Moyamoya syndrome and PHACE syndrome: clinical and radiographic characterization of the intracranial arteriopathy and response to surgical revascularization

Sarah Jernigan Departments of Neurosurgery and

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 MD, MPH
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Armide Storey Departments of Neurosurgery and

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 BA
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Christine Hammer Departments of Neurosurgery and

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Coleman Riordan Departments of Neurosurgery and

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Darren B. Orbach Departments of Neurosurgery and
Neurointerventional Radiology, Boston Children’s Hospital, Harvard Medical School, Boston, Massachusetts

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 MD, PhD
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R. Michael Scott Departments of Neurosurgery and

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Edward Smith Departments of Neurosurgery and

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OBJECTIVE

PHACE syndrome (PHACES) has been linked to cervical and cerebral vascular anomalies, including persistent embryonic anastomoses and progressive steno-occlusive disease. However, no prior studies have documented the long-term response of PHACES patients with moyamoya disease to surgical revascularization with pial or myosynangiosis. The authors present their experience with 8 consecutive patients with PHACES and moyamoya disease.

METHODS

Retrospective review of patients who underwent pial synangiosis revascularization for moyamoya disease with concurrent diagnosis of PHACES.

RESULTS

A total of 8 patients out of 456 surgically treated moyamoya patients had a diagnosis of PHACES. All patients were female, and their average age at the time of surgical treatment was 9.3 years (range 1.8–25.8 years). Five patients had associated basilar artery anomalies or stenosis. All patients had symptomatic narrowing of the petrous segment of the internal carotid artery with tortuous collateralization. Three patients underwent unilateral pial or myo-synangiosis and 5 underwent bilateral procedures. The average hospital length of stay was 5.0 days (range 3–7 days). There were no postoperative complications. Follow-up ranged from 8 to 160 months (average 56 months). Seven of 8 patients have had follow-up angiograms and all had Matsushima grade A or B collateralization without progression of stenosis in other locations. All patients had reduced cortical FLAIR signal on 6-month follow-up MRI and no evidence of new radiographic or clinical strokes.

CONCLUSIONS

Patients with moyamoya disease and PHACES had an intracranial arteriopathy characterized by ectactic anterior vasculature with concomitant basilar artery stenosis, and were all female. The patients had both radiographic and clinical responses to pial synangiosis. The surgical treatment of these patients can be challenging given facial hemangiomas located near the surgical field. Patients with unilateral disease did not have evidence of progression in other cerebral circulation during the given follow-up period.

ABBREVIATIONS

ADL = activities of daily living; mRS = modified Rankin Scale; PHACES = PHACE syndrome; TIA = transient ischemic attack.

OBJECTIVE

PHACE syndrome (PHACES) has been linked to cervical and cerebral vascular anomalies, including persistent embryonic anastomoses and progressive steno-occlusive disease. However, no prior studies have documented the long-term response of PHACES patients with moyamoya disease to surgical revascularization with pial or myosynangiosis. The authors present their experience with 8 consecutive patients with PHACES and moyamoya disease.

METHODS

Retrospective review of patients who underwent pial synangiosis revascularization for moyamoya disease with concurrent diagnosis of PHACES.

RESULTS

A total of 8 patients out of 456 surgically treated moyamoya patients had a diagnosis of PHACES. All patients were female, and their average age at the time of surgical treatment was 9.3 years (range 1.8–25.8 years). Five patients had associated basilar artery anomalies or stenosis. All patients had symptomatic narrowing of the petrous segment of the internal carotid artery with tortuous collateralization. Three patients underwent unilateral pial or myo-synangiosis and 5 underwent bilateral procedures. The average hospital length of stay was 5.0 days (range 3–7 days). There were no postoperative complications. Follow-up ranged from 8 to 160 months (average 56 months). Seven of 8 patients have had follow-up angiograms and all had Matsushima grade A or B collateralization without progression of stenosis in other locations. All patients had reduced cortical FLAIR signal on 6-month follow-up MRI and no evidence of new radiographic or clinical strokes.

CONCLUSIONS

Patients with moyamoya disease and PHACES had an intracranial arteriopathy characterized by ectactic anterior vasculature with concomitant basilar artery stenosis, and were all female. The patients had both radiographic and clinical responses to pial synangiosis. The surgical treatment of these patients can be challenging given facial hemangiomas located near the surgical field. Patients with unilateral disease did not have evidence of progression in other cerebral circulation during the given follow-up period.

