Surgical Techniques in Moyamoya Vasculopathy. Peter Vajkoczy

Chapter 14. Combined STA-MCA Bypass and Encephalo-myo-synangiosis

Marcus Czabanka and Peter Vajkoczy


Cerebral revascularization in moyamoya vasculopathy may be achieved by direct and indirect procedures. As both strategies are characterized by distinct advantages and disadvantages, combination strategies aim at combining the advantages of both procedures in order to achieve maximum restoration of cerebral blood flow. While direct superficial temporal artery-middle meningeal artery (STA-MMA) bypass leads to immediate supply of collateral flow, encephalo-myo-synangiosis (EMS) leads to revascularization in large area of the brain and may provide additional blood flow in the case of insufficient bypass function. In this chapter the technical aspects of combining STA-MCA (middle cerebral artery) bypass with EMS are demonstrated focusing on technical challenges and problem solving strategies.

Keywords: STA-MCA bypass, encephalo-myo-synangiosis, combined revascularization, moyamoya

14.1 History and Initial Description

In 1977 Karasawa et al published the first description of encephalo-myo-synangiosis (EMS) in moyamoya patients showing that in combination with direct superficial temporal artery-middle cerebral artery (STA-MCA) anastomosis novel collateral vessels develop on the surface of the brain supplied by the deep temporal artery that is known to deliver blood flow to the temporal muscle.1 The introduction of this indirect revascularization procedure for moyamoya patients initiated an ongoing debate about the ideal revascularization strategy leading to the development of various combined revascularization protocols. Matsushima et al demonstrated that combined STA-MCA bypass and EMS is superior to indirect only procedures regarding development of collateral blood flow and clinical improvement of ischemic patients.2'3 Age-dependent revascularization patterns revealed that in adult patients STA-MCA anastomosis is the main source of additional blood flow in the case of combined STA-MCA/EMS surgery, whereas in pediatric patients collateral flow via the EMS significantly improves over the course of time compensating or even replacing blood flow via the direct anastomosis.4 Functional analysis demonstrates that in adult patients combined STA-MCA/EMS leads to a significant recovery of cerebrovascular reserve capacity while single EMS does not lead to reversal of hemodynamic compromise.5 Therefore, combining STA-MCA anastomosis with EMS is especially beneficial in pediatric patients whereas the additional application of EMS seems of inferior importance in adult patients in the presence of a direct anastomosis.

14.2 Indications

Combined STA-MCA bypass and EMS is used in pediatric patients and young adults as the revascularization strategy of choice. In pediatric patients EMS has been demonstrated to lead to successful revascularization results and may represent an important additional source of collateral flow in case of small STA size and insufficient direct bypass function. In adults, EMS demonstrates less effective revascularization results and is primarily performed additionally to STA-MCA bypass in case of small or insufficient STA anatomy.

14.3 Key Principles

The general concept of combining STA-MCA bypass and EMS in moyamoya patients includes the idea that more blood flow is restored in a larger vascular territory of the brain via the combined strategy as compared to either single procedure. Additionally, the combination of both procedures promises maintenance of collateral flow in the case of failure of a single procedure (reciprocal com- pensation).Sufficient platelet antiaggregation is recommended depending on preoperative assessment of aspirin resistance using PFA-100 testing.6 Compared to single STA-MCA bypass surgery, the size of the craniotomy is increased to the size of the temporal muscle (with the sylvian fissure as the center of craniotomy) in order to allow transposition to the brain surface. Special care has to be applied to preparation of the galea and the base of the temporal muscle in order to avoid damage to the neovascular potential of the donor tissue. This includes avoidance of compression at the base of the temporal muscle especially after bone flap reimplantation in order to avoid both compression of the donor branch of the STA and the blood supply of the temporal muscle.

14.4 SWOT Analysis

14.4.1 Strengths

STA-MCA bypass supplies direct blood flow and therefore leads to immediate hemodynamic improvement. EMS may provide additional blood flow if bypass capacity is not sufficient. In case of bypass failure EMS may compensate collateral blood flow.

