect revascularization, followed by (2) a craniotomy in the region of interest (preferably a hypoperfused area as demonstrated on hemodynamic studies), (3) performing the anastomosis with a cortical M4 branch and verifying patency, (4) performing the EDAS, and (5) meticulous wound closure.

16.4 SWOT Analysis

• Strength: Bypass surgery is the only surgical therapy for MMD and MMS that carries a low complication risk and favorable clinical outcome.

 Weakness: Extensive surgical experience in bypass surgery and familiarity with the clinical key aspects of moyamoya are mandatory for successful treatment.

 Opportunity: Due to a low caseload, this surgical therapy is only performed in a few centers worldwide, which is creating an inadequate number of experienced treating facilities.

 Threat: Since the footprint of endovascular therapy is growing, fewer neurosurgeons are trained in microvascular surgery.

16.5 Contraindications

Surgery in patients who carry a high general anesthesia risk should be extensively studied and great care taken should be taken before recommending operative intervention. Asymptomatic moyamoya patients without hemodynamic compromise should not be operated on, but should be monitored over time instead. Bypass surgery in large infarcted areas should be avoided since it carries a great risk of intracerebral hemorrhage.

16.6 Special Considerations

16.6.1 Preoperative Considerations

MMV management requires a comprehensive workup including a directed medical history of the patient and physical examination. We study patients with MRI, quantitative magnetic resonance angiography (QMRA) by using noninvasive optimal vessel analysis software (NOVA; VasSol, River Forest, Chicago, IL) to assess cerebral blood flow, and single-photon emission computed tomography (CT) with and without acetazolamide to assess cerebral perfusion and vascular reserve. Conventional digital subtraction angiography (DSA) is utilized primarily in patients where treatment is being contemplated. A six-vessel DSA is performed as close to the planned surgical date as possible, since vascular anatomy can change over time in this dynamic disease. Preoperative angiographic assessment includes assessment of the specific course of the STA branches (Fig. 16.1) in order to evaluate and support successful harvesting of the donor artery. We discuss each pertinent finding with the patient and family and review the procedure step by step with our neurovascular team. We review the plan starting from hospital admission and continuing through preoperative preparation, the procedure itself, and the postoperative period. We believe that the well-educated patient familiar with all periprocedural details will achieve a better overall experience and outcome.

16.6.2 Postoperative Considerations

The first 24 hours postoperatively patients are admitted to an intensive care unit and special attention is paid to maintain normotension to ensure the patency of the bypass and to prevent hyperperfusion syndrome, which may cause temporary neurological deficits. A postoperative conventional CT angiography or DSA is performed to confirm bypass patency. In the illustrative case presented here, the postoperative angiogram at 6 months shows a robust flow through the both the STAfb direct bypass in to the MCA branches and the STApb continues to flow distal to the craniotomy site. We also perform QMRA in the immediate postoperative period. We continue to follow the patient both clinically and by QMRA at 3 months and DSA at 6 months follow-up (Fig. 16.2). The indirect graft is assessed and a contralateral “indirect only” surgery is considered on the asymptomatic hemisphere if robust collateral flow from the EDAS is seen on angiography. We maintain the patient on aspirin 81 mg per day unless there is a medical contraindication. Patients who have presented with hemorrhage have their aspirin stopped 3 months postoperatively.

16.7 Pitfalls, Risk Assessment, and Complications

An important complication of the procedure is graft thrombosis. Special attention must be paid to ensure anastomosis patency intraoperatively and postoperative secondary measures to prevent graft occlusion, such as maintaining normotension, normovolemia, and the administration of antiplatelet therapy (aspirin) is of importance. Bypass surgery should not be performed in large infarcted areas, since it carries the risk of intracerebral hemorrhage in damaged brain tissue. Wound healing problems and (low-grade) infections may occur at a higher rate due to diminished blood supply of the skin. With the careful selection of patients, morbidity and mortality rates in our and other centers12,13,15 have been acceptable and outweigh the possible complications of the procedure, especially since bypass surgery remains the only proven therapy for these patients.

