John E. Wanebo and Robert F. Spetzler
This chapter describes the use of two branches of the superficial temporal artery for direct anastomotic bypass in patients with moyamoya disease. Although some surgeons routinely perform a double-barrel bypass, it is typically used when significant superficial temporal artery ischemia is found in addition to middle cerebral artery ischemia. The technical features of the procedure are explained, including the ideal manner of harvesting both superficial temporal artery branches while minimizing wound issues. How to identify the best recipient middle cerebral artery branches for anastomoses is also discussed. Finally, specific perioperative management protocols and complication avoidance as well as management are reviewed.
Keywords: Anastomoses, middle cerebral artery, moyamoya disease, superficial temporal artery have not had time to develop sufficient collateral vascularization on their own. Since such patients have inadequate cerebral blood flow and rapid disease progression, they need STA branches and recipient cortical MCA arteries of sufficient quality to allow for a double-limbed bypass.
At Barrow Neurological Institute, we evaluate the cerebral blood flow in moyamoya patients using computed tomography (CT) perfusion imaging before and after a 1-g acetazolamide vasodilatory challenge. Patients with symptomatic moyamoya disease who have impaired cerebrovascular reserve on a CT perfusion study upon vasodilatory challenge are candidates for revascularization. In most cases, a six-vessel cerebral angiogram is performed to document the stage of moyamoya disease and to demonstrate donor suitability of the STAs. Patients with severe hemispheric hypoperfusion, usually including both STA and ACA territories, are those typically chosen for two direct anastomoses (Fig. 10.1). The decision to
Since the first superficial temporal artery (STA) to middle cerebral artery (MCA) bypass pioneered by Donaghy and Yaargil et al in 1967, neurosurgeons have utilized multiple adaptations to augment cerebral blood flow.1,2 Reich- man was the first to use both STA branches in a bypass for ischemia in 1975. Sakamoto et al3 applied the technique of using two STA branches for the treatment of pediatric moyamoya disease in 1997. Ishikawa et al4 reported using one STA branch to revascularize the anterior cerebral artery (ACA) and the other for the MCA in 2005. Several reports from Hokkaido, Japan, describe large series of patients with moyamoya disease who routinely underwent a double-barrel bypass to the MCA cortical branches as part of a larger, combined, indirect revascularization procedure.5,6 At Barrow Neurological Institute, like other centers, we use a double-barrel bypass in select patients, including those with moyamoya disease, intracranial occlusive cerebrovascular disease, and complex aneurysms.7,8
The basic indication for a double-barrel bypass in the setting of moyamoya disease is severe hemispheric hypoperfusion. This circumstance is usually the case when both the MCA and the ACA are involved and frequently when patients have severe bilateral disease. Rapid progression of the clinical course of the patient also lends support to performing a double-barrel bypass because these patients construct a double-barrel bypass depends, in part, on the philosophy of the surgeon managing the case. Some surgeons would argue for using one STA branch for an indirect onlay instead of using both for direct anastomoses. Others contend that a single direct bypass is sufficient to revascularize a patient. No single best method has been proven. As with moyamoya treatment in most centers, the specific treatment, such as a double-barrel bypass, is chosen for a particular patient on the basis of the clinical condition and specific cerebral blood flow deficits of that patient.
The pattern of blood flow deficits on the CT perfusion scan and cerebral angiogram should guide the choice of the type of bypass. For a patient with broad hemispheric hypoperfusion, a double-limbed direct bypass with a frontal branch is used for the lower division of the MCA; above the sylvian fissure, the parietal STA branch is used for the upper MCA division. Since the posterior cerebral artery supply to the temporal lobe frequently augments the lower division MCA flow, it is common for the primary perfusion deficit to involve the upper MCA division; in such cases, both STA branches can be anastomosed to the cortical branches above the sylvian fissure. Although not used at our center, STA bypasses to both the MCA and ACA cortical branches remain options.4 In addition to the appropriate targeting of the recipient artery, careful preparation of the STA grafts is crucial.
• The double-barrel STA-MCA bypass provides immediate and robust cerebral blood flow to the ischemic hemisphere.
• The procedure is more complex and requires more operating time than single-vessel bypass.
• Theoretical disadvantage is loss of use of one STA branch for an indirect encephalo-duro-arterio- synangiosis (EDAS) bypass, potentially reducing longer- term revascularization.
• A potential improvement in the execution of a doublebarrel bypass would be the use of the cut flow index to assess the need for two grafts.9
• Use of two grafts might be more likely to cause hyperperfusion syndrome (not reported as a significant problem in one large series).6
• Two separate grafts might compete for blood flow, which could limit the benefit of a second graft or lead to an occlusion.
Moyamoya patients who have exceptionally small and fragile cortical MCA branches should not, and likely technically could not, undergo direct STA-MCA bypass. In clinical practice, this group represents about 10% of moyamoya patients who present for revascularization.
