Cervical carotid sympathectomy and superior cervical ganglionectomy

CS and ganglionectomy were the first surgical procedures used in the treatment of moyamoya by Suzuki and Takaku in 1969. Previous research had demonstrated loss of adrenergic axons within the walls of arteries and arterioles in dogs after a superior cervical ganglionectomy. The authors theorized that this would promote dilation of cerebral arteries and thus improve the collateral circulation. They performed this procedure in 10 children. Even though clinical symptoms initially improved, the progression of moyamoya was not halted both clinically and angiographically. Although the procedure now can be performed using a thoracoscopic approach, it has fallen out of favor because of the development of alternate revascularization techniques with better results and less surgical morbidity.

Omentral transplantation

OT first was described in a case report by Karasawa in 1978. The patient presented with bilateral motor ischemic events and blindness. The procedure consisted of a fronto-parieto-occipital skin incision, preserving the superficial temporal artery, and associated superficial temporal vein. The anteroinferior border of the craniotomy was used for insertion of the omentum. Via a midline laparotomy, a large 13 cm × 13 cm segment of omentum containing perforating vessels of the gastroepiploic artery and vein was isolated. An end-to-end anastomosis between the superficial temporal artery and vein to the gastroepiploic artery and vein, respectively, was performed. Durotomy and arachnoid incision permitted spreading of the transplanted omentum to the cortical surface. The patient improved clinically over the next 2 years without any new cerebrovascular events. Havlik and colleagues described a procedure whereby a pedicled graft of omentum was tunneled subcutaneously to the cerebral cortex in a patient who failed a direct (superficial temporal artery [STA]-MCA) bypass. The rate for patency of the omental graft has been reported to be as high as 70% over a 2-year period.

Touho and colleagues performed OT in five children who failed prior EMS, EDAS, or STA-MCA direct bypass surgeries. All patients experienced resolution of their neurologic deficits after several months. Similar results also were achieved by Karasawa and colleagues. His study involved 30 children, of whom 19 patients underwent omental transplant using the anterior cerebral artery distribution, and 13 patients underwent omental transplant using posterior cerebral artery distribution. All these patients except two in the posterior artery distribution group demonstrated neurologic improvement and increase in collateral vessels on follow-up angiography.

Omentral transplantation

OT first was described in a case report by Karasawa in 1978. The patient presented with bilateral motor ischemic events and blindness. The procedure consisted of a fronto-parieto-occipital skin incision, preserving the superficial temporal artery, and associated superficial temporal vein. The anteroinferior border of the craniotomy was used for insertion of the omentum. Via a midline laparotomy, a large 13 cm × 13 cm segment of omentum containing perforating vessels of the gastroepiploic artery and vein was isolated. An end-to-end anastomosis between the superficial temporal artery and vein to the gastroepiploic artery and vein, respectively, was performed. Durotomy and arachnoid incision permitted spreading of the transplanted omentum to the cortical surface. The patient improved clinically over the next 2 years without any new cerebrovascular events. Havlik and colleagues described a procedure whereby a pedicled graft of omentum was tunneled subcutaneously to the cerebral cortex in a patient who failed a direct (superficial temporal artery [STA]-MCA) bypass. The rate for patency of the omental graft has been reported to be as high as 70% over a 2-year period.

Touho and colleagues performed OT in five children who failed prior EMS, EDAS, or STA-MCA direct bypass surgeries. All patients experienced resolution of their neurologic deficits after several months. Similar results also were achieved by Karasawa and colleagues. His study involved 30 children, of whom 19 patients underwent omental transplant using the anterior cerebral artery distribution, and 13 patients underwent omental transplant using posterior cerebral artery distribution. All these patients except two in the posterior artery distribution group demonstrated neurologic improvement and increase in collateral vessels on follow-up angiography.

Multiple burr holes

MBH were developed as a treatment for MD after the discovery of neovascularization around burr holes performed for ventriculostomies. Endo and colleagues first reported this in 1984 in a pediatric patient who required bifrontal ventriculostomies. Using this observation as a starting point, Endo performed the first multiple burr hole procedure for MD in 1986. Angiographically adequate neovascularization at 12 months follow-up was noted with no ischemic events.