16.8 Special Instructions, Position, and Anesthesia

Aspirin (325 mg) is administered the night before the procedure. In the perioperative period moyamoya patients are at risk of developing ischemia in a hypoperfused hemisphere during general anesthesia. This is of particular concern in patients with bilateral MMV. The following four principles are followed by an experienced neuroanesthesia team: normotension, normovolemia, normoventilation, and normothermia. Hyperventilation (causing cerebral vasoconstriction) and fluctuating blood pressures, which may cause watershed infarction, need to be avoided. Furthermore, hemoglobin and hematocrit levels need to be within the baseline levels. Mannitol and diuretic therapy should be avoided.

16.9 Patient Position with Skin Incision and Key Surgical Steps

16.9.1 Description of the Technique

We place the patient in supine position in a Sugita head frame with the head rotated contralateral to the treatment side without flexion or extension. The pinning of the calvarium should be done 7 cm posterior to the marked STApb in order to allow incision without any limitations, and especially for posterior retraction of the skin flap (Fig. 16.3). Following pinning, a hand-held Doppler is used to mark the course of both the anterior frontal branch of the STAfb and the STApb (Fig. 16.4). These branches are marked from their proximal bifurcation at the level of the tragus. The STApb is mapped distally up to 2 cm above the superior temporal line, and the STAfb distally up to the level of the frontal process of the zygomatic bone (“Key Hole”) at the anterior, superior margin of the temporal muscle.

Donor vessel dissection is performed under the microscope or exoscope. We start with the STApb dissection from distal to proximal in order to avoid proximal damage to the vessel. By using a blunt malleable brain retractor that is inserted into the subgaleal plane directly over the STA to dissect the STApb, it allows us to create a linear incision and concurrent protection of the STA in its bed.16

As we progress with the dissection, we place fish hooks over the skin flap anteriorly and posteriorly to allow for easier retraction and safer vessel dissection. We leave a periadventitial cuff along the vessels in order to avoid spasm of the vessel. We follow the vessel proximally to identify the bifurcation of the STA. At this level, veins may be adherent to the STA, which should not be mistaken for the STAfb and subsequently followed instead of the actual branch. We recommend a total length of 10 to 12 cm to be dissected to achieve good dissection of the vessel in order to prevent tension of the artery when covering the brain beneath the bone flap. The caliber of the STAfb is preferably at least 0.8 mm. Great care needs to be taken as the dissection extends to the origin of the STAfb proximally. The surface skin marking of the STAfb can serve as a target to identify the frontal branch origination point. At this point we continue the distal skin incision where we turn it anteriorly toward the mid pupillary line, an imaginary line extending from the pupil to the mid frontal region. The proximal part of the anterior limb of the skin incision should be carried with great attention not to damage the distal STApb (Fig. 16.5).

We elevate the skin flap anteriorly and dissect the STAfb from proximal toward its distal segment (Fig. 16.6). The dissection of the vessel is done within the subcutaneous tissue of the frontal skin flap utilizing tenotomy scissors and microforceps under the operating microscope. We dissect the STAfb distally beyond the level of the pterion and keyhole, where it lays over bone, at the superior edge of the temporal muscle (Fig. 16.7).

We retract the skin flap using fish hooks posteriorly, thus exposing the posterior part of the temporal muscle. The posterior cut of the temporal muscle is done at least 2 cm posterior to the STApb, and the muscle flap is elevated anteriorly under the two dissected vessels that are left in situ until the brain is exposed (Fig. 16.8). By tunneling the muscle beneath the frontal branch, the vessel is brought into the field prior to the craniotomy and does not have to be reaccessed during the course of the surgery as would be the case when rereflecting the temporal muscle (Fig. 16.9). The STAfb is marked in order to prevent twisted donor vessel (Fig. 16.10).

Two burr holes under the trajectory of STApb are created: one temporal and one parietal. These holes become the entry and exit points for the EDAS, and need to be in line with the anatomic course of the vessel. The craniotomy is performed through the burr hole to elevate a free round bone flap with diameter of approximately 4 cm (Fig. 16.11). Care must be taken not to damage the middle meningeal artery when serving an intracranial dural collateral during the craniotomy. The craniotome is used only in trajectories away from the vessels. The dura is then opened in a curved fashion and a flap is elevated anteriorly tunneled under the STAfb (Fig. 16.12).

