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

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  • 1 Departments of Neurosurgery and
  • | 2 Radiology, Boston Children’s Hospital, Harvard Medical School, Boston, Massachusetts; and
  • | 3 University of Vermont, Burlington, Vermont
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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.

ABBREVIATIONS

ACA = anterior cerebral artery; AIS = acute ischemic stroke; DSA = digital subtraction angiography; ECA = external carotid artery; ICA = internal carotid artery; MCA = middle cerebral artery; MMD = moyamoya disease; PiPeD = pial pericranial dural; STA = superficial temporal artery; TIA = transient ischemic attack.

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.

In Brief

The authors describe a modification of indirect revascularization for the anterior cerebral artery territory in pediatric moyamoya disease. Using the pericranium and the dura mater, the approach was employed in a wide range of clinical scenarios, offering robust vascular supply that was both safe and durable, as supported by long-term clinical and radiographic follow-up.

Moyamoya disease (MMD) is an idiopathic cerebrovascular condition characterized by progressive stenosis and eventually occlusion of the intracranial internal carotid arteries (ICAs) and their two main branches, namely the anterior cerebral artery (ACA) and the middle cerebral artery (MCA), with the resulting parenchymal ischemia.1–3 In the majority of the pediatric population, the clinical presentation is largely ischemic in nature, including transient ischemic attacks (TIAs), strokes, and seizures, and depends largely on the degree of arterial involvement, the rate of progression of the steno-occlusive changes, and the regions of ischemic brain parenchyma.1,2 Generally, the MCA territory is frequently affected, either alone or with the ACA territory; isolated ACA territory ischemia in pediatric MMD is relatively rare.

However, in reviewing our pediatric MMD population over the past decade, we have identified a growing number of patients—both those referred from outside centers and some of our own patients in follow-up—who were initially treated successfully for MCA disease, but who then went on to develop progressive ACA ischemia. Surgical revascularization of the ACA territory can be challenging due to limited graft choices.4 Centers have reported a wide range of approaches, from complex adaptations of adult techniques (omental flap transfers,5–8 large interhemispheric rotational grafts,9–11 and direct bypass12–14) to the simple method of placing multiple burr holes.15–19 Each of these techniques has unique strengths and limitations, making it challenging to provide uniformly effective care to our specific patient population. Consequently, this clinical cohort prompted the development of the procedure described in this report, with the specific aim of designing a surgical approach that was tailored to children.

The use of the pericranium as a graft for indirect revascularization has been previously reported in various approaches,2,11,20 but its application for treatment of ACA territory ischemia is mostly limited to use as large, interhemispheric grafts.10 Here, we describe the clinical characteristics, surgical indications, operative technique, and long-term clinical and radiographic outcomes in a pediatric cohort with MMD affecting the ACA territory who were surgically treated with a variation of indirect revascularization surgery using the pial pericranial dural (PiPeD) revascularization technique. This technique was built on the principles of pial synangiosis, but it is 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 patients of all ages with reduced risk relative to more complex procedures.

Methods

After obtaining IRB approval at Boston Children’s Hospital to conduct the current study, we retrospectively reviewed the medical records of all pediatric patients with MMD who presented at our center between July 2009 and August 2019, in order to identify patients with anterior cerebral territory ischemia who were treated with PiPeD revascularization. This acronym, initially a lighthearted attempt to more easily refer to the specific approach, ultimately gained traction simply due to its descriptive nature. To be clear, this approach is simply a variation of indirect revascularization using the same principles employed by other surgeons—the name is more to highlight that it does not use a distinct vessel (as is the typical practice in the majority of our cases)—but focuses on the use of the pericranium and the dura mater as the vascular supply. A detailed description of the technique is provided below, and all patients who received this surgery during this time period were included in the analysis. We only included patients who were 18 years of age or younger at the time of the operation.

Data Collection

A review of the medial records of the identified cohort was conducted, and the following data were collected and analyzed: age at presentation, sex, associated medical conditions, whether the patient received cranial irradiation for a tumor, clinical presentation, disease laterality, radiographic evidence of stroke, radiographic evidence of slow blood flow on axial FLAIR MR images (“ivy sign”),1 presence of collaterals at the time of diagnosis, Suzuki stage of associated ICA disease, indications for surgery, type of surgical technique, intraoperative blood loss, intra- and postoperative complications, clinical and radiographic outcomes, and follow-up duration.

Clinical outcome was determined by the clinical condition at the last follow-up clinic visit, with special consideration to the incidence of acute ischemic stroke (AIS) and/or TIA. Radiographic outcome was determined by evaluating the most recent MRI study, especially the FLAIR sequence to assess the ivy sign, and by evaluating the most recent digital subtraction angiography (DSA) findings to assess the engraftment, evidenced by ingrowth of collateral branch vessels.