14.4.2 Weaknesses

Combining both procedures adds surgical time and surgical risks. Especially in pediatric patients STA-MCA bypass may be difficult to achieve due to fragile and small donor and recipient vessels. Large craniotomy and muscle transposition represents a source for rebleeding from the temporal muscle and includes the risk of brain compression in case of muscle edema. Moreover, the efficacy of restoring blood flow via the EMS cannot be predicted and has been shown to be very variable.

14.4.3 Opportunities

The efficacy of restoring additional blood flow to the brain via the EMS may be improved by a genetic strategy.Application a myoblast-mediated gene transfer of proan- giogenic and porarteriogenic genes to the muscle/brain interface has been shown to improve collateral flow to the brain and to reduce the risk for ischemia.7 Therefore, the muscle/brain interface represents a promising target for molecular biological strategies to induce arterio- and angiogenesis.

14.4.4 Threats

Failure of anastomosis due to fragile and thin recipient and donor vessels represent a major threat. Additional threats include risks of rehemorrhage, ischemia, or hyperperfusion syndrome. A special risk must be attributed to swelling of the temporal muscle which may induce a space occupying, compressive effect on the brain. Extremely rare are long-term complications as occlusion of the donor vessel during mouth opening resulting in transient ischemic attacks.8

14.5 Contraindications

Presence of middle meningeal artery (MMA) as part of vault moyamoya vessels or the STA as contributor of vault moyamoya vessels represent the most important contraindications. The required large dural opening imposes a significant risk for dural feeders of vault moyamoya vessels potentially leading to cerebral ischemia. As combined STA-MCA/EMS revascularization is predominantly used for pediatric patients, an insufficient caliber of the STA may be a relevant disadvantage and often represents a technical challenge for the surgeon. Nevertheless, direct anastomosis is recommended in the presence of a potentially useful donor vessel. Massive brain atrophy also represents a special contraindication as physical contact between the temporal muscle and the brain surface (brain/muscle interface) is required for successful indirect revascularization. As the temporal muscle is sutured to the dural edges, brain atrophy may increase the distance between the dura and brain surface making physical contact between muscle and brain surface impossible.

14.6 Special Considerations

Vascular imaging modalities represent the most important prerequisite to plan STA-MCA/EMS revascularization. Digital subtraction angiography should focus apart from the intracranial vascular status on the external carotid artery to visualize presence, size and course of the STA. Special attention has to be paid to vault moyamoya vessels, their specific contributors (i.e., occipital artery, MMA, STA, etc.) and localization. It is especially important to analyze vault moyamoya vessels in anteroposterior and lateral views in order to judge their contribution of collateral blood flow to the brain. Presence of vault moyamoya vessels fed by the MMA may either be a contraindication for this surgical strategy or it may lead to a different surgical technique for establishing EMS by opening the dura around the MMA in order to protect collateral flow via the extraintracranial anastomoses. MRI represents another important aspect not only to rule out signs of acute ischemia but also to judge brain atrophy. Major brain atrophy may represent an important obstacle making it impossible to establish a sufficient brain/muscle interface. Anticoagulation is usually established preoperatively using aspirin 100 mg orally once daily. Platelet antiaggregation is tested preoperatively using PFA-100 testing in order to rule out aspirin resistance. In the presence of aspirin resistance, the daily dose is increased to 300 mg orally, followed by PFA-100 retesting. If aspirin resistance cannot be overcome by increasing the daily dose to 300 mg, antiaggregation strategy is changed to clopidogrel 75 mg daily. In this case, surgery is then performed under clopidogrel 75 mg. It must be mentioned that other institutions deal differently with preoperative antiplatelet therapy. Some surgeons do not even perform any antiplatelet therapy before or directly after bypass surgery. Therefore, the above named antiplatelet strategy represents a recommendation in the lack of high-level evidence regarding antiplatelet therapy in moyamoya vessel patients. In the following chapters technical descriptions of each revascularization strategy include the authors’ preferred antiplatelet strategy during revascularization surgery therefore a broad overview will be provided.

The anatomic specificities of the individuals STA govern the shape of the skin incision. Depending on which STA branch is used as donor vessel, a Y-shaped or a curved skin incision is used to prepare the donor vessel as well as the temporal muscle.

