Surgical Techniques in Moyamoya Vasculopathy. Peter Vajkoczy

Chapter 17. STA-MCA Anastomosis and EDMAPS

Satoshi Kuroda


Superficial temporal artery to middle cerebral artery (STA-MCA) anastomosis and encephalo-duro-myo-arterio-pericranial synangiosis (EDMAPS) is one of the combined bypasses for moyamoya disease. The novel indirect bypass, EDMAPS enables us to most widely cover the frontal lobe by using the vascularized frontal pericranium. This technique can provide collateral blood flow to almost the entire territory of the internal carotid artery, including the anterior cerebral artery. Thus, STA-MCA anastomosis and EDMAPS may be named as an “ultimate” bypass for moyamoya disease. In this chapter, the author introduces the concept, surgical technique, and pitfalls of STA-MCA anastomosis and EDMAPS for moyamoya disease.

Keywords: moyamoya disease, STA-MCA anastomosis, EDMAPS, ultimate bypass

17.1 History and Initial Description

17.1.1 STA-MCA Anastomosis and EDMAPS as an “Ultimate” Bypass

Fig. 17.1 shows the historical flow of bypass surgery for moyamoya disease at Hokkaido University Hospital. Nakagawa et al established encephalo-myo-arterio- synangiosis (EMAS) in the early 1980s. The temporal muscle and superficial temporal artery (STA) were used as the donor for indirect bypass.1 However, the incidence of perioperative ischemic complications was not low.Subsequent studies also showed that cerebral hemodynamics was impaired in the frontal lobe even several years after surgery.3 At that time, STA-MCA (middle cerebral artery) single or double anastomosis was routinely performed, and craniotomy was extended to the frontal area in order to further supply collateral blood to the frontal lobe in the late 1980s. The temporal muscle, STA, and dura mater were utilized as the donor for indirect bypass, called as encephalo-duro-myo-arterio-synangiosis (EDAMS). As a result, the incidence of perioperative ischemic stroke markedly decreased probably because of immediate improvement of blood flow after direct bypass.2,4 Postoperative blood flow studies revealed significant improvement of cerebral hemodynamics in the frontal lobe after STA-MCA anastomosis and EDAMS. Intellectual outcome significantly improved in pediatric patients.5 However, about 10% of pediatric patients still experienced paraplegic transient ischemic attack (TIA) even after surgery probably because the temporal muscle, a main donor tissue for indirect bypass, covers mainly the MCA territory. Hemorrhagic stroke also recurred in about 20% of adult patients even after STA-MCA anastomosis and EDAMS.6

Based on these historical observations, Kuroda et al performed STA-MCA single or double anastomosis and extended craniotomy to the medial frontal area to further improve cerebral hemodynamics in the anterior cerebral artery (ACA) territory in the late 1990s. The frontal pericranial flap was used to widely cover the medial frontal lobe in addition to the temporal muscle, STA, and dura mater. A pericranial flap has been widely used to reconstruct the anterior cranial fossa because of its simplicity, reliability, and low morbidity. As reported by Yoshioka and Rhoton, the frontal pericranium receives blood flow mainly from the supraorbital and supratrochlear arteries arising from the ophthalmic artery.7 The indirect bypass procedure was named as encephalo-duro-myo-arterio- pericranial synangiosis (EDMAPS). As a result, no pediatric patients have experienced paraplegic TIA after surgery. Clinical results strongly suggest that the incidence of recurrent hemorrhagic stroke is much lower than before.8 Now, we are routinely performing STA-MCA anastomosis and EDMAPS for patients with moyamoya disease. Very recently, we evaluated cumulative incidence of late morbidity/mortality among 93 patients who underwent STA-MCA anastomosis and EDMAPS and were followed up for longer than 5 years post-surgery (mean, 10.5 ± 4.4 years). As per results, 92 of 93 patients were free from any stroke or death, but one recurred hemorrhagic stroke during follow-up periods (0.10% per patient-year, submitted data). Therefore, we believe that STA-MCA anastomosis and EDMAPS would be the best choice to prevent further cerebrovascular events for longer than 10 years by widely providing surgical collaterals to both MCA and ACA territories. In this chapter, therefore, the author describes the concept, surgical procedures, pitfalls, risk, and perioperative managements of STA-MCA anastomosis and EDMAPS.