Surgical Technique

Our standard technique is a variation of pial synangiosis, which was used whenever an adequate vessel was located over the area of ischemia (see full description of pial synangiosis and the anterior variation as outlined in previous reports).1,23,24 However, in several cases, no adequate vessel was present in the surgical field, as determined by preoperative angiography and intraoperative Doppler ultrasonography. In these cases, we opted to utilize a variation of indirect revascularization that employs a combination of the pericranium and the dura mater as donor grafts, as described below. This approach was selected when no vessel was present (meaning that neither direct bypass nor pial synangiosis was an option) and was predicated on previous literature indicating that the pericranium and the dura mater can serve as effective, stand-alone grafts.25–27

This technique, which we have called PiPeD revascularization, was developed as a hybrid approach incorporating several principles derived from our institution and others.25–27 As noted above, it is employed when a donor vessel for a typical pial synangiosis is not present in the area of cortex in need of revascularization or is too small for consideration of direct bypass. The incision is marked over the brain region intended for revascularization. After skin incision, the plane between the galea and the pericranium is dissected with a Metzenbaum scissor, and a wide pericranial flap is prepared with a broad-based inferior pedicle. A craniotomy flap (typically about 5 cm in length along the sagittal axis but varied based on the age of the child) is created with an enlarged “dash-sign” burr hole fashioned at the base of the flap to allow tunneling of the pericranial graft later in the procedure without impairing its vasculature. The dura mater is opened in a stellate fashion, and the arachnoid is opened.23,24 At this point, the pericranial flap is laid in direct contact over the surface of the brain and is affixed to the pia with a 10-0 nylon suture. The dural leaflets are placed back on the brain without suturing to the brain but with 4-0 Nurolon sutures from the pericranium to the dura mater to add protection from tension on the pial stitches; then the site of the dural opening is covered with saline-soaked Gelfoam. The bone flap is replaced, and the incision is closed (Fig. 1 and Supplementary Fig. 1).

FIG. 1.
FIG. 1.

Steps of the PiPeD revascularization technique. A: The incision is marked over the brain region intended for revascularization. Note that the skin incision is anterior to the coronal suture and along the midpupillary line. B: A wide pericranial flap is prepared with a broad-based pedicle. C: A craniotomy flap is created with an enlarged “dash-sign” burr hole fashioned at the base of the flap. D: The dura mater is opened in a stellate fashion and the arachnoid is opened. E: The pericranial flap is laid in direct contact over the surface of the brain and the dural leaflets are placed back with sutures placed on both the pia (10-0 nylons) and the dura (4-0 Neurolons). F: The bone flap is replaced and fixed with low-profile mini plates and screws. Copyright Edward R. Smith. Published with permission.

Results

Our search yielded a total of 446 operations performed on 290 pediatric patients with MMD from the period July 2009 through August 2019. Of these, there were 25 PiPeD operations (5.6% of the total procedures) performed in 21 patients (7.2% of the total patients) with MMD that affected the anterior cerebral territory. Overall, 9 operations (36%) were done in patients with previously treated MCA territories and 12 operations (48%) were done for isolated ACA disease (no ipsilateral MCA disease).

Clinical Features

There were 12 females and 9 males in the cohort, with ages ranging from 1 to 16.5 years (mean 9.4 years). MMD-associated conditions were present in 6 patients (28.6%) as follows: 3 patients had neurofibromatosis type 1, 2 patients had Down syndrome, and 1 patient had Oliver-Adams syndrome and cutis aplasia. One patient had a positive family history of MMD on the maternal side. The common clinical presentations included TIAs in 8 patients (38%), AIS in 7 patients (33.3%), and seizure in 4 patients (19%). Other clinical presentations included cognitive deficits in 2 patients (9.5%) and headache in 2 patients (9.5%); however, headache was associated with other symptoms in 8 patients. MMD was incidentally discovered in 1 patient (4.8%) in the setting of brain imaging for follow-up of a prolactinoma (Table 1).

TABLE 1.

Demographics and clinical presentation

No. of Patients (%)
Sex
  F12 (57.1)
  M9 (42.9)
MMD-associated conditions6 (28.6)
  Neurofibromatosis type 13 (50)
  Down syndrome2 (33.3)
  Oliver-Adams syndrome & cutis aplasia1 (16.7)
Clinical presentation
  TIA8 (38)
  AIS7 (33.3)
  Seizure4 (19)
  Cognitive deficits2 (9.5)
  Headache2 (9.5)
  Incidental secondary finding1 (4.7)

Indications for Surgery

Surgery was recommended if patients had a preexisting diagnosis of MMD (either bilateral or unilateral) with 1) evidence of radiographic narrowing of the ACA on imaging and 2) evidence of reduced blood flow in the ACA territory (as defined by either ipsilateral ACA territory infarction or ivy sign). While we would offer surgery to asymptomatic individuals who had > 50% narrowing of the ACA with ipsilateral stroke or ivy sign, it is worth noting that all but 1 patient (95%) in this series had symptoms. Of the 20 symptomatic patients, only 4 (20%) had nonlocalizing findings (2 with headache only and 2 with cognitive decline), while 16 (80%) had clinical symptoms (focal seizure, contralateral leg-related TIA, or stroke) that localized to the ACA territory. To be clear, we would not offer surgery to patients who only had narrowing of the ACA without localizing clinical symptoms, corresponding radiographic evidence of slow flow (ivy sign), or stroke. At our institution, we rely on ivy sign with axial FLAIR MR images as evidence of slow flow and do not routinely perform other perfusion studies, such as acetazolamide challenges, or alternative MR perfusion. This is due to the risk radiation exposure poses to children, avoidance of additional anesthesia/sedation, and the variability in study acquisition.