A careful review of any preoperative CT angiography (CTA) and digital subtraction angiography images is required to ensure that both the frontal and the parietal STA branches are of sufficient size and quality for bypass use. Potential recipient MCA branches should also be assessed.
The perioperative risk of stroke is 3 to 5% in most large series. Rates of significant hemorrhage are greater than 1%, but they do occur, given the use of antiplatelet treatment and the potential for hyperperfusion. Infection and wound healing complications are less than 1%. Headaches and cosmetic issues such as temporalis wasting remain a possibility.
10.8.1 Preoperative Workup
A cerebral blood flow study and a catheter cerebral angiogram or a CTA must be evaluated preoperatively. Since patients with moyamoya angiopathy can have associated blood dyscrasias, it is important to verify each patient’s response to antiplatelet therapy. We test patients to determine whether they are responsive to aspirin therapy (325 mg daily), which is our preferred antiplatelet agent before surgery and then for life. We avoid clopidogrel as an antiplatelet medication because of intraoperative bleeding issues. However, we did have a patient who did not respond to aspirin and who had a small stroke on discontinuation of clopidogrel. As a compromise, clopidogrel was withheld for 3 days prior to surgery, and the case proceeded without complication.
10.8.2 Patient Position
The patient is positioned supine with the head parallel to the floor and raised slightly above the heart. The courses of both the frontal and the parietal STA branches are insonated with Doppler ultrasonography and marked on the skin. The frontal STA is followed for at least 7 cm from its origin while the parietal branch is marked clear to the superior temporal line. The surgeon makes an incision along the parietal branch alone and shaves a 1-cm strip of hair along its path. An alternative incision is shaped like a hockey stick, with the parietal branch as the posterior limb and the second limb extending forward along the superior temporal line to the hairline. In addition to appropriate patient positioning, the proper instruments are critical to ensuring optimal technical results (Table 10.1, Fig. 10.2).
The anesthesiologist should have intravenous vasopressors and antihypertensives prepared for use before induction of anesthesia. Perhaps the single most important technique of surgery in these fragile patients is the maintenance of normal blood pressure, particularly during anesthesia induction. During temporary MCA occlusion, we routinely boost blood pressure to 10 mm Hg above baseline.
10.9.1 Skin Incision and Dissection of STA
The STA resides in the deep dermal layer, and we follow the course of the parietal branch of the STA for the skin incision. The microscope is used from the outset, and we start at the junction of the superior temporal line over the parietal STA branch, making a 2-cm-long incision in the epidermis down to the fat with a number 15 blade. The STA is found just deep to the dermal fat between the superficial temporal fascia and the galea (Fig. 10.3). The STA is dissected down to the zygoma, leaving a cuff of galeal tissue 5 mm on each side of the vessel. Small branches of the STA are cauterized 1 to 2 mm lateral to the main vessel with bipolar forceps set at 25 Malis units. This power level avoids injury to the STA.
The origin of the frontal branch of the STA, which is found 2 to 4 cm above the zygoma, is carefully preserved (Fig. 10.4). An assistant then elevates the anterior edge of the scalp flap with a handheld retractor, and the frontal STA branch is dissected for 5 to 7 cm (Fig. 10.5). Visualization of the frontal STA under the scalp is not difficult with angling of the microscope and, after temporary placement of a clip, it is divided obliquely at 5 to 7 cm. The STA is flushed with pure heparin, protected with a moist cotton sponge, and carefully retracted along with the posterior border of the scalp flap using fishhooks. The STA must remain moist and free of pressure or significant tension. The parietal STA branch remains in continuity since the decision for an EDAS has not been excluded prior to the cortical MCA evaluation.
10.9.2 Temporal Muscle Dissection and Craniotomy
The temporalis muscle is incised to the bone with the Bovie Force FX electrosurgery cautery unit (Covidien/ Medtronic, plc), with the incision extending from just above the zygoma to the superior temporal line. The temporalis muscle is carefully elevated anteriorly and posteriorly to expose a 5*5cm area of temporal and frontal bone junction, allowing for exposure of the MCA branches above and below the sylvian fissure. The temporalis muscle is carefully retracted with the scalp using fishhooks. A matchstick drill bit is used to create a large bur hole at the root of the zygoma to allow room for the STA passage, and a second bur hole 5 to 7 cm superior to the first that allows for an EDAS, if needed (Fig. 10.6). A bone flap centered 2 to 3 cm above the top of the ear to straddle the sylvian fissure is created. The STA is retracted away from the intended bone cuts for each side of the craniotomy. Careful bur holes allow for preservation of dural integrity and avoidance of damage to the middle meningeal artery (MMA) branches, which are important for collateral blood flow.
