Giuseppe Esposito, Annick Kronenburg, Jorn Fierstra, Kees P.J. Braun, Catharina J.M. Klijn, Albert van derZwan, and Luca Regli
Abstract
Augmentation of cerebral blood flow (CBF) of the frontal areas is of importance in symptomatic pediatric moyamoya population. Bifrontal hypoperfusion in fact plays a deleterious role in intellectual development and cognitive performance, and in lower extremity and sphincter function.
In this chapter, we describe a technique of combined flow-augmentation bypass for managing moyamoya in children. The particularity of this technique is the one- stage surgical approach, combining direct and indirect revascularization techniques in three different vascular regions: the middle cerebral artery (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.
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.
The indication to perform the one-step combined revascularization procedure is in the presence of children with hemodynamic compromise (impaired CBF and/or cerebrovascular reserve [CVR]) and clinical symptoms involving concurrently both the MCA territory and the bifrontal areas.
Bifrontal EDPS by itself could also be used as a supplementary procedure in patients who already underwent previous revascularization procedures, in case of bifrontal hypoperfusion or progression of the moyamoya vasculopathy with symptoms referable to frontal lobe hypoperfusion.
Keywords: bypass, cerebral revascularization, children, frontal areas, moya, pediatric, periosteum, synangiosis
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 neuro- cognitive 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 techniques1,5.
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*8cm 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
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.
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 neuro- cognitive 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 neuro- cognitive 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 sup- ply.1 The frontal pericranium receives from the supraorbital and supratrochlear arteries (as well as from frontal branches of the STA).13
The strengths of this technique are as follows:
• Revascularization of both frontal areas with reduced risk of injuries to the superior sagittal sinus (SSS) and the parasagittal veins. This is obtained by the use of two separate parasagittal frontal craniotomies, located 2 cm away from the midline and the SSS. Similarly, this technique avoids exposure and opening of the interhemispheric fissure.4,7
• Expanding the area of synangiosis by inverting and reflecting dural flaps under the craniotomy edges. This expands thereby the cortical coverage area for neoangiogenesis.
• Good cosmetic results: the scalp is not incised separately for this combined procedure. The skin incision is located behind the hairline and requires no shaving. The use of a single skin incision (either curvilinear or in a zig-zag fashion) and three craniotomies gives excellent cosmetic results.
• No compromise of other revascularization strategies: the technique does not compromise eventual future contralateral MCA territory revascularization, as well as revascularization procedures in the posterior circulation territory.4
• Easy procedure: the EDPS is technically easy to perform. EDPS represents therefor a very useful alternative to the existing indirect procedures for frontal lobe revascularization or to direct STA-ACA bypass for revascularization of frontal areas.1 STA-ACA bypass is known to be technically challenging, especially in pediatric patients. In fact the site of microanastomosis into the ACA territory needs a very distal preparation of the STA frontal branch and the cortical recipient of the ACA is generally also very small and often located in a sulcus. Furthermore, performing a direct STA-ACA bypass may be difficult in combination with a direct STA-MCA bypass.4,7
The opportunities offered by this technique are as follows:
• Revascularization in one session of three different vascular regions: the MCA territory unilaterally and the frontal areas bilaterally.
• Combination of direct and indirect revascularization procedures: 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 areas bilaterally.4,7
The main weaknesses and threats of this technique are as follows:
• Long duration of surgery: in 8 cases the mean duration of the procedure (from incision to closure of the skin) was 6 hours and 54 minutes (range, 5:10-9:35).
• Possibility of considerable blood loss (with three craniotomies) in children. However, the immediate postoperative and short-term (within 30 days) followup confirms the feasibility and safety of this technique.4
No contraindications for indirect revascularization of bifrontal areas via EDPS and of MCA territory via EDMS are reported. Direct revascularization via STA-MCA bypass may not be feasible if a suitable donor vessel (STA) is absent.
Patients undergo surgery under aspirin. Intraoperatively, no heparin is used.
Besides all the classical risks of every neurosurgical procedures via craniotomy, the parents should be informed that, despite the above reported advantages, the procedure represents a long surgery, mostly for young children. Eventual necessity of blood transfusion must be mentioned. Classical risks connected with every direct revascularization procedure via bypass need also to be elucidated: bypass malfunction and eventual reoperation for bypass revision, hyperperfusion syndrome (epilepsy, etc.), postoperative hemorrhage and infarcts.
Children are encouraged to have a higher than normal fluid intake (according to their weight) overnight, until 1.5 hours before anesthesia. The environment is adapted to avoid preoperative stress and hyperventilation. Lines and routine laboratory examinations are performed after the child is anesthetized. Peri- and postoperatively we aim at normotension, normovolemia, normoventilation and normothermia.
After the operation, children are observed in an intensive care unit for the first night, before they move to the medium care unit and thereafter to the ward.
MRI-MRA of the child is performed postoperatively prior to discharge.4
MMV is a progressive disease; therefore, at 1-year follow-up, we perform the same workup as done preop- eratively (described earlier in Chapter 8.2).
