5.1 History and Initial Description

Surgical treatment of hemodynamic compromise typically uses the external carotid artery (ECA) as a source of new blood flow to the ischemic hemisphere. The two general methods of revascularization are as follows: (1) direct, where an extracranial to intracranial (EC–IC) bypass anastomosis between a donor vessel (typically the frontal or parietal branch of the superficial temporal artery [STA]) and a cortical recipient vessel (typically an M4-segment branch of the middle cerebral artery [MCA]) is grafted, or (2) indirect, where a vascularized, autologous graft supplied by the ECA is placed in direct contact with the surface of the brain, which results in spontaneous transpial vessel sprouting from the vascularized graft into the hypoperfused brain. The earliest attempt of indirect revascularization in humans was reported in 1942 by Kredel, who placed a vascularized pedicle graft of the temporalis muscle directly onto the surface of the brain after removal of the underlying bone and opening of the dura. ¹ However, Kredel was discouraged by the high rate of perioperative seizures and abandoned the procedure until it was revived in 1977 by Karasawa, who termed the procedure encephalo-myo-synangiosis (EMS). ¹ In 1981, Kobayashi used cerebral angiograms to confirm patent EC–IC collaterals at the muscle/brain interface of an EMS. ² Later, Perren and colleagues nicely showed that a patent EMS not only results in transpial collateralization, but that these EC–IC collaterals also carry functional hemodynamic efficacy. ³ Meanwhile, several other procedures for indirect revascularization exist, such as encephalo-duro-arterio-synangiosis (EDAS), encephalo-myo-arterio-synangiosis (EMAS), pial synangiosis, dural inversion, and the drilling of burr holes without vessel synangiosis. ^{4 – 8} However, most experts agree that usage of the temporalis muscle as a vascularized graft probably provides the best prerequisite for successful indirect revascularization due to its rich blood supply and large surface area.

5.2 Indications

The key factor for compensation of hemodynamic compromise is endogenous flow augmentation through outgrowth of preexisting collaterals. ⁹ This requires an active proliferation of endothelial and perivascular cells, which is naturally limited. In cases of hemodynamic failure, surgical revascularization is a recognized treatment option. However, there remains considerable debate about the merits and shortcomings of direct versus indirect revascularization. In certain cases, however, the grafting of a direct bypass is technically more challenging and sometimes not feasible due to the small caliber and fragile cortical vasculature, such as in moyamoya vasculopathy, where vascular remodeling of the tunica muscularis renders the cortical vessels prone to rupture during suturing of the anastomosis. Also, there are situations where direct grafting of a standard STA–MCA bypass is not possible due to lack of a suitable STA donor vessel. In these cases, an EMS has the advantage of being less complex and safer than a direct bypass with proven benefit in pediatric patients with moyamoya vasculopathy. ^{10 – 13} Sometimes, even a combination of a bypass with an EMS may be indicated, for example, above the symptomatic hemisphere in pediatric patients with moyamoya vasculopathy. On the other hand, compared to a direct bypass, an EMS has the main disadvantages that (a) it offers no immediate ischemic protection and (b) that it is characterized by lower hemodynamic effectiveness and inconsistent revascularization results in adults and patients suffering from arteriosclerotic disease. ¹⁴ Therefore, we recommend that an EMS alone as the primary revascularization option should only be considered for treatment of the asymptomatic hemisphere in pediatric patients with moyamoya vasculopathy.

5.3 Key Principles

The general principle of an EMS is to transpose a vascularized pedicle graft of the temporalis muscle onto the surface of the underlying brain after performing a craniotomy and opening the dura. In all cases, the following key principles need to be considered in order to ensure successful indirect revascularization and limit the risk of complications:

1. 
   

   The size of the craniotomy should match the size of the temporalis muscle to provide the largest possible contact surface between the muscle and the brain.

   
   
2. 
   

   The sylvian fissure should be at the center of exposure so that the temporal and frontal regions of the brain are equally able to receive transpial collaterals.

   
   
3. 
   

   Meticulous hemostasis of the dura border and at the surface of the muscle is imperative to minimize the risk of postoperative subdural hemorrhage.

   
   
4. 
   

   Compression of the muscle with the bone flap at the base of the craniotomy should be avoided so that perfusion of the graft is not compromised.

5.4 SWOT Analysis

5.5 Contraindications

Although an EMS offers a technically simple alternative to direct revascularization, the following contraindications need to be considered in order to ensure safety and effectiveness of the procedure. First, patients should not have a history of coagulopathy or platelet dysfunction because hemorrhage from the dissected surface of the temporalis muscle is one of the most feared postoperative complications. Prior to EMS surgery, we therefore recommend pausing anticoagulants or platelet inhibitors that may be required for treatment of the underlying vascular pathology. Second, EMS revascularization should not be performed in patients with brain atrophy because direct contact between the surface of the temporalis muscle and the brain is essential to ensure sprouting and ingrowth of transpial collaterals. Third, the angiograms of the patient should be studied for signs of preexisting EC–IC collaterals from the MMA because although EMS revascularization with sparing the MMA and its branches is technically feasible, this requires advance planning of the craniotomy and dural opening (i.e., with image guidance) in order to avoid perioperative ischemia due to iatrogenic transection of preexisting MMA collaterals.

5.6 Special Considerations

When planning for an EMS, specific details need to be considered. Despite the recent advances of 7 Tesla magnetic resonance imaging (MRI), digital subtraction angiography (DSA) remains the gold standard in the preoperative workup of moyamoya patients planned for cerebral revascularization. ^{17 ,​ 18} Here, a DSA with an external carotid injection is required not just for identification of a suitable donor vessel in the case of a direct revascularization, but also to identify vault moyamoya vessels. ¹⁹ These preformed EC–IC collaterals at the surface of the brain typically feed off branches from the MMA, superficial temporal or occipital artery or from branches of tentorial arteries or the anterior falx and need to be preserved during dissection in order to avoid ischemic complications. Also, a recent MRI scan is needed to identify the extent of brain atrophy and exclude extensive preexisting postischemic tissue damage in the cortical region below the intended EMS. Further, patients scheduled for an EMS require an in-depth hemostasiological analysis to exclude coagulopathies and platelet dysfunction and any anticoagulant or antiplatelet therapy should be discontinued perioperatively. To further optimize the revascularization result, the EMS can be combined with additional inversion of a frontal dural pedicle graft (encephalo-duro-synangiosis).