In Brief

The authors evaluated the long-term response to surgical revascularization in patients with both PHACE syndrome (PHACES) and moyamoya syndrome. This is the first case series to describe the intracerebral vascular anomalies in PHACES and the response of PHACES-associated moyamoya syndrome to surgical treatment.

Phace syndrome (PHACES) is a congenital neurocutaneous condition that manifests as plaque-like facial hemangiomas along with one (or more) of the following: posterior fossa brain malformations, cerebrovascular arterial anomalies, structural cardiovascular disorders, eye anomalies, and ventral developmental defects, such as sternal defects or a supraumbilical raphe.10 Its etiology and pathogenesis are unknown and there is a significant female predominance, with a female/male ratio of 9:1. PHACES has been linked to cervical and cerebral vascular anomalies, including persistent embryonic anastomoses and progressive steno-occlusive disease. The moyamoya syndrome found in association with PHACES shows narrowing of the internal carotid artery in the petrous segment as well as intracerebral vascular tortuosity and frequent basilar artery stenosis. These cerebrovascular anomalies and vasculopathy lead to an increased risk of early strokes. No prior series has documented the response of PHACES patients with moyamoya syndrome to pial synangiosis revascularization. We present our experience with 8 consecutive patients with PHACES and moyamoya syndrome.

Methods

This was a retrospective review of 8 cases in which patients were identified as having both moyamoya syndrome and PHACES from a database of 465 patients undergoing pial or myo-synangiosis revascularization for moyamoya syndrome or disease at Boston Children’s Hospital between 1988 and 2012. Institutional board review approval was obtained. The charts of these patients were retrospectively reviewed to determine demographics and symptomatology at presentation, radiological studies (including CT, MRI/MR angiography, and cerebral angiography), perioperative and late complications, length of follow-up, and long-term clinical and radiographic outcomes. The functional status of each patient was evaluated using the modified Rankin Scale (mRS; 0 = no symptoms, 1 = minor symptoms not affecting lifestyle, 2 = minor handicap but independent in activities of daily living [ADL], 3 = requiring some help with ADL, 4 = requiring substantial help with ADL, 5 = totally dependent).

Results

Patient Demographics

Of the 456 patients treated for moyamoya syndrome, 8 (1.8%) also had a diagnosis of PHACES. All 8 patients were female. Their average age at presentation was 9.3 years (range 1.8–25.8 years), and 62.5% had basilar artery anomalies or stenosis. All 8 patients had symptomatic narrowing of one or both petrous carotid segments with tortuous collateralization. Figure 1 shows lateral vertebral artery and common carotid artery injection angiograms obtained in 1 patient with basilar artery anomaly and characteristic petrous carotid narrowing.

Fig. 1.
Fig. 1.

Lateral vertebral artery injection (left) and common carotid artery injection (right) angiograms obtained in a patient with a basilar artery anomaly and characteristic narrowing of the petrous segment of the internal carotid artery.

Clinical Presentation

All 8 patients (100%) presented with symptoms consistent with chronic cerebral ischemia. There was a history of transient ischemic attack (TIA) in 4 (50%) of the 8 patients, and clinical evidence of completed strokes in 3 (37.5%). At surgery, all of the patients had recovered with no evident neurological deficits on examination. A history of seizures was present in 3 patients (37.5%). Four patients (50%) had chronic headaches at presentation. No patient presented with hemorrhage (Table 1).

TABLE 1.