Radiographic Characteristics

ACA territory MMD affected the right side in 8 patients, the left side in 9 patients, and was bilateral in 4 patients. ACA territory arteriopathy was associated with MMD in the same MCA territory in 11 hemispheres (44%), and with both middle cerebral and posterior cerebral territories in 2 hemispheres (8%), while 12 hemispheres (48%) had an isolated ACA disease. “Isolated ACA disease” is meant to define that found in patients with typical MCA/ACA disease on the contralateral side (e.g., a patient with isolated ACA disease might have left ACA disease in addition to concomitant MCA/ACA disease on the right). We use the phrase “isolated ACA disease” to distinguish from patients who have both MCA and ACA disease on the same side. We did not have patients who only had ACA disease without MCA disease on at least one side.

Preoperative DSA studies were available for 18 patients. The Suzuki stage of disease was stage I or II in 11 patients, stage III or IV in 5 patients, and stage V or VI in 2 patients. Five patients demonstrated intrinsic external carotid artery (ECA) to ICA collateral branches on preoperative DSA. Brain MRI with FLAIR sequence demonstrated ivy sign presence in 16 hemispheres (64%). Radiographic evidence of stroke at the ACA/MCA watershed zone was present in 7 patients (Table 2).

TABLE 2.

Radiographic findings and surgical intervention

Value
Laterality (25 hemispheres)
  Rt8 (32)
  Lt9 (36)
  Bilat8 (32)
ACA territory involvement (25 hemispheres)
  Isolated ACA disease12 (48)
  MCA11 (44)
  Middle & posterior cerebral territory2 (8)
Suzuki stage (18 patients)
  I–II11 (61.1)
  III–IV5 (27.8)
  V–VI2 (11.1)
Other radiographic findings (25 hemispheres)*
  ECA to ICA collateral branches5 (20)
  Ivy sign presence16 (64)
  Stroke at ACA/MCA watershed zone7 (28)
Surgical intervention (25 hemispheres)
  Previous pial synangiosis for MCA disease9 (36)
  Mean time btwn previous synangiosis & PiPeD, mos33.5 ± 9.4
  Mean blood loss, ml18 ± 2.2
Complications (21 patients)
  Intraop0 (0)
  Postop1 (4.8)

Categorical data are represented as number (%), and continuous data are represented as mean ± SD.

Some patients had more than one finding.

Surgical Intervention

The PiPeD revascularization procedure was performed in all patients (25 hemispheres). Previous pial synangiosis for MCA disease was performed in 9 (36%) of 25 hemispheres. The mean duration between previous synangiosis and the anterior cerebral revascularization procedure was 33.5 months (SD ± 9.4 months, range 11–75 months). The mean blood loss was 18 ml (range 10–50 ml). There were no intraoperative complications in the cohort. Only 1 patient had a superficial infection (stitch abscess), which was managed successfully. None of the patients in the cohort had postoperative strokes, hemorrhage, seizures, neural deficits, or death (Table 2).

Clinical and Radiographic Outcomes

Follow-up data were available in 18 of 21 patients (22/25 hemispheres), as 3 patients were lost to follow-up. All patients were followed up clinically and radiographically (with brain MRI including FLAIR sequence, and cerebral angiography at 1 year), with a mean follow-up duration of 24.9 months (range 4–60 months). Symptoms of TIA improved in 7 (100%) of 7 patients with preoperative TIA, and none of the patients had worsening of their preoperative ischemic symptoms. Radiographic engraftment was present in 16 (88.9%) of 18 patients (20/22 hemispheres, 90.9%); no new strokes were evident on MRI (0/18, 0%) on long-term follow-up despite radiographic progression of the disease. Of the 16 hemispheres that demonstrated preoperative ivy sign, it was markedly improved or absent in 7 hemispheres (44%), while 8 hemispheres (50%) had some documented reduction in ivy sign at follow-up, leaving only 1 patient (6.3%) without postoperative radiographic improvement of this finding. Two patients (9.5%) had worsening or progression of MMD during follow-up (Table 3).

TABLE 3.

Clinical and radiographic follow-up and outcomes

Value
Clinical follow-up (18/21 patients)
  Worsening/progression of MMD2 (9.5)
  Mean follow-up, mos24.9 ± 4.1
Clinical outcomes (18/21 patients)
  Preop TIA symptom improvement7/7 (100)
  Worsening ischemic symptoms0/18 (0)
Radiographic outcomes
  Engraftment (patients)16/18 (88.9)
  Engraftment (hemispheres)20/22 (90.9)
  New stroke0/18 (0)
  Ivy sign improvement (hemispheres)
   Complete or near complete7/16 (44)
   Partial8/16 (50)

Categorical data are represented as number (%), and continuous data are represented as mean ± SD.

Illustrative Case

A 5-year-old boy with no past medical history presented with a series of TIAs that had been occurring for a few years but were accelerating in their tempo and intensity over several months prior to presentation. Most of the TIAs he experienced were bilateral, more on the left side, and involved weakness of the arms more than legs. Brain MRI/MRA findings were consistent with bilateral MMD and demonstrated extensive ivy sign on FLAIR (Fig. 2A–C). The patient underwent bilateral pial synangiosis with an uneventful postoperative course. His TIA symptoms dramatically improved; however, 6 months later the TIAs returned, with involvement of both legs. Brain MRI was performed (Fig. 2D), which showed significant bilateral engraftment at the synangiosis sites. DSA demonstrated brisk flow through the synangiosis bilaterally (Matsushima grade A) and new, markedly worsened ACA disease (Fig. 2E–H). The decision was made to perform bilateral PiPeD revascularization of the ACA territories. The procedure was uneventful, with no postoperative complications. DSA at the 1-year follow-up demonstrated brisk flow at the PiPeD revascularization sites (Fig. 3A and B). At the 5-year follow-up visit, the patient was asymptomatic with no TIAs since the surgery, and MRI demonstrated significant reduction or disappearance of the ivy sign (Fig. 3C and D).