17.2 Indicationsand Contraindications

Direct bypass procedures can quickly improve cerebral hemodynamics after surgery, and thus can significantly lower the incidence of perioperative ischemic events, including TIA and ischemic stroke.1 Furthermore, TIA and/or headache attack quickly decreases in frequency or disappears during follow-up periods after direct bypass procedure. These clinical results of direct bypass are supported by immediate blood flow improvement just after surgery.2,3 The procedures can flexibly be modified as STA-anterior cerebral artery (ACA) or STA-posterior cerebral artery (PCA) anastomosis according to patients’ condition, such as dense ischemia in the territory of the ACA or PCA.4 However, surgical procedure for direct bypass requires skillful technique and thus a certain surgical training, because the recipients have a small caliber (0.51.0 mm in diameter) and more importantly a very thin wall in a majority of patients with moyamoya disease. In addition, it should be reminded that direct bypass procedure would carry the risk for postoperative hyperperfusion, which sometime causes severe neurological sequelae and/or mortality unless appropriate managements are indicated (see Fig. 17.1).5 On the other hand, indirect bypass procedures are technically simple and easy, because the vascularized donor tissues are only put onto the surface of the brain. Surprisingly, an aggressive neovascularization occurs between the donor tissues and the brain and start to provide collateral blood flow to the ischemic brain in moyamoya disease. However, indirect bypass may increase the incidence of perioperative TIA and/or ischemic stroke especially in patients with dense ischemia before surgery, because the neovascularization requires 3 to 4 months to establish collateral blood flow.2,6 It is well known that surgical collaterals develop in almost all pediatric patients, although previous reports have shown that efficient surgical collaterals develop through indirect bypass in about 50 to 70% of adult patients with moyamoya disease.7 Furthermore, surgeons should be aware that the extent of craniotomy largely determined the extent of surgical collaterals through indirect bypass. As aforementioned, it is well known that cerebral ischemia is most dense in the frontal lobe, thus craniotomy for indirect bypass should widely be extended to the frontal area.

Table 17.1 Indirect bypass versus direct bypass




Indirect bypass

• Simple and easy

• Surgical collaterals develop 2 to 3 months postsurgery

• Higher incidence of perioperative ischemic stroke

• Effective in only 50% of adults

Direct bypass

• CBF improves just after surgery

• Lower incidence of perioperative ischemic stroke

• TIA quickly disappears

• Surgical training needed

•Possibility of hyperperfusion

Combination of direct and indirect bypass may be the best choice for moyamoya disease because an immediate supply of collateral blood flow can compensate for the shortcoming of indirect bypass. Indirect bypass often functions as a major source of surgical collaterals in a certain subgroup of patients even after combined bypass procedure in a majority of pediatric patients and a certain subgroup of adult patients. Thus, reciprocal STA regression occurs in about 30% of the hemispheres during the transition from the postoperative acute phase to the chronic phase during indirect bypass development.7

17.2.1 Asymptomatic Moyamoya Disease

Recent studies have shown that the prevalence of asymptomatic moyamoya disease is much higher than considered before. Based on the exhaustive survey in Hokkaido Island, Japan, about 20% of patients with newly diagnosed moyamoya disease were asymptomatic.9 Although the natural course of asymptomatic moyamoya disease is not fully understood, previous nation-wide observational study in Japan revealed that the annual risk of any cerebrovascular events and stroke was 5.7 and 3.2%, respectively. Disturbed cerebral hemodynamics at initial diagnosis was significantly linked to ischemic episodes. Disease progression during follow-up periods also highly caused ischemic cerebrovascular episodes. However, the cohort of this study was small (n = 34).10 Therefore, the Research Committee on Moyamoya Disease in Japan started a prospective multicenter, nation-wide observational study, called as Asymptomatic Moyamoya Registry (AMORE) in January 2012 to further clarify the epidemiology, pathophysiology, and prognosis in asymptomatic moyamoya disease. As a result, a total of 109 subjects were enrolled during 4 years, and they were carefully followed-up for 5 years. Therefore, the author believes that no bypass surgery should be indicated for asymptomatic moyamoya disease at least until AMORE study reaches any conclusion in 2020.11