Clinical presentation

SymptomNo. of Patients (%)
TIA4 (50)
Stroke3 (38)
Persistent neurologic deficit0 (0)
Seizure3 (38)
Headache4 (50)
Intracranial hemorrhage0 (0)

Radiographic Presentation and Features

The 8 patients had a total of 13 affected hemispheres. Preoperative MRI studies were available for all 8 patients and all 13 hemispheres. Preoperative digital subtraction angiography studies were also available for all 8 patients (100%) preoperatively, involving 13 affected hemispheres (100%). The mean Suzuki grade at presentation on the affected side was 3.4 (range 3–5). The angiographic characteristics of moyamoya syndrome in this patient population with PHACES were distinct from our series of over 400 moyamoya patients without PHACES. Of the 8 patients with both moyamoya syndrome and PHACES, 7 (87.5%) had evidence of previous infarction in hemispheres on preoperative MRI. Only 1 patient had no radiographic evidence of previous stroke. Bilateral disease was present in 5 patients (63%), and 3 patients (38%) had only 1 side affected at the time of surgery. In the unilateral group, 1 affected hemisphere was on the left and 2 were on the right. All 8 patients (100%) had symptomatic narrowing of 1 or both petrous carotids with tortuous collateralizations. Five patients (63%) had basilar artery anomalies or stenosis (Table 1).

Surgical Treatment

All but one of the patients in this series were treated surgically with pial synangiosis, a standardized method of indirect revascularization. The eighth patient was treated with myosynangiosis because she did not have a superficial temporal artery on the affected side, leading to a preoperative plan for performing myosynangiosis. Our current practice for bilateral disease is to perform the operation on both sides during a single anesthesia procedure (assuming that there are no anesthetic or surgical concerns during the first-side surgery), and 4 of the 5 bilateral cases were so treated. One bilateral case was staged due to subarachnoid hemorrhage at the time of the first synangiosis. The second-side procedure was performed 6 weeks later, and there were no postoperative complications after either procedure. The anesthesia and perioperative management of all patients with moyamoya is standardized at our institution.

The surgical technique for pial synangiosis involves dissection of the parietal branch of the superficial temporal artery under the microscope, followed by a generous craniotomy and stellate opening of the dura. Two key technical points that differentiate pial synangiosis from other indirect procedures include wide opening of the arachnoid under the microscope and suturing the donor vessel to the pia with 10–0 nylon suture. The dura is left open, and the craniotomy is closed, with resorbable sutures used for skin closure (Fig. 2).

Fig. 2.
Fig. 2.

Operative photographs demonstrating aspects of pial synangiosis. A: Initial wide, stellate dural opening. B: Arachnoidal opening throughout operative field. C: Synangiosis with 10–0 nylon. D: Conclusion of synangiosis, with dural leaflets reflected back into area of arachnoidal opening, without dural closure. Figure is available in color online only.

Surgical Results

A total of 13 hemispheres were treated during 9 operations. There were 3 unilateral and 5 bilateral cases. Four (80%) of the 5 bilateral cases were completed as 1 anesthesia procedure. The mean amount of blood loss was 42 ml per hemisphere (range 20–80 ml), and the mean length of the procedures was 149 minutes (range 110–190 minutes). The mean length of stay was 5.2 days (range 3–7 days), including a scheduled admission to the hospital on the night prior to surgery for preoperative hydration (Table 2).

TABLE 2.

Surgery parameters

ParameterValue
Total no. of operations13
 Unilateral3
 Bilateral5 (10 hemispheres)
Blood loss, ml
 Mean42
 Range20–80
Length of procedure (single hemisphere), mins
 Mean149
 Range110–190
Length of hospital stay, days
 Mean5.2
 Range3–7
Complications, no. of cases0
 Death0
 Stroke0
 TIA0
 Seizure0
 Infection0

Perioperative Complications

There were no complications.

Clinical Outcome After Hospital Discharge

The mean duration of follow-up after surgery was 56.4 months (range 8–160 months; Table 3). No new clinical symptoms were noted at 6 months in any of the 8 cases. Patients were evaluated for any new clinical symptoms or deterioration, comparing the findings at their preoperative examinations to those at follow-up using the mRS. Using this scale, 4 (50%) of 8 patients had improved neurological function and 4 (50%) were stable (Table 3). All patients were maintained on chronic aspirin therapy postoperatively.

TABLE 3.