FIG. 2.
FIG. 2.

Illustrative case. Preoperative images. A and B: Axial T2-weighted MR images obtained at the level of the basal cisterns (A) and at the level of the basal ganglia (B) demonstrating extensive proliferation of the lenticulostriates (yellow arrows in A) and the void signals (yellow arrows in B) of the proliferated MMD collaterals. C: Axial FLAIR sequence showing ivy sign bilaterally (white arrows). D: Axial time-of-flight MRI/MRA sequence demonstrating significant bilateral engraftment at the synangiosis sites (red dotted ovals). E and F: Digital subtraction angiograms of the bilateral ICA (anteroposterior projection) demonstrating marked worsening of the ACA disease (red arrows) along with extensive proliferation of the lenticulostriates (yellow arrows). G and H: Digital subtraction angiograms of the bilateral ECA (lateral projection) demonstrating brisk flow through the synangiosis bilaterally (Matsushima grade A).

FIG. 3.
FIG. 3.

Illustrative case. Follow-up images after PiPeD revascularization. A and B: One-year follow-up digital subtraction angiograms with bilateral ECA injections in the lateral projection demonstrating brisk flow at the PiPeD revascularization sites (yellow dotted ovals) and Matsushima grade A at the previous pial synangiosis site (red dotted ovals). C and D: Axial FLAIR sequences before PiPeD revascularization (C) and at the postoperative 5-year follow-up (D) demonstrating significant reduction/disappearance of ivy sign (yellow arrows) compared with the preoperative MR images.

Discussion

The ACA territory is frequently involved as MMD vasculopathy progresses, with subsequent ischemia and hypoperfusion of this region resulting in drop attacks, lower-limb weakness, and impairment of intellectual and cognitive functions, which are crucial in the pediatric population.21,22 Early diagnosis and prompt treatment help in restoration of the ACA territory hemodynamics and improve the quality of life of such patients.4 We describe a variant surgical technique—PiPeD—that can be helpful in this location. The PiPeD technique incorporates methods used by our group and others. We have tried to be very transparent in acknowledging the contribution of previous efforts in providing various components of this strategy. Our goal in putting a name to it is to (hopefully) better codify the approach so that surgeons have a very specific technique to choose from when weighing treatment options.

Clinical and Radiographic Indications, and Timing of Surgery

Typically, the PiPeD revascularization procedure is performed as a “rescue” procedure in patients who had previous MCA revascularization and still have progressive disease affecting the ACA territory on the same hemisphere; those who have unilateral MCA disease, but progressive, new contralateral ACA disease (without contralateral MCA disease); or, less commonly, those with MMD presenting solely with isolated ACA disease. In the current study, ACA territory ischemia was associated with MMD in MCA territory in 11 hemispheres (44%) and with both MCA and PCA territories in 2 hemispheres (8%), while 12 hemispheres (48%) had isolated ACA disease.

Patient selection criteria are based on both clinical symptoms and radiographic evidence of ischemia in the ACA territory (see Indications for Surgery in Results). As noted above, this typically manifests clinically with drop attacks, lower-limb weakness, seizures, and/or intellectual dysfunction. In our cohort, 15 patients (71%) presented with ischemic symptoms of drop attacks and lower-limb weakness. Two patients (9.5%) presented with worsening school performance, memory deficit, and executive function problems. Radiographically, brain MRI/MRA is a key diagnostic tool for evaluation of cerebral ischemia. In addition to assessment of structural anatomy and detecting acute and chronic stroke burden, a FLAIR sequence is of high value in identifying areas with slow flow, demonstrated as high signal intensity (ivy sign) that represents slow flow in leptomeningeal collaterals. As noted in Indications for Surgery, we do not routinely employ additional perfusion techniques in the pediatric population, due to the risk of additional exposure and sedation/anesthesia, and the relatively minimal benefit conferred for most patients. (However, we will employ additional testing in select cases.) DSA is usually performed, as it carries high diagnostic sensitivity for disease progression and provides pertinent data that are valuable for preoperative planning, including detection of possible frontal vessels that could be used for pial synangiosis, and revealing transdural collateral branches that must be avoided during surgery to avoid risk of postoperative strokes.28

Clinically asymptomatic children who have radiographic or functional evidence of impaired cerebral perfusion should also be considered as operative candidates. This is particularly important if serial imaging confirms progressive disease. In addition, development of ivy sign on MRI—even in asymptomatic patients—portends a high risk of stroke within 2 years.30 This indication is supported by current American Heart Association/American Stroke Association recommendations.31 Surgery is usually scheduled as soon as feasible for the family, with the exception of a recent stroke. In cases of acute stroke or hemorrhage, we will often suggest waiting several weeks to reduce the risk of secondary stroke.4 In our cohort, we found a number of patients with relatively early angiographic disease (Suzuki stage I or II) in the affected hemisphere. While usually not an indication for surgery in isolation, our group (and others) has noted that in the pediatric population there is a tendency for the disease to progress relatively rapidly, even with lower Suzuki stages, especially when found in conjunction with signs of radiographic ischemia such as ivy sign or stroke, as was common in the patients in this study.30,31