17.2.2 Ischemic-Tpe Moyamoya Disease

There are no effective medical therapies to reduce or prevent further TIA and/or ischemic stroke in moyamoya disease. Importantly, the physicians should be aware that headache attack is closely related to cerebral ischemia and should be recognized as one symptom of TIA in pediatric moyamoya disease. Most of “symptomatic” hemispheres have disturbed cerebral hemodynamics in the territory of internal carotid artery (ICA) due to the reduction of cerebral perfusion pressure (CPP), which is characterized by the most severe ischemia in the frontal lobes. In addition, the involvement of the posterior cerebral artery (PCA) may often impair cerebral hemodynamics in the occipital lobe.

When determining the indication of bypass surgery for moyamoya disease, it is quite valuable to assess the CPP by measuring cerebral blood flow (CBF) before and after intravenous injection of acetazolamide using single photon emission computed tomography (SPECT), positron emission tomography (PET), or cold xenon CT. Reduced reactivity to acetazolamide would be a key finding to identify the reduced CPP in the involved hemispheres. Therefore, STA- MCA anastomosis and EDMAPS should be indicated to the “symptomatic” hemispheres of both pediatric and adult patients who experienced TIA and/or ischemic stroke.8

17.2.3 Hemorrhagic-Type Moyamoya Disease

For a long time, it remained to be debated whether surgical revascularization would reduce the incidence of recurrent hemorrhagic stroke in adult patients with moyamoya disease. Recently, however, Japan Adult Moya- moya (JAM) Trial Group has shown that direct or combined bypass could significantly reduce it in adult patients who developed hemorrhagic stroke due to bilateral-type moyamoya disease within 6 months after the onset.12

17.3 Key Principles

STA-MCA anastomosis combined with EDMAPS can quickly improve cerebral hemodynamics through direct bypass procedure and can widely improve it through indirect bypass that entirely covers the involved hemisphere by using the whole vascularized donor tissues around the head, including the artery, dura, muscle and pericranium. Our 20-year experience has proved that this procedure can markedly reduce any further stroke for up to 20 years after surgery.

17.4 SWOT Analysis

 Strengths: STA-MCA anastomosis combined with EDMAPS quickly improves cerebral hemodynamics through direct bypass procedure and widely improves it through indirect bypass that entirely covers the involved hemisphere by using the whole vascularized donor tissues around the head, including the artery, dura, muscle and pericranium. In addition, this procedure can markedly reduce any further stroke for up to 20 years after surgery.

 Weakness: Only well-trained or experienced surgeons are allowed to perform this procedure in order to minimize the incidence of surgical and/or perioperative complications.

 Opportunities and Threats: Refer to the detailed description under Chapter 17.2.

17.5 Special Considerations

As described in Chapter 3, CBF measurement is essential to determine the surgical design, including the extent of craniotomy and the recipient. Especially, craniotomy and dural opening should be planned to cover the frontal lobe as widely as possible, because the frontal lobe is severely exposed to cerebral ischemia in moyamoya disease. Indeed, intellectual outcome is significantly poor in pediatric patients who underwent surgical revascularization through a small craniotomy that does not cover the frontal lobe.

It is still determined whether the antiplatelets or anticoagulants would be useful to reduce the frequency of ischemic attacks or the incidence of perioperative complications, including ischemic stroke and graft occlusion. However, the author never uses either of them because TIA and ischemic stroke occur due to hemodynamic compromise, but not artery-to-artery embolism. Furthermore, adult patients are at high risk for hemorrhagic stroke before and even after surgical revascularization.

17.6 Pitfalls, Risk Assessment, and Complications

As reported previously, STA-MCA anastomosis and EDMAPS may carry perioperative complications with 3-month morbidity of 4.3%. No mortality is recorded in our institute.8 Therefore, the author informs the patients and their family that surgical risk of STA-MCA anastomosis and EDMAPS is around 5% according to his 20-year experience, but may be higher in patients with frequent ischemia attach and/or dense ischemia.