Postoperative outcomes

VariableValue
Duration of follow-up, mos
 Mean56.4
 Range8–160
Clinical outcome, no. of patients (%)
 Stroke0/8 (0)
 TIA0/8 (0)
 Seizure0/8 (0)
 Headache0/8 (0)
mRS score, no. of patients (%)
  0 or 1, no or minimal neurological deficit4/8 (50)
  2 or 3, mild neurological deficit4/8 (50)
  4 or 5, dependent0/8 (0)
mRS score change, preop to postop
  Improved, no. of patients (%)4/8 (50)
  Stable, no. of patients (%)4/8 (50)
Radiographic outcome
 Radiographic follow-up in mos
  Mean52.6
  Range19–160
MRI available, no. of patients (%)8/8 (100)
Angiogram available, no. of patients (%)8/8 (100)
Radiographic evidence of new strokes, no. of patients (%)0/8 (0)
Evidence of new surgical collateral vessels, no. of affected hemispheres (%)13/13 (100)
Matsushima grade, no. of affected hemispheres (%)
  A5/13 (38.4)
  B8/13 (61.5)
  C0/13 (0)

Radiographic Outcome After Hospital Discharge

All patients had postoperative MRI and/or angiography studies available for review. The mean duration of radiographic follow-up was 52.6 months (range 19–160 months) with a mean of 4.8 studies per patient (range 2–7 studies). Magnetic resonance imaging was available and angiograms were performed in all 8 patients (100%).

All 8 patients had a 6-month postoperative follow-up MRI, which showed reduced cortical FLAIR signal, a marker of improved blood flow. None of the patients with unilateral disease went on to develop disease on the contralateral side and 2 of these patients are at least 2 years out from surgery. The mean duration of follow-up for these patients was 36.9 months (range 19–46.8 months).

There were no new strokes identified in any radiographic studies following hospital discharge and no radiographic evidence of moyamoya progression in any patients. New surgical collateral vessels were identified in the 13 hemispheres (100%) imaged with angiography. These collateral vessels were evaluated using the Matsushima scale; grade A collaterals were observed in 5 of 13 affected hemispheres (38.4%) and grade B collaterals in 8 of 13 affected hemispheres (61.5%). No progression of the basilar artery stenosis was seen in any patient.

Discussion

The term “moyamoya disease” is used to differentiate idiopathic cases from those seen in patients with associated syndromes or diseases, such as this series of cases involving patients with PHACES, which are classified as moyamoya syndrome.13,14 In addition to facial segmental superficial hemangiomas, PHACES is known to have other associated vascular malformations, including coarctation of the aorta, cardiovascular anomalies, and intracerebral arterial anomalies.2,10 Two prior studies describe intracerebral vascular anomalies in PHACES patients. In 2006, Drolet et al. described 5 PHACES patients who had strokes in infancy and their associated intracerebral arteriopathy.1,11 None of these patients underwent surgical treatment. Heyer et al. reported on a single PHACES patient who underwent bilateral pial synangiosis after development of moyamoya syndrome and multiple strokes.3,4 Postoperatively, she had no further radiographic strokes or clinical progression with 2 years of follow-up. These data are in concordance with our practice, as early intervention helps to prevent stroke and results in improved outcomes. For this reason, we recommend early surgical treatment for our patients.7,15,16 More recently, Satishkumar et al.12 and Jack et al.5 described individual patients with PHACES and moyamoya vasculopathy, and Tortora et al.18 compiled a case series, in which the presence of basilar artery stenosis in this cohort was noted, as we describe here. In addition, the Tortora series includes 3 patients who underwent surgery, with one of these 3 patients having reported follow-up. However, these prior publications represent scattered approaches to therapy among multiple practitioners, while the present study represents a systematic review of this subgroup within the context of our much larger cohort of moyamoya patients, with a unified treatment approach and careful follow-up.

Our patients were diagnosed at an average age of 9.3 years. The most common presenting symptom was transient ischemic attack (TIA) or stroke. Patients with both PHACES and moyamoya syndrome differ from other moyamoya patients in that they often have other vascular anomalies or significant intracranial vascular tortuosity in addition to their moyamoya disease. Of particular note, our study demonstrated that PHACES patients frequently have associated basilar artery stenosis, which did not progress on follow-up imaging in this series. Also of interest, the internal carotid artery narrowing occurred proximally within the petrous segment of the artery—as opposed to the more typical distal narrowing seen in non-PHACES moyamoya patients.

All but one of the patients in this series underwent pial synangiosis, with the exception being a patient who did not have a viable superficial temporal artery and therefore underwent a myosynangiosis.8,9 The overlying or adjacent segmental superficial hemangiomas can complicate surgery both by affecting the superficial soft tissue, but also the associated superficial temporal arteries can be more friable or nonviable for synangiosis.