Surgical Technique and Potential Advantages

There is no treatment modality known to halt or reverse the primary steno-occlusive process of MMD; however, current treatments aim to improve the cerebral perfusion, thus protecting against future strokes, decreasing the frequency of symptoms, and reducing the MMD-associated collaterals. Surgical revascularization (direct, indirect, or combined) is the fundamental treatment modality for MMD.1,4

The majority of previously reported revascularization techniques have been described and further advanced to improve the blood flow in the MCA territory; however, surgical options to restore the ACA territory hemodynamics are very limited. This might be attributed to 1) the high risk and technical challenge of direct revascularization procedures in children due to the small caliber of the vessels;29 2) limited arterial grafts of the external carotid system that could be utilized for the standard pial synangiosis, especially in the setting where a previous frontal branch of the superficial temporal artery (STA) has been used for previous MCA territory revascularization; and 3) limited vascularized graft choices for indirect revascularization, including omentum, muscle, galea, and pericranium. The sheer number of potential surgical approaches to revascularize this territory underscores the challenge it presents. We readily acknowledge the excellent work done by colleagues around the world and hope that the technique we present is viewed as an attempt to provide an additional method that tries to incorporate some of the best aspects of numerous strategies.

The first omental transfer for MMD was described by Karasawa et al.,5 where the authors anastomosed a large segment of the omentum to the STA. The omentum can be used as free graft or vascularized pedicled flap. Several authors have then advocated this technique for indirect revascularization of MMD affecting the anterior circulation.9–11 Potential disadvantages of this technique include wound infection, intracranial mass effect, constriction of the transposed graft, and abdominal hernia.2 Multiple burr holes as a surgical option for indirect revascularization has been described in small case series;15–19 however, most of the reported cases required subsequent additional revascularization procedures. Multiple burr holes may offer limited efficacy outside of infancy due to the thickness of the skull, precluding robust ingrowth of collaterals through long, narrow bony corridors. While this may have efficacy in some cases, our experience suggests that this may be less useful in older patients.

The pericranium is a unique graft for revascularization as it can be easily harvested, is highly anastomotic, and is present all over the entire skull where other vascularized tissues (e.g., muscle) for indirect revascularization are not present.2 Kinugasa et al.9 have described a ribbon interhemispheric rotational flap using the galea and the pericranium, and they reported good to excellent results in their series of 7 patients. Kim et al.10 modified the ribbon procedure, where they used a bifrontal craniotomy over the midline to insert a galeal and pericranium flap into the interhemispheric fissure. The authors reported favorable outcome of ACA symptoms in 81% of cases. In both procedures, the craniotomy flap was large in size and the superior sagittal sinus was exposed. Kuroda et al.11 used the pericranium as a graft for revascularization of ACA territory, in combination with direct STA-MCA bypass for MCA territory ischemia. Zhao et al.20 reported a modification of the above-mentioned approaches in which they used a pericranial flap through a large frontal (unilateral or bifrontal) craniotomy, however, without exposing the sinus. They reported improved outcome in 5 of 9 patients on long-term follow-up. These results are impressive, but the approaches vary in complexity and case number and have not been standardized for application in pediatric ACA territory revascularization.

Taken together, these data suggest that there is a continued need for additional methods to treat anterior circulation disease in pediatric MMD. In our institution, we have codified a technique—PiPeD revascularization—as a hybrid approach incorporating several principles derived from our program and others.25–27 The main advantage of this technique is its versatility, as it can be used directly over the ischemic brain region in need of revascularization, without being limited by the course of a donor vessel. This technique is safe, simple, less time consuming than many of the previously described methods (with the exception of burr holes, which have limited efficacy outside of very young patients),15–19 and reliable (in terms of outcome). Our average operative time from incision to closure was less than 40 minutes. As with many surgical approaches, this procedure builds on previous work, and we hope that this article will help clinicians by providing a reference that outlines a specific procedure with long-term follow-up to add another tool to their armamentarium.

Clinical and Radiographic Outcomes, With Limitations

Overall, this series demonstrates that PiPeD revascularization is a generally safe and effective technique. The surgery, performed in 21 patients in 25 hemispheres (with long-term follow-up available for 18 patients in 22 hemispheres), provided robust evidence of radiographic engraftment in 16 (88.9%) of 18 patients and 20 (90.9%) of 22 hemispheres, indicating that the pericranium and the dura mater can supply a rich collateral network that persisted over the long-term on serial imaging. Importantly, this radiographic success correlated with protection from future strokes (no new strokes were evident on long-term follow-up MRI in all 18 patients) and TIAs, despite ongoing evidence of worsening primary arteriopathy. Additionally, all patients with preoperative TIA became symptomfree (7/7 patients, 100%), and none of the patients had worsening of their preoperative ischemic symptoms. This long-term follow-up demonstrates that the technique confers durable, long-term radiographic and clinical protection from stroke in pediatric patients with MMD.

There are limitations to this approach. Our series is and needs validation in larger cohorts. We want to be careful to acknowledge that the available data will not prove the superiority of this or any procedure in the retrospective nature of how it is reported here. While not our practice to routinely utilize perfusion studies in children, we acknowledge that future work may be bolstered by additional data of this nature to help assess radiographic outcomes. Ultimately, larger multicenter studies to compare approaches for well-defined cohorts will help to improve delivery of care to patients with MMD.