17.7 Special Instructions and Anesthesia

All patients should receive intravenous drip (500 to 1,000 mL) overnight before surgery to avoid ischemic complications during and after surgery. After induction of general anesthesia, PaCO2 is strictly maintained around 40 mm Hg.8

The skin incision is then made along the course of the parietal branch of the STA (Fig. 17.3, Fig. 17.4). The parietal branch of the STA was dissected from the surrounding tissues, being kept patent at the point where the STA crosses the skin incision, so that the patency can be preserved just before STA-MCA anastomosis. After the scalp flap was reflected laterally, the frontal branch of the STA was also dissected under a surgical microscope (Fig. 17.5). The vascularized frontal pericranial flap, consisting of the cranium periosteum and the overlying loose areolar layer, is created for subsequent encephalo- pericranio-synangiosis (Fig. 17.6). Then, the temporal muscle was dissected as widely as possible and was made as a vascularized flap for encephalo-myo-synangiosis (EMS). Careful dissection is essential to preserve the arterial and venous pedicles of the muscular and pericranial flaps (Fig. 17.6).

17.8 Patient Position with Skin Incision and Key Surgical Steps

17.8.1 Skin Incision and Donor Tissue Preparation

Refer to Fig. 17.2 for a design of skin incision. The patients are placed in the supine position and their head is fixed with a three-point fixation device. The course of the STA is identified with a Doppler ultrasound probe.

17.8.2 Craniotomy and Dural Opening

A frontotemporal craniotomy extending into the frontal area is made, preserving the middle meningeal artery (MMA). The size of craniotomy should be extended to the frontal area as widely as possible (Fig. 17.7). The dura is incised and rolled back, preserving the main branches of the MMA. Thorough hemostasis is essential for direct STA-MCA anastomosis (Fig. 17.7).

17.8.3 Direct STA-MCA Anastomosis

STA-MCA single or double anastomosis is performed in an end-to-side fashion with 10- or 11-0 nylon threads. The author prefers 11-0 nylon threads for pediatric patients younger than 10 years and 10-0 nylon threads for adolescent and adult patients. The frontal branches of the MCA should be selected as the first recipients of anastomoses in every case, because cerebral hemodynamics is impaired especially in the frontal lobe in moya- moya disease. The second recipient should be the cortical branch of the MCA that is feeding the temporal lobe. The diameter of the recipients ranges from 0.5 to 1.1 mm. The wall of the recipients is also very thin. The blue dye is put onto the surface of cut ends of the donor and recipient to visualize them clearly. A green silicon sheet is inserted beneath the recipient for the same purpose. Usually, 12 to 14 sutures would be enough to complete STA-MCA anastomosis. The clamping time of recipient is approximately 20 to 30 minutes (Fig. 17.8). Indocyanine green (ICG) videoangiography is quite useful to confirm the patency of STA-MCA anastomosis and also the MMA (Fig. 17.9).

17.8.4 Indirect Bypass and Cranioplasty

The dural flaps are turned into the epiarachnoid space for the development of surgical collaterals between the outer surface of the dura and the brain (encephalo-duro-synangiosis [EDS]). Then, the dural opening through frontotemporal craniotomy is covered with both the temporal muscle and pericranial flap (Fig. 17.9). Cranioplasty is performed as usual. Titanium plates are usually employed for cranioplasty, but the author prefers the absorbable plates for pediatric patients younger than 10 years not to disturb the normal growth of their skull. The wound is closed in a layer-by-layer fashion. Total operation time ranges from 5 to 6 hours. Blood transfusion is usually unnecessary.

17.9 Difficulties Encountered

17.9.1 Preservation of Scalp Blood Flow

It is quite important to avoid the delayed wound healing after surgical revascularization for moyamoya disease. The delay of wound healing may prolong a hospital stay and furthermore require surgical repair. The author has modified surgical technique to avoid this problem for these 20 years. First, the curvature of skin incision should be designed at an obtuse angle so that the blood flow would be maintained at the top of curvature (Fig. 17.3d). Second, the STA branches should be carefully dissected from the surrounding galeal tissue under the surgical microscope. The dissected STA should be “naked,” because the surrounding galeal tissue is quite important for wound healing and should be left to the scalp (Fig. 17.4c, d). Third, the galeal “track” after dissecting the frontal branch of the STA should always be repaired by suturing the galeal tissue so that the scalp blood flow would be recovered earlier after surgery (Fig. 17.6a, b). The small amounts of time and effort contribute to the preservation of scalp blood flow, thus supporting wound healing.13