More recently this procedure was reported on 15 patients and 24 hemispheres by Sainte-Rose and colleagues. The patient is placed supine with head flexed to expose the entire calvarium if bilateral procedures are necessary. The incision is bi-coronal in a zigzag form for cosmesis. The exposure allows access to the frontal, parietal, temporal, and partial occipital regions bilaterally. If a unilateral procedure is indicated, the head is rotated to the contralateral side, and a T-shaped incision is fashioned.

The galea is dissected carefully, in a meticulous fashion to preserve vascularity of the scalp. The periosteum should remain intact, to preserve the vessels that will form future collateral networks. The reason that complete subperiosteal dissection is not preferred is mainly to prevent postoperative collection of cerebrospinal fluid (CSF), and also to minimize blood loss. Many triangular incisions are made in the periosteum and lifted as small flaps to expose the skull ( Fig. 1 ). These openings are placed roughly 3 cm apart, covering the appropriately targeted vascular territories, and 3 cm from the midline to avoid bleeding resulting from injury to the superior sagittal sinus or the associated draining veins. Burr holes then are made at each exposed area ( Fig. 2 ). The dura is opened through each burr hole using the microscope to avoid middle meningeal arterial branches. The arachnoid and pia are carefully opened while preventing any bleeding. Hemostasis is obtained by using cottonoid patties and gentle saline irrigation, as cautery is to be avoided to preserve any potential anastomotic vessels. The periosteal flap that elevated was previously is now placed in contact with the exposed parenchyma through each burr hole. The galea is carefully repositioned, with a two-layered skin/galea closure. A compressive dressing is applied for 4 days to facilitate hemostasis and limit facial swelling. Postoperative skull radiographs and a CT scan are obtained to exclude complications and assess placement of burr holes as a baseline, for comparison to follow-up angiograms and to assess for hemorrhage and CSF collections. None of their patients suffered ischemic events postoperatively, and angiography revealed excellent revascularization of the hemisphere by the external carotid system. Subcutaneous CSF collections occurred in 5 of the 18 procedures, but were treated successfully by tapping and wrapping the head; one patient also required a temporary lumbar drain.

Multiple burr hole technique (MBH). Schematic diagram depicting the location of the periosteal incision, elevation of the flap, and opening of the dura.

Reprinted from Sainte-Rose C, Oliveira R, Puget S, et al. Multiple bur hole surgery for the treatment of moyamoya disease in children. J Neurosurg 2006;105(6):439; with permission.

MBH technique. After the scalp is reflected ( A ), multiple triangular incisions in the periosteum are made ( B ). The burr holes then are made in the exposed skull, approximately 3 cm apart ( C ). The dura is opened, followed by the arachnoid and pia. The triangular flap of periosteum then is placed into the burr hole, making direct contact with the exposed cortex ( D ).

Reprinted from Sainte-Rose C, Oliveira R, Puget S, et al. Multiple bur hole surgery for the treatment of moyamoya disease in children. J Neurosurg 2006;105(6):438; with permission.

The most significant benefit of this technique is the ability to use it anywhere on the cranium. It can be, and often is, combined with other procedures, direct or indirect, and it is technically simpler than other approaches. Another potential benefit as discussed by Baaj and colleagues is that certain patients can undergo this procedure under local anesthesia, thus avoiding the risks of general anesthesia.

Encephalomyosynangiosis

Encephalomyosynangiosis (EMS) first was described by Karasawa and colleagues in 1975 and represented the first indirect revascularization technique for the treatment of MD. It was developed after reports in 1950 from Henschen, who demonstrated revascularization from muscle flaps after cerebral injuries. EMS requires opening the dura and arachnoid layer of the cerebral cortex, then placing a vascularized section of temporalis muscle directly over it ( Fig. 3 ). The muscle then is sutured or tacked up to the superior aspect of the durotomy, to prevent mobility of the muscle, and resultant mass effect. The dural flap is sutured back in place over the muscle, allowing a portion of the temporalis to enter the inferior aspect of the durotomy. A small craniectomy at the site where the temporalis enters the calvarium may be necessary to prevent ischemic compression of the muscle. Over time, collateral angiogenesis will develop between the vascular-rich muscle and the ischemic underlying cerebral tissue. One must be careful to allow the inflow vessels of the transplant to be patent and perfusing through the temporalis muscle by not applying too much pressure on it with the head wrap. Touho and colleagues have described a gracilis muscle transplantation technique, unilaterally and bilaterally, to revascularize frontal and occipital regions with good results.

