Nils Hecht and Peter Vajkoczy
An encephalo-myo-synangiosis (EMS) describes a form of indirect revascularization, where a vascularized pedicle graft of the temporalis muscle is placed directly onto the surface of the brain, which results in spontaneous sprouting of transpial extracranial-intracranial collaterals in patients suffering from moyamoya vasculopathy. Compared to a direct bypass, the advantages of an EMS are its technical simplicity and lower perioperative stroke risk. On the other hand, current research focuses on how to improve the hemodynamic efficacy and overall effectiveness of an EMS. Against this background, this chapter reviews and focuses on the indication and technical aspects of an EMS as well as its pearls, pitfalls, and limitations.
Keywords: cerebral revascularization, encephalomyo-synangiosis, indirect revascularization, moyamoya vasculopathy
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), encephalomyo-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.
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.
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.
Compared to direct revascularization, an EMS is a technically simple, safe and quick procedure, which provides a large surface for spontaneous transpial EC-IC collateralization.
The muscle surface and border of the dura are potential sources of postoperative subdural hemorrhage. Also, hemodynamic effectiveness is inconsistent and does not occur immediately after surgery.
The current challenge in EMS surgery is to improve functional and morphological collateralization across all patient populations, for example, by local boosting of proangiogenic activity with continuous delivery of vascular growth factors at the muscle/brain interface.15,16
The indirect EC-IC collaterals of an EMS may be ineffective in restoring hemodynamic compromise in some cases. Further, certain steps of the surgical preparation, such as the craniotomy and durotomy may injure spontaneously formed middle meningeal artery (MMA) collaterals, which are termed "vault moyamoya vessels" and frequently encountered in patients with moyamoya vasculopathy.
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.
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).
At present, there are no reports regarding the risk of perioperative complications following an EMS. However, most experts agree that the main specific surgical risk of an EMS is subdural hemorrhage and/or hemorrhagic swelling of the temporalis muscle that requires revision in approximately 5% of all cases. Another typical complication in patients undergoing cerebral revascularization is ischemic stroke, which was shown to occur in up to 15% after direct bypass revascularization.20 Even in highly specialized centers this perioperative stroke risk rarely drops below 5%,10,21,22,23 against which the estimated perioperative stroke risk of 1 to 2% after an EMS alone compares favorably.
The key element of neuroanesthesia is to maximize brain relaxation (“slack brain”) in order to avoid swelling and venous congestion of the cerebral veins at the border of the durotomy. For this purpose, anesthetic agents that lower the cerebral metabolic rate, neuronal activity, and cerebral blood volume, such as propofol and remifentanil are commonly used.24'25 Barbiturates may be administered up to burst suppression on electroencephalography (EEG). Osmotic agents (i.e., mannitol) may gain additional brain relaxation. Hyperventilation should be avoided in order to prevent further reduction of the already compromised cerebral perfusion. Most importantly, blood pressure should be maintained at high normal level with a mean arterial pressure (MAP) targeted between 80 and 90 mm Hg at all times. Next to anesthesia, positioning of the patient is equally important to prevent jugular venous congestion and subsequent cerebral swelling, since there is usually no relevant amount of cerebrospinal fluid to be gained from the sulci and fissures of the juvenile brain with moyamoya vasculopathy. For an EMS, we generally recommend a horizontal surgical field orientation similar to a standard STA-MCA bypass, particularly in cases where a combined revascularization is planned and feasibility of a bypass cannot be anticipated.
5.9.1 Patient Position and Skin Incision
To avoid excessive head rotation, the ipsilateral shoulder should be supported with the patient secured to the operating table. Final 90-degree positioning is then accomplished by the following two measures:
• Head rotation of 50 to 60 degrees.
• Tilting of the operating table to 30 to 40 degrees.
Fig. 5.1 describes patient positioning and head rotation.
5.9.2 Pterional Skin Incision
An extended pterional skin incision (Fig. 5.2) is planned according to the required dimensions of the craniotomy along the insertion border of the temporalis muscle and to expose an equally large frontal-temporal surface area including the end of the sylvian fissure, which can be identified with the help of the target point described by Pena and colleagues.26
5.9.3 Separate Skin and Muscle Flaps
To allow transposition of the temporalis muscle below the underlying bone, the skin is dissected from the outer fascia of the temporalis muscle to create separate skin and muscle flaps (Fig. 5.3). The insertion of the temporalis muscle at the superior temporal line is cut with monopolar cautery. Importantly, monopolar cautery should only be used to cut the insertion line of the muscle and not to dissect the muscle from the bone (see Chapter 5.9.4).
