8.1 History and Initial Description

Although most flow-augmentation bypass techniques aim to revascularize the middle cerebral artery (MCA) territory, augmentation of cerebral blood flow (CBF) of the frontal areas is of importance, especially in the pediatric population affected by moyamoya vasculopathy (MMV). Bifrontal hypoperfusion plays a deleterious role in intellectual development and cognitive performance, and in lower extremity and sphincter function. ^{1 ,​ 2}

In pediatric MMV, CBF in the bifrontal areas and in the anterior watershed territory as well as in the anterior MCA regions may continue to worsen despite good collateral formation or successful revascularization of the MCA territory. Therefore, it is important to consider timely revascularization of the frontal areas to prevent neurocognitive decline in pediatric patients. ²

Besides the direct STA to anterior cerebral artery (STA–ACA) bypass, ³ indirect and combined bypass techniques have been proposed for bifrontal reinforcement of blood supply. ⁴

We describe a technique of combined flow-augmentation bypass for managing MMV in children. This technique represents a modification of existing techniques ^{1 ,​ 5} .

In fact Kim et al reported in 2003 on unilateral encephalo-duro-arterio-synangiosis (EDAS) and bifrontal encephalo-galeo(periosteal)-synangiosis (EGPS) for treating pediatric moyamoya disease. ⁶ Two separate scalp incisions (one for EDAS and one for EGPS) and a bifrontal 4 × 8 cm craniotomy across the superior sagittal sinus were performed. The prepared galea was inserted deep in the interhemispheric fissure.

Park et al reported in 2007 on a modified EDAS with bifrontal EGPS. ¹ The authors increased the area of synangiosis by the use of a dural flap (inserted in into each interhemispheric fissure) in addition to a galeoperiosteal flap (that was used to cover the paramedian anterior frontal lobe). Also in this case, two scalp incisions were performed.

The particularity of our technique is the one-stage surgical approach, combining direct and indirect revascularization techniques in three different vascular regions: the MCA territory unilaterally and the frontal areas bilaterally.

The procedure consists of: (1) a direct superficial temporal artery-to-middle cerebral artery (STA–MCA) bypass with encephalo-duro-myo-synangiosis (EDMS) for unilateral MCA revascularization, and (2) a bifrontal encephalo-duro-periosteal-synangiosis (EDPS) for bifrontal revascularization. ^{4 ,​ 7}

Direct STA–MCA bypass increases flow immediately and EDMS promotes progressive neoangiogenesis over time in the MCA territory. Bifrontal EDPS aims at inducing progressive neoangiogenesis over the frontal lobes bilaterally.

We first described this technique in 2014. ⁷ In 2015 we reported on the early postoperative and short-term (within 30 days) results of eight consecutive children treated with this technique. ⁴ The results showed that the technique is feasible and safe for treating children with moyamoya. Data on long-term clinical, neuropsychological, radiological, and hemodynamic follow-up of the whole case series are currently being collected. ⁴

8.2 Indications

We perform this one-step revascularization procedure in children with hemodynamic compromise (impaired CBF and/or cerebrovascular reserve [CVR]) and clinical symptoms involving concurrently both the MCA territory and the bifrontal areas. ⁴

In addition to symptoms that can be ascribed to the MCA territory, children may present with lower extremity motor weakness and neuropsychological dysfunctions probably due to involvement of the frontal lobes. ^{1 ,​ 2 ,​ 8 – 10} In pediatric MMV, the CBF in the bifrontal areas as well as in the anterior watershed territory may continue to worsen despite good collateral formation or successful revascularization of the MCA territory. ^{1 ,​ 2 ,​ 9 ,​ 10} Therefore, it is important to consider timely revascularization of the frontal areas to prevent neurocognitive decline in pediatric patients. ^{1 ,​ 2 ,​ 8 – 10}

Direct revascularization by STA–ACA anastomosis in children can be technically challenging due to a small caliber of the cortical recipient of the ACA and very distal preparation of the frontal branch of the STA. ⁴

Preoperative workup includes magnetic resonance imaging (MRI), six-vessel digital subtraction angiography (DSA), H₂O-positron emission tomography (PET) with and without acetazolamide challenge to study CBF and CVR and neuropsychological evaluation.

8.3 Key Principles

Adequate CBF supply in the bifrontal areas is of importance, especially in pediatric moyamoya patients. ^{1 ,​ 7} Cerebral ischemia in this region can in fact lead to lower extremity motor weakness and to intellectual and neuropsychological dysfunction. ¹ Stepwise decline of neurocognitive performance has been described in 44% of the pediatric population. ¹¹ There is also growing evidence that decreased CBF, especially in the frontal lobes, is correlated with diminished neurocognitive development. ¹²

In theory, by surgically restoring blood flow in the bifrontal areas, one expects a beneficial effect on neurocognitive performance. ² An analysis of neurocognitive profiles pre- and postoperatively on 65 pediatric patients with MMV operated by means of a combination of indirect bypass procedures was recently presented. Unilateral EDAS was performed in 12 patients, bilateral EDAS in 11 patients, and bilateral EDAS and bifrontal EGPS in 42 patients. This study showed a retained intelligence quotient (IQ) and a significant improvement in performance IQ after surgery. ¹¹ The benefits of bifrontal revascularization on long-term cognitive outcome in children with MMV, however, remain to be established in larger clinical series. ⁴

The use of frontal pericranial flaps to induce neoangiogenesis in patients with MMV has shown to be effective. ^{1 ,​ 5} The use of periosteum (frontal pericranium) for bifrontal revascularization relies on the abundant blood supply. ¹ The frontal pericranium receives from the supraorbital and supratrochlear arteries (as well as from frontal branches of the STA). ¹³