Special surgical care has to be applied to preparation of the temporal muscle and the galea apart from preparation of the STA, as the sacrifice of the STA and the staged preparation of the skin and temporal muscle may lead to problems with wound healing. Therefore, a clear concept for the skin incision as well as muscle preparation should be followed in order to minimize surgical trauma to these tissues (Fig. 14.1). Blunt dissection of the temporal muscle from the underlying bone is performed starting from the base of the temporal muscle with stepwise dissection toward the temporal line in order to maintain structural and vascular integrity of the muscle surface. Preparation of the temporal muscle imposes an ambivalent problem as bipolar or monopolar coagulation should be avoided to protect microvascular integrity; on the other side, bleeding sources should be addressed as the surface of the temporal muscle may represent a source for postoperative hemorrhages, especially subdural hematomas. Moreover, sensitive handling of the muscle is important in order to reduce the risk for muscle edema, which may lead to compression of the cerebral surface after establishing the brain/muscle interface. As the deep temporal artery courses along the base of the temporal muscle, avoid dissection of the basal part in order to protect blood supply. The craniotomy is centered around the sylvian fissure and its individual size and shape is orientated on the shape and size of the temporal muscle before dissection is started.

14.7 Pitfalls, Risk Assessment, and Complications

Major pitfalls include presence of the MMA as part of vault moyamoya vessels. In these cases, opening of the dura around the MMA is performed and the temporal muscle is placed on this fenestrated transdural approach on the brain surface. Injury of the MMA during craniotomy represents a major problem for hemodynamically relevant vault moyamoya vessels as this may lead to cerebral ischemia. Establishing the craniotomy centered around the sylvian fissure usually avoids the pitfall of a nonsuitable recipient vessel on the brain surface as the perisylvian area usually represents a hotspot for sufficient recipient arteries.9 The major risks for combined STA- MCA bypass and EMS are development of perioperative cerebral ischemia with a reported risk of 5 to 8%.10,11 Wound healing problems occur in 2 to 6% of surgeries due to the greater wound surface generated by the combined approach compared to a targeted bypass-only approach. Hyperperfusion syndrome has been reported to range between 15 and 30% in adult moyamoya patients (lower in pediatric patients); however, most hyperperfusion syndromes present with a good prognosis.12 Interestingly, differences are reported in hyperperfusion syndrome between Asian patient series and North American or European patient series, in which a lower incidence of hyperperfusion syndrome is reported.10,13,14

14.8 Special Instructions, Position, and Anesthesia

The patient is positioned keeping the surgical field in a horizontal plane as performed in standard STA-MCA bypass surgery. This approach includes the advantage that STA-MCA bypass may be performed in patients with unknown bypass feasibility prior to surgery. During positioning prevention of jugular venous congestion and subsequent cerebral swelling are important features that should be paid attention to as intraoperative surgical rescue maneuvers like CSF drainage to reduce brain swelling are limited in a juvenile brain with moyamoya vasculopathy. Anesthesia is usually performed following the concept of a “slack brain” in order to avoid swelling and venous congestion of the cerebral veins at the border of the durotomy. For this purpose propofol and remifentanil are key elements as they reduce cerebral metabolism and blood volume. Burst suppression on electroencephalography may be achieved by the use of barbiturates. Definitely, osmotic agents (i.e., mannitol) are administered to achieve further relaxation of the brain. Maintenance of sufficient cerebral perfusion pressure by aiming for the right mean arterial blood pressure is the second key step.

Blood pressure should be maintained at high-normal level with a mean arterial pressure targeted between 80 and 90 mm Hg at all times. A fraction of inspired oxygen of 1.0 (100%) may offer additional ischemic protection. In any case, hyperventilation should be avoided in order to prevent further reduction of the already compromised cerebral perfusion.