Conclusions

Surgical management of ACA territory ischemia in pediatric patients with MMD is crucial. The use of the pericranium and the dura mater for indirect revascularization (PiPeD) provides 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 confers 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.

Acknowledgments

We would like to acknowledge the support of Kids@Heart and The Chae Family Fund.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: ER Smith, Montaser. Acquisition of data: ER Smith, Montaser, Driscoll, H Smith, Karsten, Day, Mounlavongsy. Analysis and interpretation of data: ER Smith, Montaser, Orbach. Drafting the article: ER Smith, Montaser, Driscoll, H Smith, Karsten, Day, Orbach. Critically revising the article: ER Smith, Montaser, Driscoll, H Smith, Karsten, Day, Mounlavongsy. Reviewed submitted version of manuscript: ER Smith, Driscoll, H Smith, Karsten, Day, Mounlavongsy, Orbach. Approved the final version of the manuscript on behalf of all authors: ER Smith. Administrative/technical/material support: ER Smith, Driscoll, H Smith, Karsten, Day, Mounlavongsy, Orbach. Study supervision: ER Smith, Montaser.

Supplemental Information

Online-Only Content

Supplemental material is available with the online version of the article.

Previous Presentations

Portions of this work were presented as an e-poster at the virtual 2020 AANS Annual Scientific Meeting.

References

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    • Crossref
    • PubMed
    • Search Google Scholar
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    Smith ER, Scott RM. Spontaneous occlusion of the circle of Willis in children: pediatric moyamoya summary with proposed evidence-based practice guidelines. A review. J Neurosurg Pediatr. 2012;9(4):353360.

    • Crossref
    • PubMed
    • Search Google Scholar
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    Karasawa J, Kikuchi H, Kawamura J, Sakai T. Intracranial transplantation of the omentum for cerebrovascular moyamoya disease: a two-year follow-up study. Surg Neurol. 1980;14(6):444449.

    • PubMed
    • Search Google Scholar
    • Export Citation
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    Karasawa J, Touho H, Ohnishi H, et al. Cerebral revascularization using omental transplantation for childhood moyamoya disease. J Neurosurg. 1993;79(2):192196.

  • 7

    Yoshioka N, Tominaga S, Suzuki Y, et al. Vascularized omental graft to brain surface in ischemic cerebrovascular disease. Microsurgery. 1995;16(7):455462.

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    Havlik RJ, Fried I, Chyatte D, Modlin IM. Encephalo-omental synangiosis in the management of moyamoya disease. Surgery. 1992;111(2):156162.

  • 9

    Kinugasa K, Mandai S, Tokunaga K, et al. Ribbon enchephalo-duro-arterio-myo-synangiosis for moyamoya disease. Surg Neurol. 1994;41(6):455461.

  • 10

    Kim SK, Wang KC, Kim IO, et al. Combined encephaloduroarteriosynangiosis and bifrontal encephalogaleo (periosteal) synangiosis in pediatric moyamoya disease. Neurosurgery. 2008;62(6)(suppl 3):14561464.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Kuroda S, Houkin K, Ishikawa T, et al. Novel bypass surgery for moyamoya disease using pericranial flap: its impacts on cerebral hemodynamics and long-term outcome. Neurosurgery. 2010;66(6):10931101.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Iwama T, Hashimoto N, Miyake H, Yonekawa Y. Direct revascularization to the anterior cerebral artery territory in patients with moyamoya disease: report of five cases. Neurosurgery. 1998;42(5):11571162.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13

    Egashira Y, Yoshimura S, Enomoto Y, et al. Single-stage direct revascularization for bilateral anterior cerebral artery regions in pediatric moyamoya disease: a technical note. World Neurosurg. 2018;118:324328.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Iwama T, Hashimoto N, Tsukahara T, Miyake H. Superficial temporal artery to anterior cerebral artery direct anastomosis in patients with moyamoya disease. Clin Neurol Neurosurg. 1997;99(suppl2):S134S136.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Endo M, Kawano N, Miyaska Y, Yada K. Cranial burr hole for revascularization in moyamoya disease. J Neurosurg. 1989;71(2):180185.

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    McLaughlin N, Martin NA. Effectiveness of burr holes for indirect revascularization in patients with moyamoya disease-a review of the literature. World Neurosurg. 2014;81(1):9198.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
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    Kapu R, Symss NP, Cugati G, et al. Multiple burr hole surgery as a treatment modality for pediatric moyamoya disease. J Pediatr Neurosci. 2010;5(2):115120.

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    Oliveira RS, Amato MCM, Simão GN, et al. Effect of multiple cranial burr hole surgery on prevention of recurrent ischemic attacks in children with moyamoya disease. Neuropediatrics. 2009;40(6):260264.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    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)(suppl):437443.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Zhao Y, Yu S, Li J, et al. Modified encephalo-duro-periosteal-synangiosis (EDPS) for the revascularization of anterior cerebral artery territory in moyamoya disease: a single-center experience. Clin Neurol Neurosurg. 2019;178:8692.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Song YS, Oh SW, Kim YK, et al. Hemodynamic improvement of anterior cerebral artery territory perfusion induced by bifrontal encephalo(periosteal) synangiosis in pediatric patients with moyamoya disease: a study with brain perfusion SPECT. Ann Nucl Med. 2012;26(1):4757.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Williams TS, Westmacott R, Dlamini N, et al. Intellectual ability and executive function in pediatric moyamoya vasculopathy. Dev Med Child Neurol. 2012;54(1):3037.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Penn DL, Wu KC, Presswood KR, et al. General principles for pial synangiosis in pediatric moyamoya patients: 2-dimensional operative video. Oper Neurosurg (Hagerstown). 2019;16(1):E14E15.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24

    Adelson PD, Scott RM. Pial synangiosis for moyamoya syndrome in children. Pediatr Neurosurg. 1995;23(1):2633.

