Long-term clinical and radiographic outcomes after pial pericranial dural revascularization: a hybrid surgical technique for treatment of anterior cerebral territory ischemia in pediatric moyamoya disease

Abstract

OBJECTIVE Isolated anterior cerebral artery (ACA) territory ischemia in pediatric moyamoya disease (MMD) is rare but has been increasingly recognized, particularly in children manifesting progression of disease in a delayed fashion after middle cerebral artery revascularization surgery. Surgical treatment is complicated by limited graft choices, with the small number of case series largely focused on complex, higher-risk operations (omental flap transfers, large interhemispheric rotational grafts); direct bypass (often untenable in children due to vessel size); or, alternatively, the technically simpler method of multiple burr holes (of limited efficacy outside of infants). Faced with the problem of a growing cohort of pediatric patients with MMD that could benefit from anterior cerebral revascularization, the authors sought to develop a solution that was specifically designed for children and that would be lower risk than the more complex approaches adapted from adult populations but more effective than simple burr holes. In this study, the authors aimed to describe the long-term clinical and radiographic outcomes of a novel approach of pial pericranial dural (PiPeD) revascularization, building on the principles of pial synangiosis but unique in using the pericranium and the dura mater as the primary vascular supply, and employing a larger craniotomy with arachnoid dissection to provide robust full-territory revascularization in all ages with reduced risk relative to more complex procedures. METHODS The medical records of all pediatric patients with MMD who presented at a single center between July 2009 and August 2019 were retrospectively reviewed to identify patients with MMD with anterior cerebral territory ischemia. Clinical characteristics, surgical indications, operative techniques, and long-term clinical and radiographic follow-up data were collected and analyzed. RESULTS A total of 25 operations (5.6% of total procedures) were performed in 21 patients (mean age 9.4 years [range 1–16.5 years]; 12 female and 9 male). Almost one-third of the patients had syndromic associations, with no familial cases. Complications included 1 patient (4.7%) with a superficial infection, with no postoperative strokes, hemorrhage, seizures, or deaths. Long-term follow-up was available in 18 of 21 patients (mean 24.9 months [range 4–60 months]). Radiographic engraftment was present in 90.9% (20/22 hemispheres), and no new strokes were evident on MRI on long-term follow-up, despite radiographic progression of the disease. CONCLUSIONS The use of the pericranium and the dura mater for indirect revascularization provided robust vascularized graft with great flexibility in location and high potential for engraftment, which may obviate more complex and higher-risk operations for ACA territory ischemia. Long-term follow-up demonstrated that PiPeD revascularization conferred durable, long-term radiographic and clinical protection from stroke in pediatric patients with MMD. Based on the results of the current study, the PiPeD technique can be considered an additional tool to the armamentarium of indirect revascularization procedures in select pediatric patients with MMD.

Wide Arterial Sparing Encephalo-Duro-Synangiosis for Moyamoya: Surgical Technique and Outcomes

“…They note that although EDAS has been successful for most, looking beyond this technique may be beneficial for larger surface area and multiple territory revascularization. 21 In our experience, WASEDS is a safe and effective indirect cerebral revascularization procedure with several advantages: (1) It is an effective salvage technique after failure of other surgical treatment; (2) on the surface, the larger craniotomy and extent of dural slits may provide wider cortical coverage than traditional procedures, and imaging shows extensive collateralization across the hemisphere with enlargement of associated MMA vasculature (Figure 4); and (3) unlike EDAS or external carotid to internal carotid bypass, it preserves large-sized and medium-sized MMA branches, thus preserving their terminal collateralization with intracranial vasculature.…”

“…They note that although EDAS has been successful for most, looking beyond this technique may be beneficial for larger surface area and multiple territory revascularization. 21…”

Magnetic Resonance Imaging/Angiography Versus Catheter Angiography for Annual Follow-up of Pediatric Moyamoya Patients: A Cost Outcomes Analysis

“…2 The median duration of follow-up was 31 months, ranging up to 110 months. Most patients underwent bilateral pial synangiosis (n = 62, 76%), with the remaining group receiving other indirect revascularization, including pial pericranial dural 11 or myosynangiosis.…”

“…12 This is also the case for moyamoya in the pediatric population, where DSA is frequently used to assess patients in the postoperative period. 11,[13][14][15][16][17][18][19][20] However, MRI/A has shown similar efficacy in diagnostic performance compared with DSA when following other cerebral vascular lesions, including aneurysms 21 and arteriovenous malformations. 22 Given recent evidence that Matsushima grade does not correlate with clinical outcome or hypovascular territories 8 and that the ivy sign scoring system provides useful and prognostic clinical data, 9 MRI/A could potentially halve the number of DSA studies for many moyamoya patients.…”

Surgical revascularizations for pediatric moyamoya: a systematic review, meta-analysis, and meta-regression analysis

“…Direct bypass (DB) is accomplished by anastomosing extracranial vessels to intracranial vessels (EC-IC bypass), most often the superficial temporal artery (STA) to the middle cerebral artery (MCA) (STA-MCA bypass) [3,4]. Indirect bypass (IB) has many variations but is generally accomplished by incorporating well-vascularized tissue usually from external carotid artery sources onto the surface of the brain to promote angiogenesis and neovascularization, rather than by direct anastomosis [5][6][7][8][9]. Unlike DB, IB begins to alter the cerebral blood flow only after angiogenesis has taken place, the timescale for which is unpredictable [3].…”