5.9.4 Mobilization of the Temporalis Muscle
To spare the blood supplying vessel branches and limit dissection trauma to the muscle fibers, the temporalis muscle should be mobilized from proximal to distal along the course of the muscle fibers with the help of a curved raspatorium (Fig. 5.4). Caution should be exercised to preserve the integrity of the inner muscle fascia.
5.9.5 Elevation of the Muscle Flap
After mobilization, the muscle flap is elevated and turned towards the base of the exposure (Fig. 5.5). The muscle is then held back over the skin as a separate flap by gentle retraction.
5.9.6 Craniotomy and Drilling of the Sphenoid Wing
After retraction of the muscle pedicle graft, the lateral sphenoid wing should be spared when performing the craniotomy to preserve potential MMA collaterals. After removal of the bone flap, the lateral sphenoid wing is drilled down to spare potential MMA collaterals (see Fig. 5.6).
5.9.7 Opening of the Dura and Encephalo-duro-synangiosis
The dura is opened along the border of the MMA using a window technique to preserve potential vault moyamoya vessels beyond the area of exposure (Fig. 5.7). The dural f laps are then inverted as an encephaloduro-synangiosis to provide an additional surface for spontaneous EC-IC collateralization beyond the border of the craniotomy.
5.9.8 Suturing of the Muscle Fascia to the Edge of the Dural Opening
To complete the EMS, the muscle graft is placed onto the surface of the brain after final hemostasis and the muscle fascia is sutured to the outer edge of the dural opening with a nonabsorbable 3-0 running suture (see Fig. 5.8).
5.9.9 Bone Flap Reimplantation
After completion of the EMS, the bone flap is reimplanted and secured with titanium pins. To avoid compression of the graft, it is important to leave sufficient space for the muscle to pass through at the base of the craniotomy by removal of excess bone (see Fig. 5.9).
Frequently, the MMA is very adhesive to the bone and/or has a prolonged course within the flap, which may result in unintentional injury to the MMA during turning of the flap. As outlined above, this can be avoided by drilling the lateral sphenoid wing with a diamond burr and careful elevation of the flap under visual inspection. In case intramuscular hemorrhage or swelling occurs prior to suturing the fascia to the dural edges, the bone flap should be left out to avoid compression of the brain. Further, compression of the muscle at the base of the craniotomy during flap reimplantation may result in venous stasis and additional swelling of the graft, which can be prevented by removing excess bone from base of the craniotomy. If a subdural hematoma is noted on routine postoperative imaging, revision surgery may be required for hematoma evacuation. In addition, the surgeon should steer clear of the following typical pitfalls:
• Inadequate (too small) size of the craniotomy.
• Inadequate hemostasis.
• Antiplatelet therapy continued.
• Injury to vault moyamoya (MMA) collaterals.
• Injury to the cortical surface during suturing.
For utilization of the maximum surface area for endogenous EMS collateralization, the craniotomy should be enlarged if the sylvian fissure and both opercula are not well exposed. Coincidentally, patient safety is ensured by management of coagulation disorders or platelet dysfunction.
In conclusion, an EMS poses an effective alternative to a direct bypass procedure in juvenile patients with moyamoya vasculopathy. Most importantly, simplicity and safety of an EMS remain ensured if the following technical aspects are observed:
1. The craniotomy should be large enough to expose the whole sylvian fissure.
2. Temporal-basal muscle retraction should be gentile to avoid facial nerve palsy.
3. Avoid monopolar cautery to spare the muscle fascia and vasculature.
4. The temporalis muscle should be mobilized from proximal to distal.
5. The lateral sphenoid wing should be spared during the craniotomy.
6. Thorough hemostasis should be performed at the muscle surface.
7. The EMS should be combined with dural inversion (encephalo-duro-synangiosis).
8. The muscle fascia should be stitched to the dura using the operating microscope.
9. Sufficient bone should be removed at the base of the craniotomy.
After surgery, we recommend overnight postoperative intensive care unit monitoring for adults and 24-hour observation in a neurological/neurosurgical intensive care unit (NICU) for pediatric patients. On the day after surgery, a noncontrast computed tomography is performed to rule out procedure related hemorrhage or ischemia. At 12 months, morphological function of the graft in terms of transpial EC-IC collateralization is assessed by conventional DSA.
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