The patient is placed supine, the head mildly extended and 30-degree rotated to the opposite side. In case of the use of any frame, take notion of the risk of damaging the STA on the other side as this would compromise future STA-MCA bypass on the opposite side. We do not shave the hair.4
8.9.1 Direct (STA-MCA) and Indirect (EDMS) Bypass for Unilateral MCA Territory Revascularization
The incision starts over the parietal branch of the STA. The STA-MCA bypass is performed according to the classic technique described elsewhere.14 Shortly, the parietal branch of the STA branch is dissected and prepared with the microscope: the STA is kept intact up to the anastomotic procedure (Fig. 8.1a). The temporal muscle is cut along the skin incision, and a craniotomy performed on the sylvian point. The dura mater is opened in a star shaped fashion: care has to be paid to preserve the main branches of the middle meningeal artery (Fig. 8.1b). After meticulous hemostasis, the dural flaps are reflected subdurally under the bone window to obtain encephaloduro-synangiosis (EDS). The largest cortical M4 recipient artery is selected as recipient artery. A segment with no or only few cortical side branches is chosen (one to two tiny side branches may need to be interrupted) (Fig. 8.1c). A temporary nontraumatic microvascular clip is placed on the exposed STA proximally. The distal STA is cut in a fish mouth to increase the opening diameter of the donor vessel and prepared for the microanastomosis. A blue dye is applied onto the donor and recipient vessels to improve visualization during the anastomotic procedure (Fig. 8.1d). A linear arteriotomy on the cortical recipient is performed so that the microanastomosis is at least 2.5 times the size of the diameter of the recipient vessel. Two 10-0 monofilament sutures are applied at the toe and the heel of the anastomotic site to anchor the donor and recipient vessel. The microanastomosis is performed with interrupted 10-0 monofilament sutures to allow anastomosis growth with time. Before knotting the last suture, the anastomosis is flushed to clear air. Flow is reestablished by removing first the distal and then the proximal temporary clips on the cortical MCA recipient artery, and finally the clip on the proximal STA (Fig. 8.1e). Bypass patency is assessed with indocyanine green videoangiography (performed by the use of a commercially available microscope, OPMI Pentero, Carl Zeiss Co., Oberkochen, Germany) (Fig. 8.1f). The flow in the bypass is quantitatively assessed using an intra-operative flow probe (Transonic Systems Inc., Ithaca, NY). In pediatric moyamoya patients, flow values are expected to be between 15 and 50 mL per minute, depending on patients’ age, donor and recipient characteristics, and hemodynamic conditions. The microanastomosis is observed for 20 minutes to exclude decrease in flow.4 Closure is performed by covering the exposed cortex with the temporal muscle and by suturing the muscle to the dural edges (to obtain encephalo-myo-synangiosis [EMS]) (Fig. 8.1g). The bone flap is then secured into place above the muscle. Attention is paid to avoid any compression of the bypass47
8.9.2 Bifrontal EDPS
After completing the direct (STA-MCA) and indirect (EDMS) revascularization for the MCA territory, the skin incision is extended frontally 4 cm over the midline, staying behind the hairline (Fig. 8.2a). The scalp flap is reflected anteriorly and a vascularized bifrontal pericranial flap, consisting of the periosteum and the overlying loose areolar layer, is prepared (Fig. 8.2a, b). This pericranial flap is kept pediculated toward the bitemporal and biorbital regions to maximize vascular supply. This pediculated pericranial flap will serve to perform the bifrontal encephalo-periosteal-synangiosis (EPS). Two separate frontal parasagittal craniotomies (4x5 cm) are performed, one on the left and one the right side. The craniotomies extend up to 2 cm away from the midline to avoid injuring the SSS and the parasagittal veins. The dura is then opened in a star-shaped fashion and, after meticulous hemostasis, the dural flaps are inverted and reflected under the edges of each frontal bone window to obtain EDS (Fig. 8.2b). Small cortical arachnoidal openings are made. The periosteal flap is then positioned over the cortical convexity and sutured laterally to the dura (to obtain EPS) (Fig. 8.2c). Both frontal bone flaps are repositioned and fixed (Fig. 8.2d). The scalp flap is reapproximated and the skin incision closed in two layers taking care not to compromise the STA-MCA bypass.4,7
If the STA is not suitable for a direct bypass, another donor artery might be considered (posterior auricular artery), or the MCA territory has to be revascularized using an indirect technique only. We did not encounter technical difficulties for the bifrontal EDPS in our series.
Intraoperatively, bypass occlusion/malfunction may need bypass reexploration, brain swelling may occur, and anemia may necessitate transfusion.
Bifrontal EDPS by itself could also be used as a supplementary procedure in patients who already underwent previous revascularization procedures, in case of bifrontal hypoperfusion or progression of the MMV with symptoms referable to frontal lobe hypoperfusion. Bifrontal EDPS itself is doable by means of a short bifrontal incision, from one superior temporal line to the contralateral one.
References
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