Encephalomyosynangiosis (EMS). The temporalis muscle is freed from its fascia and placed directly on the exposed surface of the brain. The dura is reflected posteriorly.

Takeuchi and colleagues performed EMS on 13 patients and 24 total hemispheres. Seventy-five percent of these patients achieved revascularization in more than one third of the MCA distribution. In addition, seven of these patients presented with transient ischemic attacks (TIAs) preoperatively, and four of seven had complete resolution of the TIAs, the remainder having significant decreases in the frequency of TIAs postoperatively. Similar good results were reported by Caldarelli and colleagues. Disadvantages of EMS include the need for a larger craniotomy, and reported postoperative complications include seizures, mass effect from the muscle, and associated increase in intracranial pressure. A case report by Touho described calcification of the graft with significant mass effect and ischemia 6 years after EMS. This complication resulted in removal of the graft. The use of EMS now is incorporated more often into a combination of procedures and used less frequently as a single operation.

Encephaloarteriosynangiosis

Encephaloarteriosynangiosis (EAS) is mainly an intermediate procedure most often used as part of an EDAS or EDAMS. It, however, has been described as a single procedure in the past when a direct anastomosis between the STA and the MCA cannot be achieved due to MCA insufficiency, especially in posthemorrhagic presentation of moyamoya disease. Because it is commonly used as part of the EDAS or EDAMS, the results on its isolated use are not readily available. The technique involves first carefully dissecting the STA. It then is retracted softly while a temporal craniotomy and durotomy are performed. The STA then simply is placed in contact with the brain. Using this technique, Touho recently reported complete resolution of TIAs in 19 of 21 operative sides, with the remaining two sides having marked decrease in TIA frequency. Houkin and colleagues found that neovascularization from the superficial temporal artery in EAS often was insufficient and that the deep temporal artery (temporalis muscle) and middle meningeal artery (dura) were better sources. Thus EAS, like EMS, often is used in combination with other procedures both direct and indirect.

Encephalodurosynangiosis

Encephalodurosynangiosis (EDS) is also an intermediate procedure that is used as part of the EDAS or the EDAMS. EDS involves the direct placement of dura with its blood supply (usually the middle meningeal artery) on the pial surface. The same principle can be applied in a more localized fashion by a burr hole with a dural incision as described with the MBH technique. EDS is used most commonly to generate collaterals to ischemic anterior cerebral artery (ACA) territories. This procedure, like the EMS and the EAS mentioned previously, can be used in combination with other procedures both direct and indirect. As an isolated procedure, EDS has not been studied in depth, and results of its isolated use are not available.

Encephalomyoarteriosynangiosis

Encephalomyoarteriosynangiosis (EMAS) is also basically a sum of its parts. Matsushima and colleagues explained the procedure in detail. They described it in variants of a frontal EMAS. In the frontal EMAS, the anterior superficial temporal artery is exposed using a cut-down technique, and then divided distally to make a muscle flap attached to it. The skin incision is extended to create a horseshoe skin flap with the epicenter in the anteroinferior skull, at the origin of the STA. A craniotomy then is performed and the dura resected. The temporalis muscle flap with the STA branch attached is sutured to the dural edge to make contact with the frontal cortical surface. This technique can be applied to posterior and middle cerebral circulation as well using the posterior branch of the superficial temporal artery and the posterior auricular or the occipital artery as needed. In Matsushima’s study, 10 patients and 16 hemispheres were studied. The results of this technique yielded vascular collateral formation in 88% of the procedures as evidenced by angiogram at 25 months after surgery. EMAS was used as a combined technique in this study and therefore clinical outcomes were not directly correlated to revascularization from EMAS alone.