  • 25

    King JAJ, Armstrong D, Vachhrajani S, Dirks PB. Relative contributions of the middle meningeal artery and superficial temporal artery in revascularization surgery for moyamoya syndrome in children: the results of superselective angiography. J Neurosurg Pediatr. 2010;5(2):184189.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Baaj AA, Agazzi S, Sayed ZA, et al. Surgical management of moyamoya disease: a review. Neurosurg Focus. 2009;26(4):E7.

  • 27

    Gadgil N, Lam S, Pyarali M, et al. Indirect revascularization with the dural inversion technique for pediatric moyamoya disease: 20-year experience. J Neurosurg Pediatr. 2018;22(5):541549.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Storey A, Scott RM, Robertson R, Smith E. Preoperative transdural collateral vessels in moyamoya as radiographic biomarkers of disease. J Neurosurg Pediatr. 2017;19(3):289295.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Macyszyn L, Attiah M, Ma TS, et al. Direct versus indirect revascularization procedures for moyamoya disease: a comparative effectiveness study. J Neurosurg. 2017;126(5):15231529.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Lin N, Baird L, Koss M, et al. Discovery of asymptomatic moyamoya arteriopathy in pediatric syndromic populations: radiographic and clinical progression. Neurosurg Focus. 2011;31(6):E6.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Ferriero DM, Fullerton HJ, Bernard TJ, et al. Management of stroke in neonates and children: a scientific statement from the American Heart Association/American Stroke Association. Stroke. 2019;50(3):e51e96.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

Illustration from Seaman et al. (pp 260–267). Copyright Jane Whitney. Published with permission.

  • View in gallery

    Steps of the PiPeD revascularization technique. A: The incision is marked over the brain region intended for revascularization. Note that the skin incision is anterior to the coronal suture and along the midpupillary line. B: A wide pericranial flap is prepared with a broad-based pedicle. C: A craniotomy flap is created with an enlarged “dash-sign” burr hole fashioned at the base of the flap. D: The dura mater is opened in a stellate fashion and the arachnoid is opened. E: The pericranial flap is laid in direct contact over the surface of the brain and the dural leaflets are placed back with sutures placed on both the pia (10-0 nylons) and the dura (4-0 Neurolons). F: The bone flap is replaced and fixed with low-profile mini plates and screws. Copyright Edward R. Smith. Published with permission.

  • View in gallery

    Illustrative case. Preoperative images. A and B: Axial T2-weighted MR images obtained at the level of the basal cisterns (A) and at the level of the basal ganglia (B) demonstrating extensive proliferation of the lenticulostriates (yellow arrows in A) and the void signals (yellow arrows in B) of the proliferated MMD collaterals. C: Axial FLAIR sequence showing ivy sign bilaterally (white arrows). D: Axial time-of-flight MRI/MRA sequence demonstrating significant bilateral engraftment at the synangiosis sites (red dotted ovals). E and F: Digital subtraction angiograms of the bilateral ICA (anteroposterior projection) demonstrating marked worsening of the ACA disease (red arrows) along with extensive proliferation of the lenticulostriates (yellow arrows). G and H: Digital subtraction angiograms of the bilateral ECA (lateral projection) demonstrating brisk flow through the synangiosis bilaterally (Matsushima grade A).

  • View in gallery

    Illustrative case. Follow-up images after PiPeD revascularization. A and B: One-year follow-up digital subtraction angiograms with bilateral ECA injections in the lateral projection demonstrating brisk flow at the PiPeD revascularization sites (yellow dotted ovals) and Matsushima grade A at the previous pial synangiosis site (red dotted ovals). C and D: Axial FLAIR sequences before PiPeD revascularization (C) and at the postoperative 5-year follow-up (D) demonstrating significant reduction/disappearance of ivy sign (yellow arrows) compared with the preoperative MR images.

  • 1

    Scott RM, Smith ER. Moyamoya disease and moyamoya syndrome. N Engl J Med. 2009;360(12):12261237.

  • 2

    Wanebo JE, Khan N, Zabramski JM. Spetzler RF Moyamoya Disease: Diagnosis and Treatment. Thieme; 2013.

  • 3

    Suzuki J, Takaku A. Cerebrovascular “moyamoya” disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol. 1969;20(3):288299.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Smith ER, Scott RM. Spontaneous occlusion of the circle of Willis in children: pediatric moyamoya summary with proposed evidence-based practice guidelines. A review. J Neurosurg Pediatr. 2012;9(4):353360.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Karasawa J, Kikuchi H, Kawamura J, Sakai T. Intracranial transplantation of the omentum for cerebrovascular moyamoya disease: a two-year follow-up study. Surg Neurol. 1980;14(6):444449.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Karasawa J, Touho H, Ohnishi H, et al. Cerebral revascularization using omental transplantation for childhood moyamoya disease. J Neurosurg. 1993;79(2):192196.