17.9.2 Preservation of the MMA during Craniotomy

The MMA is known to function as important collaterals to the ACA territory, but often courses within the lesser wing of the sphenoid bone. Therefore, usual fashioned craniotomy easily injures the MMA. Therefore, the author has evaluated the surgical anatomy around the lessor wing of the sphenoid and developed a novel technique to preserve it during craniotomy. Briefly, the anatomical relationship between the anterior branch of the MMA and the lesser wing of the sphenoid bone can be classified into three types: bridge, monorail, and tunnel types. In the bridge type (18.5%), the anterior branch of the MMA runs within the shallow groove in the medial surface of bone, which looks like a bridge over a river. In the monorail type (37.0%), the anterior branch of the MMA runs within the deep groove in the medial surface of bone, which looks like a monorail vehicle over a rail. In the tunnel type (44.5%), the anterior branch of the MMA is completely enclosed within the bony canal in the lesser wing of the sphenoid bone, which looks like a tunnel. Patients’ age is closely related to the anatomical relationship between the anterior branch of the MMA and the lesser wing of the sphenoid wing. The bridge-type MMA can frequently be observed in younger patients.

During large frontotemporal craniotomy, a total of five burr holes are made. The burr hole at the center of craniotomy site is made rostral to the pterion to preserve the anterior branch of the MMA, because it is known to pierce the bony tunnel of the middle meningeal groove just beneath the junction of the sphenoparietal, sphenosquamosal, and squamosal sutures (Fig. 17.7a). A heartshaped craniotomy is performed, preserving the lesser wing of the sphenoid bone. Then, the lesser wing is resected carefully preserving the anterior branch of the MMA, using a rongeur or high-speed drill. Careful resection of the lesser wing with a rongeur can preserve the bridge- and monorail-type MMA (100 and 71.4%, respectively). However, drilling out of the lesser wing under a surgical microscope is essential to preserve the tunneltype MMA(Fig. 17.10).

Before surgery, the anatomical relationship between the anterior branch of MMA and the lesser wing of the sphenoid bone can precisely be analyzed on the raw images of time-of-flight (TOF) MR angiography. Plain CT scans are also useful to visualize the bony groove or tunnel around the pterion in all patients.14

17.9.3 ICG Videoangiography before Craniotomy

Using ICG videoangiography, the author has visualized the course of the MMA before craniotomy to further advance the methodology to preserve the MMA during craniotomy. Precise analysis has revealed that ICG videoangiography could clearly visualize the anterior branch of the MMA in 10 (37%) of 27 sides. The patients with the “visible” MMA are significantly younger than those without. ICG videoangiography can visualize it through the cranium when the diameter of the MMA is more than 1.3 mm and the sphenoid bone thickness over the MMA is less than 3.0 mm. The MMA can be preserved during craniotomy in all “visible” MMA, but not in 4 (23.5%) of the 17 “invisible” MMA. Therefore, ICG videoangiography can visualize the anterior branch of the MMA before craniotomy in about one-third of patients with the large-diameter MMA (> 1.3 mm) and thin sphenoid bone (< 3.0 mm). ICG videoangiography would be a safe and valuable technique to preserve it during craniotomy for moyamoya disease in them (Fig. 17.11).15

17.9.4 STA-MCA Anastomosis

The recipients are known to have a very small caliber and a very thin wall in moyamoya disease. Therefore, accurate suturing is essential to yield a good patency of direct bypass. For this purpose, a marking pin technique is quite useful. Thus, each needle should be left keeping the surface of both cut ends in good position until the next needle is placed, like a pin fastens pieces of cloth together when sewing (Fig. 17.12).

17.10 Bailout, Rescue, and Salvage Maneuvers

The surgeons should postpone direct STA-MCA anastomosis when the diameter of all recipients is too small (<0.5 mm). The surgeons should carefully observe the patency of direct STA-MCA anastomosis because the incidence of its thrombotic occlusion is higher than usual STA-MCA anastomosis for patients with atherosclerotic carotid occlusion. In such a case, the surgeons should open the anastomosed site by removing several stitches, remove the thrombus, and reanastomose it.


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