14.9 Patient Position and Key Surgical Steps

Head is positioned in the Mayfield clamp in 90-degree rotation with the head slightly elevated above the heart level. A Y-shaped skin incision is used to dissect either the frontal or the parietal branch of the STA and to allow preparation of the temporal muscle (Fig. 14.2). After skin retraction, the STA is dissected, leaving a tissue sheath around the STA to protect the vessel from manipulation and to reduce manipulation induced vasospasm (Fig. 14.3). Retraction of the dissected STA branch and further skin retraction along the Y-shaped skin cut allow incision of the galea along the temporal line and the dorsal aspect of the temporal muscle (Fig. 14.4). Gentle blunt preparation of the temporal muscle from proximal to distal avoiding coagulation preserves structural and vascular integrity of the temporal muscle. Avoid dissection at the base of the muscle to protect the deep temporal artery (Fig. 14.5).

The size of the craniotomy is orientated on the size of the temporal muscle and it is centered around the sylvian fissure (Fig. 14.6a). Anastomosis between the STA and a cortical perisylvian branch of the MCA is performed using a microsurgical technique (Fig. 14.6b, c). A large dural flap is prepared and transposed upon the cortical surface to install an additional encephalo-duro-synangiosis instead of resecting the dural flap (Fig. 14.6d).

The temporal muscle is then transposed to the cortical surface and the edges of the muscle are sutured to the dural edges (Fig. 14.7b). Special attention has to be paid to the course of the STA donor vessel, which should not be compromised by the transposed muscle. Bone flap is reimplantated and fixed with craniofix system. Special attention has to be paid to the base of the bone flap to leave enough space for the transposed muscle flap and the STA bypass branch (Fig. 14.7c). Avoid any compromise of either the muscle or the bypass vessel usually requiring removal of bone at the base of the bone flap.

14.10 Difficulties Encountered

Major difficulties include low bypass cut flow, which usually represents flow capacity of the STA. Assessment of cut flow requires measurement of blood flow in the designated bypass branch using a flow microprobe with a diameter of 1.5 mm. If cut flow is low, check for STA compression by the temporal muscle or by an accompanying vein. In the case of bypass failure after anastomosis (checked by intraoperative indocyanine green videoangiography) revision of the anastomosis should be performed. As this may be difficult in individual bases, a new anastomosis may be performed on a new recipient vessel. This rescue strategy requires sufficient length of the donor vessel and the presence of another sufficient recipient artery. If there is a lack of suitable recipient on the cortical surface, the perisylvian approach used for combined STA-MCA/EMS allows opening the sylvian fissure and preparing an M2 branch as recipient. Preparation of the temporal muscle may lead to intramuscular edema or hemorrhage which will result in a space occupying lesion if it is placed on the brain. This space occupying effect may be counteracted by leaving out the bone flap, which holds the advantage that indirect revascularization may still occur.

14.11 Bailout, Rescue, and Salvage Maneuvers

There are two options to deal with an insufficient bypass anastomosis. First, reopen the anastomosis and check for an intravascular thrombus occluding the anastomosis. Sometimes stitches to the posterior wall of the anastomosis become evident. In these cases redo the anstomosis. Second, cut the bypass branch, occlude the part of the branch that is left on the M4 segment of the MCA with a clip and redo the anastomosis with a new recipient. This option is only available if the donor branch provides enough length to cut it and to displace it to a novel recipient. In the case of bleeding from the temporal muscle look for careful hemostasis focusing on targeted coagulation in order to maintain vascular and structural integrity of the temporal muscle for secondary vascular sprouting to the ischmemic cerebral cortex. Applying an EMS provides the opportunity that indirect revascularization may occur in the presence of an insufficient direct anastomosis representing a rescue strategy if repetitive anastomoses fail. When massive swelling of the temporal muscle is observed during preparation, leaving out the bone flap allows for indirect decompression and may save the EMS.

14.12 Tips, Pearls, and Lessons learned

Skin incision was changed from a curved incision to a linear incision over the donor branch of the STA. If the frontal branch is the donor vessel of choice, a Y-shaped incision is used to allow wide access to the temporal muscle and direct preparation of the STA bypass branch with one part of the Y-shaped incision designated above the donor artery. This allows direct preparation of the donor branch without the need to prepare the donor in the skin flap after curved incision while guaranteeing good access to the temporal muscle. If the parietal branch represents the donor vessel of choice a small curved incision (as used for a small pterional approach) is performed to allow direct preparation of the parietal branch without the need to dissect the donor from the skin flap (see Fig. 14.1). Proximal to distal preparation of the temporal muscle in a blunt technique is recommended to maintain structural and vascular integrity of the temporal muscle while reducing hemorrhage from the muscle requiring coagulation. After opening the dura meticulous coagulation of dural edges is important to reduce bleeding into the operative field during the anastomosis preparation. For optimal bypass anastomosis the recipient artery is identified using intraoperative vidoeangiography assessing blood flow characteristics in the recipient prior to anastomosis. Another important aspect is to make sure that the bypass branch and the translocated temporal muscle do not interfere with each other.


