Alessandro Narducci and Peter Vajkoczy
Superficial temporal artery (STA) to middle cerebral artery (MCA) bypass is one of the most widespread techniques to provide blood supply from external carotid to intracranial circulation. The procedure contemplates the microsurgical dissection of an STA branch in the scalp (donor vessel) and of a cortical MCA branch (recipient vessel) near to the end of Sylvian fissure, and their subsequent anastomosis. It represents a universal indication for moyamoya disease, since it lowers the risk of ischemic and hemorrhagic strokes, due to the immediate revascularization provided. For technical feasibility, the size of vessels to anastomose should not be inferior to 1 mm; thus, in pediatric patients, the procedure can be sometimes difficult or impossible.
The performance of this bypass requires specialized training and experience with the use of microvascular techniques. It is mandatory for a careful preoperative assessment (i.e., digital subtraction angiography, coagulation, and platelet function tests), as well as meticulous intraoperative attention to technical details because the risk of postoperative neurological deficits, hemorrhages, and ischemic stroke is non-negligible.
The major contraindication to STA-MCA bypass is represented by the presence of acute stroke; in such case it is recommended to postpone the procedure for a few weeks.
In this chapter we provide a detailed description of the surgical technique and patient care, basing on evidence and high-volume experience.
Keywords: moyamoya disease, bypass, superficial temporal artery, middle cerebral artery, direct revascularization, microvascular anastomosis
Superficial temporal artery (STA) to middle cerebral artery (MCA) nowadays represents an established technique for flow augmentation in chronic cerebral ischemic diseases. Yasargil was the first who described this procedure after technical development of microvascular anastomosis in dogs. He performed the first STA-MCA bypass in a human in 1967 to treat a patient with complete MCA occlusion,1 carrying out an end-to-side anastomosis between a distal branch of STA and a cortical branch of MCA near the sylvian fissure. Variations of this procedure have been described, such as end-to-end anastomosis and double-limb STA-MCA grafts, but the original technique is still the most widespread.
One of the first applications in moyamoya disease was reported in 1980, by Holbach and coworkers, on a 41- year-old Libyan woman.2 The authors evaluated the usefulness of direct revascularization through postoperative EEG (electroencephalography), which showed an “increase in the electrical brain activity.”2 The effectiveness of this procedure has been afterward evaluated through flow measurement tools3 and imaging, such as magnetic resonance (MR) angiography,4 even if angiography provided the clearest evidence in terms of improvement of intracranial circulation following bypass.
The value of STA-MCA bypass in moyamoya disease has been unclear for a long time, due to the scarcity of large series with long-term follow-up and the presence of patients largely treated with indirect revascularization techniques. In 2009, Steinberg and coworkers5 reported a large cohort of patients with moyamoya treated at Stanford University, describing the benefit of direct bypass in terms of prevention of ischemic events and improvement of life quality.
Several studies have subsequently confirmed these findings and at present, STA-MCA bypass is well recognized as a useful treatment approach for moyamoya patients.
STA-MCA bypass, compared to indirect revascularization techniques, provides a great advantage of immediately increasing the blood flow in chronic hypoperfused brain. Its protective effect has been demonstrated both for ischemic and hemorrhagic moyamoya disease6 because it implies a double result: improvement of cerebral perfusion and reduction of hemodynamic stress on collateral fragile moyamoya vessels, usually very prone to rupture. Medium term follow-up studies showed that the incidence of both ischemic and hemorrhagic strokes decreases, making STA-MCA bypass a universal indication for moyamoya disease, when technically feasible. The size of the vessels represents, in fact, the most important feature in decision making because a diameter of less than 1 mm makes the anastomosis technically difficult or even impossible. It is therefore deductible that in pediatric patients, indirect revascularization is sometimes the sole practicable surgical option.
Preoperative digital subtraction angiography (DSA) is the gold standard in assessing the caliber of STA;
nevertheless, the surgeon must keep in mind that, sometimes, the existent size of parietal and frontal branches observable during surgery is superior to the one expected according to imaging.