10.9.3 Dural Opening
The dura is opened along the course of one or two large MMA branches, leaving approximately a 5-mm strip of dura next to the MMA. Cruciate incisions of the dura horizontal to the bone edge create triangular flaps of dura; the dura is then inverted and tucked under the bone (Fig. 10.7). Preserving the MMA and the dural inversion maintains the collateral blood flow. The arachnoid membrane should be preserved, if possible, until the actual MCA dissection to minimize loss of cerebrospinal fluid, which can result in sagging of the brain.
10.9.4 Anastomotic Site Selection
The ideal cortical MCA recipient branches for anastomoses with the STA are 1.0 mm in diameter or larger and reside on the surface. MCA branches less than 0.7 mm in diameter are difficult to work with and provide less significant flow augmentation. Although surface MCA branches are easier to work with, dissection into a sulcus usually provides the advantage of a larger caliber vessel. For the double-barrel bypass, an MCA branch below the sylvian fissure is selected as a recipient for the frontal STA, and an MCA branch above the fissure is used for the parietal STA. Nonetheless, both anastomoses may be above or below the sylvian fissure, one anterior and one posterior if cerebral blood flow deficits support this pattern. Ideal recipient MCA branches near the bone edge can be accommodated with an additional small craniectomy. Cadaveric dissection of both the STA branches superimposed over the frontal and temporal lobes demonstrates the variety of cortical arterial branches, which can be reached by fully dissected STA branches (Fig. 10.8).
10.9.5 Donor STA Preparation
If possible, the frontal STA branch is prepared before opening the arachnoid membrane while the parietal STA remains intact. The frontal STA is flushed with pure heparin; a 30-degree blunt ophthalmic needle works well for flushing. The adventitia of the STA end is held by an assistant while the primary surgeon grasps the loose adventitia and dissects it sharply from the vessel to clear the distal 1 cm of the artery of adventitia. A single cut is made from the STA tip 3 mm along the barrel to create a fish-mouth opening in the vessel. A single cut avoids jagged vessel edges, and 3 mm creates a large opening three times the diameter of the recipient artery for blood flow (Fig. 10.9).
10.9.6 Recipient MCA Branch Preparation
The arachnoid membrane is sharply cut from a 10-mm segment of the target MCA branch; 10 mm allows extra room for the 3-mm opening in the STA donor artery and for temporary microaneurysm clips. Small perforating branches off the recipient MCA can be preserved, if they are large enough, with a temporary clip but are more commonly divided. Use of gentle bipolar cautery (settings of 25 W or less) at a safe distance (1-2 mm) from the MCA target branch helps protect the delicate lumen from injury or spasm. After the recipient branch is dissected, a colored triangular-shaped Silastic dam is placed under the artery, and 3 mm of cortical MCA is marked for the arteriotomy. A 3-French MicroVac suction catheter (PMT Corp., Chanhassen, MN) is placed under the Silastic dam to remove any pooling cerebrospinal fluid or blood (Fig. 10.10a).
10.9.7 MCA Arteriotomy
The patient is placed in electroencephalographic burst suppression by anesthesia, and systolic blood pressure of 10 mm Hg above baseline is verified. Low-pressure, temporary microaneurysm clips are applied to the MCA branch to maximize the space around the planned 3-mm arteriotomy (Fig. 10.10b). The MCA can be opened with an arachnoid knife or with the tip of a 27-gauge needle. Microscissors can then be used to extend the opening to exactly 3 mm. The vessel is flushed with pure heparin, and the edges of the opening are marked with either dye or a fresh skin marker. Adjustment of the temporary clips may be necessary if residual flow is noted, which sometimes requires a third microaneurysm clip. The assistant remains responsible for actively irrigating the lumens of both the STA and the MCA with heparinized saline.
For the anastomosis, 10-0 nylon precut to 5-cm lengths is used. The arteriotomies of both the STA and MCA are placed in opposition, and the first suture passes from the adventitia of the heel of the STA to the lumen and then from the lumen of the MCA to its adventitia side, where it is secured with three knots. The second suture again starts in the adventitia side of the STA but at its toe side, passing into the lumen and then into the MCA lumen and out the adventitia. Now the STA and MCA are nicely adjacent to each other (Fig. 10.11). The more difficult far limb of the anastomosis is typically done first, with three equally spaced interrupted sutures. The inside of the anastomosis is then inspected to ensure accurate suture placement. The second limb of the anastomosis is performed like the first. Although sutures can be done in one pass, a separate pass for each vessel wall maximizes accuracy.
An alternative to interrupted sutures is the continuous technique, with a series of 8 to 10 loops per limb. All loops are tightened before locking down the knot to the tail of the opposing suture.