[1] Karasawa J, Kikuchi H, Furuse S, Sakaki T, Yoshida Y. A surgical treatment of “moyamoya” disease “encephalo-myo synangiosis”. Neurol Med Chir(Tokyo). 1977; 17(1 Pt 1):29-37

[2] Matsushima T, Inoue T, Katsuta T, et al. An indirect revascularization method in the surgical treatment of moyamoya disease—various kinds of indirect procedures and a multiple combined indirect procedure. Neurol Med Chir (Tokyo). 1998; 38 Suppl:297-302

[3] Matsushima T, Inoue T, Suzuki SO, Fujii K, Fukui M, Hasuo K. Surgical treatment of moyamoya disease in pediatric patients—comparison between the results of indirect and direct revascularization procedures. Neurosurgery. 1992; 31(3):401 -405

[4] Czabanka M, Vajkoczy P, Schmiedek P, Horn P. Age-dependent revascularization patterns in the treatment of moyamoya disease in a European patient population. Neurosurg Focus. 2009; 26(4):E9

[5] Czabanka M, Pena-Tapia P, Scharf J, et al. Characterization of direct and indirect cerebral revascularization for the treatment of European patients with moyamoya disease. Cerebrovasc Dis. 2011; 32(4):361-369

[6] Jussen D, Horn P, Vajkoczy P. Aspirin resistance in patients with hemodynamic cerebral ischemia undergoing extracranial-intracranial bypass surgery. Cerebrovasc Dis. 2013; 35(4):355-362

[7] Hecht N, Pena-Tapia P, Vinci M, von Degenfeld G, Woitzik J, Vajkoczy P. Myoblast-mediated gene therapy via encephalomyosynangiosis—a novel strategy for local delivery of gene products to the brain surface. J Neurosci Methods. 2011;201(1):61-66

[8] Freyschlag CF, Seiz M, Brockmann MA, et al. Effect of mouth opening on bypass function after combined revascularization for moyamoya disease. Acta Neurochir Suppl (Wien). 2011; 112:35-38

[9] Pena-Tapia PG, Kemmling A, Czabanka M, Vajkoczy P, Schmiedek P. Identification of the optimal cortical target point for extracranial- intracranial bypass surgery in patients with hemodynamic cerebro- vascularinsufficiency.J Neurosurg. 2008; 108(4):655-661

[10] Guzman R, Lee M, Achrol A, et al. Clinical outcome after 450 revascularization procedures for moyamoya disease. Clinical article. J Neuro- surg. 2009; 111(5):927-935

[11] Kazumata K, Ito M, Tokairin K, et al. The frequency of postoperative stroke in moyamoya disease following combined revascularization: a single-university series and systematic review. J Neurosurg. 2014; 121(2):432-440

[12] Fujimura M, Mugikura S, Kaneta T, Shimizu H, Tominaga T. Incidence and risk factors for symptomatic cerebral hyperperfusion after superficial temporal artery-middle cerebral artery anastomosis in patients with moyamoya disease. Surg Neurol. 2009; 71(4):442-447

[13] Acker G, Goerdes S, Schmiedek P, Czabanka M, Vajkoczy P. Characterization of clinical and radiological features of quasi-moyamoya disease among European Caucasians including surgical treatment and outcome. Cerebrovasc Dis. 2016; 42(5-6):464-475

[14] Acker G, Goerdes S, Schneider UC, Schmiedek P, Czabanka M, Vaj- koczy P. Distinct clinical and radiographic characteristics of moya- moya disease amongst European Caucasians. Eur J Neurol. 2015; 22 (6):1012-1017

If you find an error or have any questions, please email us at Thank you!