The classic and most widespread technique for STA-MCA bypass consists in performing a direct end-to-side anastomosis of one STA distal branch (parietal or frontal) with a cortical M3 branch, exposed through a small craniotomy ideally targeted on the distal portion of the sylvian fissure. The selection of the most prominent STA branch as well as an appropriate antiplatelet management are milestones for success.
• Immediate revascularization with subsequent immediate protection against stroke.
• Working horse of bypass surgery.
• Universally applicable.
• Proven efficacy against both ischemic and hemorrhagic strokes.
• Technical complexity (good microsurgical skills required).
• Risk of intraoperative and postoperative graft occlusion.
• Risk of postoperative hyperperfision.
• Further reduction of invasiveness (navigation, augmented reality).
• Poor quality of vessels.
• Risk of hyperperfusion.
• Involvement of posterior cerebral artery in the disease.
Contraindications are few but significant. First, the presence of acute stroke with large restricted signal in diffusion weighted imaging represents a major contraindication; performing the procedure at least 6 weeks after the stroke can be considered safe. Second, it is possible that none of STA branches is suitable as a donor vessel or the artery is absent for different reasons (i.e., previous surgery); in this situation, alternative techniques must be considered. Lastly, the presence of substantial contribution to collateralization from STA needs to be evaluated in each patient prior surgery, weighting risks and benefits of the procedure.
9.6.1 Preoperative Imaging
Preoperative imaging studies are fundamental for planning the correct strategy and include computed tomography (CT) scan, MR imaging, as well as six-vessel cerebral angiography. Lateral external carotid angiogram allows the evaluation of diameter, course, and tortuosity of STA, so that the prominent branch can be used as a donor vessel; it also provides information helpful in avoiding unexpected anatomical variations that can be encountered (i.e., atresia of parietal branch).
Optimal anticoagulation and antiplatelet therapy is still a matter of debate. Preoperative single dose of aspirin (100 mg) or clopidogrel (75 mg) or intraoperative administration of a bolus of aspirin seems to have no effect in increasing hemorrhagic risk; nevertheless, their efficacy in improving outcome is still unknown. Similar evidence regards administration of low molecular weight heparin. On the other hand, postoperative use of a single antiplatelet agent (aspirin 100 mg or clopidogrel 75 mg) is correlated with improved outcome, without increasing hemorrhagic risk. Double antiplatelet therapy does not offer additional benefits. Tests for platelet function and individual resistance to antiplatelet drugs can provide useful information for the best management.
9.6.3 Other Considerations
The concomitant exposure of both intracranial and extracranial vasculature gives the chance to perform further studies (i.e., evaluation of moyamoya-like change in external carotid circulation) by means of vessel biopsy (STAorMCA).
STA-MCA bypass carries non-negligible risk of complications. Steinberg and coworkers, in their large cohort, experienced postprocedural hemorrhagic strokes in 1.8% of treated patients, as well as 3.5% of neurological deficits. Schubert et al7 reported an incidence of 8.5% of perioperative ischemic strokes, and a revision rate of 3.1%. General risks (i.e., infections, cerebrospinal fluid leak) are comparable to other neurosurgical procedures.
No special measures are required in terms of positioning and anesthesia, except for optimal intraoperative blood pressure management, since hypertension can be associated with decrease in bypass patency. Local anesthesia should be avoided, as it carries the risk of STA vasoconstriction or injuries.
The patient is placed in supine position with the ipsilateral shoulder elevated. The head, fixed by a Mayfield head holder, is rotated with almost 90 degrees to the opposite side, in such a way as to have the surgical field parallel to the floor. The donor vessel can be identified by palpation or with the aid of Doppler ultrasound, if needed. According with the STA branch chosen, the skin is marked directly along the course of the vessel (Fig. 9.1). The craniotomy should be centered over the distal portion of the sylvian fissure. This relatively confined area, where several MCA branches emerge (Fig. 9.2), is located
approximately 6 cm above the external auditory canal. In our institution, for optimal location of craniotomy, we use a special designed template8 (Fig. 9.3), which allows the identification of the end of sylvian fissure with high accuracy. In our experience, a 3 cm craniotomy around the target point is sufficient to expose at least one suitable recipient MCA branch.