10.9.9 Graded Release of the Temporary Clips and Hemostasis
Release of the clip on the distal MCA, which usually has the lowest blood flow, facilitates identification of any leaking areas of the anastomosis. Single interrupted sutures can address any leaks. The use of Surgicel (Ethi- con, Inc., Somerville, NJ) on the edges of the anastomosis also aids hemostasis. The proximal MCA clip is then released. Finally, the STA clip is released. The clips can be adjusted and released in such a way to allow for flushing of debris from the MCA out the parietal STA before the full release of the frontal STA (Fig. 10.12). An indocyanine green (ICG) angiogram is performed to ensure adequate flow through the anastomoses.
10.9.10 Second Anastomoses
A second anastomotic site is chosen above the sylvian fissure posterior to the frontal STA anastomoses. If a second site is not found, then the parietal STA branch can be sutured to the pia as an EDAS procedure. The second anastomosis is performed just like the first, with preparation of the STA and then the MCA recipient artery. A temporary clip is placed on the parietal branch STA beyond the frontal branch take-off (Fig. 10.13). A second ICG angiogram is performed to evaluate flow through both anastomoses (Fig. 10.14).
10.9.11 Closure Phase
The use of Gelfoam hemostat (Pfizer, Inc., New York, NY) under the bone flap should be avoided because of the potential for impairment of collateral revascularization. The bone flap is placed back in position and secured with plates, with sufficient room for passage of the STA inferiorly and superiorly, if needed. The temporalis closure allows for gaps at the inferior and superior end, if needed. The STA must not have significant compression. The galea is closed with 2-0 Vicryl sutures (Ethicon, Inc.), and the skin is closed with staples.
10.9.12 Postoperative Care
We monitor patients for 48 hours postoperatively in the neurosurgical intensive care unit with critical attention to tight blood pressure control, within the range of baseline blood pressure to 30 points above baseline, usually maintaining a systolic blood pressure of 120 to 150 mm Hg. Patients continue to receive daily antiplatelet medications. Postoperative CTA is performed later on the day of surgery. A repeat noncontrast CT is obtained the following morning to assess potential hemorrhaging. Hyperventilation must be avoided to minimize hypocapnia.
We repeat the CTA and CT perfusion studies 6 months after surgery and perform a catheter cerebral angiogram yearly for 3 years. A yearly CTA is performed thereafter.
During the procedures, either the frontal or parietal STA branch may be too short to reach recipient cortical arteries. The length of available STA should be assessed before the STA branch is cut. Additional length may be gained from dissection of the proximal STA in the region of the zygoma or distally at the ends of the parietal or frontal branches.
ICG angiography is performed after each anastomosis to confirm patency.10 If partial or total occlusion is noted at the anastomosis site, replacement of the temporary clips and removal of one or two sutures usually allows access to see the problem. Alternatively, flushing with pure heparin using a 27-gauge needle into the robust STA may clear any thrombus. This process might require a single suture to close the needle hole. If an STA branch is of poor quality, then it might be used as an onlay indirect bypass instead of for an anastomosis.
When setting up for the anastomoses, select the shorter graft for the lower division MCA bypass. After temporary clipping, ensure that there is no back-bleeding. Do not hesitate to adjust a temporary clip or add a second supporting clip to halt back-bleeding on the MCA or STA. However, avoid trapping a column of blood in the MCA or during CTA because doing so may lead to thrombosis. When performing the anastomoses, do the most difficult side first. If the recipient artery is near the bone edge, perform a small craniectomy to make the anastomoses easier. Compared to continuous suturing, interrupted sutures allow for fewer compound problems. However, interrupted sutures are more likely to leak, most commonly near the heel of the anastomosis. Placing sutures close to the heel stitch minimizes the chance of leakage. If the endothelium or the tip of the STA becomes damaged, recut the end in order to obtain a clean cut. If the MCA opening tears, the STA fish mouth may be enlarged to fit the opening.
Direct bypasses can be finicky procedures; therefore, do not rush the case. Be mindful to accurately execute the technical details of each step of the procedure. Repeating steps reduces the likelihood of success because of degradation of the arterial intima, thromboses, or fatigue. Simple technical errors can lead to bypass failure. Adherence to the procedural rules improves the likelihood of success. Placing temporary clips far enough from the anastomosis site requires some additional exposure, but the added room aids with suturing. Persistent filling of the MCA lumen due to incomplete occlusion by temporary clips impairs progress and increases the likelihood of thrombosis. Avoid the use of high bipolar cautery too close to the wall of the donor or recipient arteries. Finally, passage of the suturing needle through each arterial wall independently affords the most accurate suture placement during the anastomosis.
The importance of the surgical assistant cannot be overemphasized. Most centers involved with bypass surgery train residents or fellows who are eager for a chance to perform anastomoses. A key role for them is to keep the STA graft moist and the field free of blood by irrigating the exposed lumens with heparinized saline.
The authors thank Dr. Kaan Yagmurlu for his skillful cadaveric skull dissection used in the photograph for Fig. 10.8.
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