  • 7

    Yoshioka N, Tominaga S, Suzuki Y, et al. Vascularized omental graft to brain surface in ischemic cerebrovascular disease. Microsurgery. 1995;16(7):455462.

  • 8

    Havlik RJ, Fried I, Chyatte D, Modlin IM. Encephalo-omental synangiosis in the management of moyamoya disease. Surgery. 1992;111(2):156162.

  • 9

    Kinugasa K, Mandai S, Tokunaga K, et al. Ribbon enchephalo-duro-arterio-myo-synangiosis for moyamoya disease. Surg Neurol. 1994;41(6):455461.

  • 10

    Kim SK, Wang KC, Kim IO, et al. Combined encephaloduroarteriosynangiosis and bifrontal encephalogaleo (periosteal) synangiosis in pediatric moyamoya disease. Neurosurgery. 2008;62(6)(suppl 3):14561464.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Kuroda S, Houkin K, Ishikawa T, et al. Novel bypass surgery for moyamoya disease using pericranial flap: its impacts on cerebral hemodynamics and long-term outcome. Neurosurgery. 2010;66(6):10931101.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Iwama T, Hashimoto N, Miyake H, Yonekawa Y. Direct revascularization to the anterior cerebral artery territory in patients with moyamoya disease: report of five cases. Neurosurgery. 1998;42(5):11571162.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13

    Egashira Y, Yoshimura S, Enomoto Y, et al. Single-stage direct revascularization for bilateral anterior cerebral artery regions in pediatric moyamoya disease: a technical note. World Neurosurg. 2018;118:324328.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Iwama T, Hashimoto N, Tsukahara T, Miyake H. Superficial temporal artery to anterior cerebral artery direct anastomosis in patients with moyamoya disease. Clin Neurol Neurosurg. 1997;99(suppl2):S134S136.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Endo M, Kawano N, Miyaska Y, Yada K. Cranial burr hole for revascularization in moyamoya disease. J Neurosurg. 1989;71(2):180185.

  • 16

    McLaughlin N, Martin NA. Effectiveness of burr holes for indirect revascularization in patients with moyamoya disease-a review of the literature. World Neurosurg. 2014;81(1):9198.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Kapu R, Symss NP, Cugati G, et al. Multiple burr hole surgery as a treatment modality for pediatric moyamoya disease. J Pediatr Neurosci. 2010;5(2):115120.

  • 18

    Oliveira RS, Amato MCM, Simão GN, et al. Effect of multiple cranial burr hole surgery on prevention of recurrent ischemic attacks in children with moyamoya disease. Neuropediatrics. 2009;40(6):260264.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    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)(suppl):437443.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Zhao Y, Yu S, Li J, et al. Modified encephalo-duro-periosteal-synangiosis (EDPS) for the revascularization of anterior cerebral artery territory in moyamoya disease: a single-center experience. Clin Neurol Neurosurg. 2019;178:8692.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Song YS, Oh SW, Kim YK, et al. Hemodynamic improvement of anterior cerebral artery territory perfusion induced by bifrontal encephalo(periosteal) synangiosis in pediatric patients with moyamoya disease: a study with brain perfusion SPECT. Ann Nucl Med. 2012;26(1):4757.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Williams TS, Westmacott R, Dlamini N, et al. Intellectual ability and executive function in pediatric moyamoya vasculopathy. Dev Med Child Neurol. 2012;54(1):3037.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Penn DL, Wu KC, Presswood KR, et al. General principles for pial synangiosis in pediatric moyamoya patients: 2-dimensional operative video. Oper Neurosurg (Hagerstown). 2019;16(1):E14E15.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24

    Adelson PD, Scott RM. Pial synangiosis for moyamoya syndrome in children. Pediatr Neurosurg. 1995;23(1):2633.

  • 25

    King JAJ, Armstrong D, Vachhrajani S, Dirks PB. Relative contributions of the middle meningeal artery and superficial temporal artery in revascularization surgery for moyamoya syndrome in children: the results of superselective angiography. J Neurosurg Pediatr. 2010;5(2):184189.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Baaj AA, Agazzi S, Sayed ZA, et al. Surgical management of moyamoya disease: a review. Neurosurg Focus. 2009;26(4):E7.

  • 27

    Gadgil N, Lam S, Pyarali M, et al. Indirect revascularization with the dural inversion technique for pediatric moyamoya disease: 20-year experience. J Neurosurg Pediatr. 2018;22(5):541549.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Storey A, Scott RM, Robertson R, Smith E. Preoperative transdural collateral vessels in moyamoya as radiographic biomarkers of disease. J Neurosurg Pediatr. 2017;19(3):289295.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Macyszyn L, Attiah M, Ma TS, et al. Direct versus indirect revascularization procedures for moyamoya disease: a comparative effectiveness study. J Neurosurg. 2017;126(5):15231529.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Lin N, Baird L, Koss M, et al. Discovery of asymptomatic moyamoya arteriopathy in pediatric syndromic populations: radiographic and clinical progression. Neurosurg Focus. 2011;31(6):E6.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Ferriero DM, Fullerton HJ, Bernard TJ, et al. Management of stroke in neonates and children: a scientific statement from the American Heart Association/American Stroke Association. Stroke. 2019;50(3):e51e96.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

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