9.9.2 Surgical Technique
Donor Vessel Isolation
All surgical steps described are performed under microscope magnification. Isolation of donor vessel starts with incision through the skin and dermal fat. The initial steps carry the highest risk of STA injury; for this reason, it is advisable to begin the dissection distally, since if injury occurs, a substantial portion of vessel is still intact. Once STA is identified, a careful dissection is performed, cauterizing the side branches and releasing the artery from the surrounding tissue (Fig. 9.4). Mechanical vasospasm is avoided by leaving a connective tissue cuff around the artery, which protects it from excessive manipulation and damage (Fig. 9.5).
In cases in which parietal branch is used as a donor vessel, only 1 linear skin incision is needed, as it usually runs slightly in front of the target point for craniotomy, into the parietal scalp region (Fig. 9.1c, d). On the other hand, when frontal branch is prominent and more suitable as a donor vessel, we use a double-skin incision technique (Fig. 9.1a, b). A first linear cut is performed, starting in front of the ear and extending along the course of the artery into the lateral forehead. Next, a separate second 5 cm skin incision is made over the target point of craniotomy (Fig. 9.6). After a sufficient length of artery is isolated, it is divided, distally clamped with a temporary clip, and subsequently tunneled under the skin which separates the two incisions, in order to reach the operative field. The donor vessel is then placed between cottonoids wet with papaverine.
Craniotomy and Recipient Vessel Preparation
A 3 cm craniotomy is performed after division and lateral retraction of the temporalis muscle. It is advisable to place the burr hole caudally, in order to allow the passage of STA after bone flap replacement (Fig. 9.7). The dura is opened in a U-shaped fashion, and turned cranially (Fig. 9.8).
The cortical surface is inspected to identify the most suitable recipient vessel. It is important to select the most prominent one, evaluating also the absence of major side branches. After opening the arachnoid, minor collaterals can be sacrificed without sequelae, in order to release tethering of M3 branch to cerebral cortex (Fig. 9.9). After preparation of the recipient vessel, the cuff of connective tissue surrounding the distal end of STA is meticulously removed, and the vessel is irrigated with heparinized saline to prevent clot formation. The distal end is cut in oblique form and fish mouthed; this is fundamental because it allows obtaining a 4-times increase of cross-sectional area, so that the blood flow is ensured even if the anastomosis will provoke some degree of stenosis. The donor vessel should be adapted to the appropriate length in order to minimize intravascular resistance but at the same time ensure enough redundancy without tension.
A triangular-shaped plastic pad is placed under the recipient vessel and small arteriovenous malformation (AVM) clips are applied at a distance of about 5 mm to interrupt the blood flow within the recipient artery (Fig. 9.10).
Arteriotomy can be performed in different ways. We place a 10-0 nylon stitch on the arterial wall parallel to the vessel course—this allows exerting a moderate traction in order to perform an easier arteriotomy using microscissors. The length of arteriotomy should ideally be twice the diameter of the recipient vessel, and match with the fish-mouthed donor vessel.
A 10-0 nylon microsuture is used to perform the anastomosis. The heel of the fish mouth is sawn to one of the two ends of the recipient artery, considering the flow direction (Fig. 9.11). The toe of the donor vessel is then sutured to the second end of arteriotomy. Next, it is possible to start suturing the two walls, using interrupted or running technique. Suturing the back wall is more difficult, so it is advisable to perform it first (Fig. 9.12); moreover, this strategy makes it possible to double-check the correct placement of sutures from the open front wall.
After completion of the anastomosis, the clips are removed from recipient and donor vessels; during this step, some bleeding is commonly observable and somehow auspicable, witnessing the presence of blood flow. Small amount of bleeding is easily controlled applying cottonoids on the anastomosis with gentle pressure, and with the apposition of Surgicel or Gelfoam. Significant leaks can be closed with additional sutures. Direct revascularization can be supplemented with encephalo-duro- synangiosis, underturning the dural flap over the cortical surface; the remaining gap can be filled with a layer of Gelfoam (Fig. 9.13).