The donor STAfb is then addressed. Preferably, a cortical M4 branch is chosen as a recipient for the direct bypass (Fig. 16.13). We measure the length of the vessel to verify that the transposition will reach the anastomosis site without tension by using a silk suture as measurement (Fig. 16.14, Fig. 16.15). The vessel is temporarily clipped as proximal as possible. The distal STAfb is cut and vessel fully heparinized. Coloring of the distal vessel with ink often helps to identify loose adventitial tissue that should be removed. The distal vessel is then fishmouthed. We measure the cut flow in the STAfb using the Charbel flow probe (Transonic Systems Inc. Ithaca, NY). The distal aspect of the STAfb utilized for the direct graft must be cleaned thoroughly by dissecting all distal periadventitial tissue over a length of 1.0 to 1.5 cm. We then proceed with the direct bypass as described in Chapter 2 (Fig. 16.16, Fig. 16.17, Fig. 16.18, Fig. 16.19, Fig. 16.20). We use 10-0 nylon with a BV 75-3 needle from Ethicon Surgical. We verify flow by using micro-Doppler (Mizuho Inc. Tokyo, Japan), measure cut flow index utilizing the Charbel flow probe and patency by using indocyanine green videoangiography.

With the bypass completed, we proceed with the EDAS: the STApb is laid over the cortex. Several openings of the arachnoid are created underlying the STApb in order to enhance spontaneous vascularization. The STApb cuff is sutured to the pia or dural edge with a 9-0 Ethilon nylon monofilament needle (BV130-5) to achieve fixation of the vessel over the cortex (2-3 sutures). This graft must be tension free and the vessel must lay loosely and with adequate contact to the brain surface. We then divide the dural flap into two flaps based on anterior pedicle to facilitate their flipping with their periosteal layer over the cortex (Fig. 16.21, Fig. 16.22).

We prepare the bone flap with enlargement of the burr hole sites to allow for the EDAS and direct graft vessels to enter and exit under the bone without compression or kinking. The temporalis muscle is closed with 2-0 vicryl. Very often the muscle itself is partially incised with a monopolar to avoid muscular compression of the two grafts. A submuscular drain is placed. The closure of the skin is performed with great attention especially at the penetrating site of the donor vessels under the bone flap. The skin is closed in layers with the subgaleal layer closed with 2-0 vicryl and the skin closed with a nylon stitch. We usually do no not use a subgaleal suture over the proximal STA, but prefer continuous nylon sutures of the skin. Care must be taken not to strangle the skin edges as the flap is at risk for wound healing problems due to reduced blood supply to the skin of the STA.

16.10 Difficulties Encountered

• Dissection of the STA branches may be difficult since small veins may cross the course of the arteries.

 The middle meningeal artery can be damaged during craniotomy (which may serve as an indirect transdural collateral).

 If the donor graft is not of adequate length, tension on the anastomosis may make the bypass impossible.

 Donor vessel spasm can occur. Generous use of papaverine-soaked Gelfoam and cottonoids may be of benefit.

 Opening of the arachnoid while performing the EDAS may cause small cortical bleedings from the typical cortical moyamoya vessels resulting in microinfarcts.

 Whenever the bone flap is not fitted to allow the graft vessels to enter and exit under the bone, the arteries may be compressed and occlude.

 During skin closure sutures may entangle or perforate the grafts possibly rendering them useless.

16.11 Bailout, Rescue, and Salvage Maneuvers

In case the STAfb is extensively damaged during the dissection, it may be considered to use the STApb for the direct procedure. Preoperatively the flow and patency of the anastomosis is verified. Whenever the graft is not patent, it has to be reopened to ensure that sutures are not misplaced and/or to inspect if blood clots are occluding the graft. To prevent puncturing of the direct graft during skin closure, a small surgical spatula can be placed covering and protecting the graft while suturing the cutaneous layer of the skin.

16.12 Tips, Pearls, and Lessons Learned

 Gain experience in a laboratory facilitating the training in microsurgical and anastomosis procedures.

 Besides mastering the technical skills, it is of importance to familiarize with all aspects of this rare disease to optimize clinical outcome in this group of patients.

 The right indication and patient selection has as much if not more to do with the success of the procedure than the physical performance of the surgery. “Far more patients suffer form poor indication rather than poor operation.”


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