Patency of the graft is intraoperatively assessed using different tools, such as indocyanine green videoangiography, micro Doppler probes, and DSA.
During closure, it is fundamental to allow graft to pass safely through the burr hole (Fig. 9.14), and avoid too tight closure of muscle, potentially leading to compressive effects and stenosis of STA. The graft is inspected for kinking or compression during all phases of the closure.
Preparation of donor vessel
1. Injury of STA branch
2. Low cut-flow in the STA/ intraoperative STA occlusion
1. Absence of adequate recipient vessel in the exposed field
1. Short STA branch
2. Intraoperative detection of nonfunctioning bypass
9.11 Bailout, Rescue, and Salvage Maneuvers
If the STA injury is small and clearly identifiable, it can be sutured, even if the vessel is completely broken off, performing an end-to-end reconstruction; conversely, if the damage is not recoverable, the use of the other branch needs to be considered.
Irrigation with heparinized saline can prevent or resolve clot formation, while the use of papaverine and hydrostatic dilation through saline flushing can decrease vasospasm.
Craniotomy must be enlarged in cases in which no adequate recipient vessels are detected in the surgical field. In case of short STA, it is possible to remedy, identifying a more proximal recipient vessel, splitting the sylvian fissure and using an infrasylvian recipient.
In cases of nonfunctioning bypass, it is mandatory a revision of anastomosis or, eventually, redo it choosing a different recipient vessel.
For a successful STA-MCA bypass, some precautions are of basic importance in preventing minimal and severe complications.
9.12.1 Preoperative Evaluations
Identification of hypercoagulable states, evaluation of coagulation parameters, as well as platelet function tests help to avoid thrombotic or hemorrhagic complications, which can badly affect the outcome.
Preoperative evaluation of STA course and detection of variation can alert the surgeon to a more mindful dissection, especially in case of tortuous artery, lowering the risk of injury.
9.12.2 Technical Tips
Minimizing skin incision decreases the incidence of wound-related problems, with a linear cut along the course of donor vessel. As mentioned earlier, it is safer to perform a distal to proximal dissection.
The distal portion of sylvian fissure (6 cm above the external auditory canal) represents an optimal location for craniotomy; adjunctive tools (i.e., navigation, augmented reality) could further increase the accuracy.
During anastomosis, it is fundamental to avoid excessive handling of arterial edges.
Marking the margins of donor and recipient arteries with ink, as well as keeping the surgical field dry and bloodless, improve visualization during suturing process. This is of particular importance in moyamoya disease, in which the thin wall of vessels may lead to collapse and difficult identification of arteriotomy edges.
Interrupted and running techniques for anastomosis provide the same level of efficacy, even if the latter is less time consuming. It is anyway advisable for beginners to start with interrupted technique because it allows fixing and redoing every single suture. Performing a running suture, in fact, requires a solid experience, since uncontrolled and unintentional movements may tear off the whole anastomosis.
Vasospasm is a common event during the procedure, particularly affecting recipient vessels: the frequent use of papaverine during all steps is helpful in tackling this issue.
Besides the strategies described in the previous paragraph to achieve a good final hemostasis at the suture line, a muscle patch could be helpful in the most troublesome cases. It is important to keep in mind that attempts in coagulation can lead to definitive opening.
In case of intraoperative detection of bypass failure, redo the anastomosis is safer than revising it, as revision carries higher risk of long-term occlusion.
9.12.3 Postoperative Care
STA-MCA bypass needs postoperative low intensity monitoring. One night in the intensive care is sufficient for adult patients, 48 hours for pediatric patients. The most important parameter to monitor is blood pressure, in order to avoid early graft failure (hypotension) or leakage from anastomosis leading to subdural hematoma (hypertension). Lowering the blood pressure is also important in management of postoperative hyperperfusion.
Postoperative radiological assessment contemplates CT scan to evaluate the presence of hemorrhagic complications, and DSA to assess bypass function.
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