In our series, the clinical presentation of patients with PHACES who developed moyamoya syndrome was similar to that of other described moyamoya syndrome patients. However, patients with both PHACES and moyamoya syndrome frequently have other intracerebral anomalies, including basilar artery stenosis or anomalies. These other intracerebral anomalies did not progress in our follow-up period.

Although approximately 30% of patients with unilateral moyamoya disease demonstrate progression of disease on the previously unaffected side within 2 years of diagnosis, there was no such progression in the 3 patients in this series who presented with unilateral disease; we hypothesize that this difference may be related to the segmental developmental anomalies unique to PHACES.6,17 Moreover, no progression of the other intracerebral vascular tortuosity or anomalies was seen in any of the patients with long-term follow-up. There was both clinical and radiographic response with stabilization or improvement in symptoms in all patients and development of collateral vessel formation. While we found good clinical and radiographic response to revascularization in our patients, these cases do present surgical challenges given the associated segmental superficial facial hemangiomas.

Conclusions

This is the first series to describe the intracerebral vascular anomalies in PHACES and the response of PHACES-associated moyamoya syndrome to surgical treatment. This series was notable for the preponderance of the female sex, the association of basilar artery stenosis, and the unique proximal stenosis of the internal carotid artery. The surgical treatment of these patients can be challenging given the proximity of the facial hemangiomas to the surgical field as well as the fragility of the superficial temporal artery. Our patients had both a radiographic and clinical response to revascularization. Patients with unilateral disease did not have evidence of progression in other cerebral circulation in our follow-up period.

Acknowledgments

We would like to acknowledge the Kids at Heart Fund and Marcus Chae 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: Smith, Scott. Acquisition of data: Jernigan, Storey, Hammer. Analysis and interpretation of data: Jernigan, Storey, Hammer. Drafting the article: Jernigan, Hammer. Critically revising the article: Smith, Orbach, Scott. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Smith. Administrative/technical/material support: Riordan. Study supervision: Smith.

References

  • 1

    Drolet BA, Dohil M, Golomb MR, Wells R, Murowski L, Tamburro J, et al.: Early stroke and cerebral vasculopathy in children with facial hemangiomas and PHACE association. Pediatrics 117:959964, 2006

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Hess CP, Fullerton HJ, Metry DW, Drolet BA, Siegel DH, Auguste KI, et al.: Cervical and intracranial arterial anomalies in 70 patients with PHACE syndrome. AJNR Am J Neuroradiol 31:19801986, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Heyer GL: PHACE(S) syndrome. Handb Clin Neurol 132:169183, 2015

  • 4

    Heyer GL, Millar WS, Ghatan S, Garzon MC: The neurologic aspects of PHACE: case report and review of the literature. Pediatr Neurol 35:419424, 2006

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

    Jack AS, Chow MM, Fiorillo L, Chibuk T, Yager JY, Mehta V: Bilateral pial synangiosis in a child with PHACE syndrome. J Neurosurg Pediatr 17:7075, 2016

  • 6

    Kelly ME, Bell-Stephens TE, Marks MP, Do HM, Steinberg GK: Progression of unilateral moyamoya disease: a clinical series. Cerebrovasc Dis 22:109115, 2006

  • 7

    Koss M, Scott RM, Irons MB, Smith ER, Ullrich NJ: Moyamoya syndrome associated with neurofibromatosis Type 1: perioperative and long-term outcome after surgical revascularization. J Neurosurg Pediatr 11:417425, 2013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Matsushima T, Inoue T, Katsuta T, Natori Y, Suzuki S, Ikezaki K, et al.: An indirect revascularization method in the surgical treatment of moyamoya disease—various kinds of indirect procedures and a multiple combined indirect procedure. Neurol Med Chir (Tokyo) 38 Suppl:297302, 1998

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Matsushima Y: [Indirect anastomoses for moyamoya disease.] No Shinkei Geka 26:769786, 1998 (Jpn)

  • 10

    Metry D, Heyer G, Hess C, Garzon M, Haggstrom A, Frommelt P, et al.: Consensus Statement on Diagnostic Criteria for PHACE Syndrome. Pediatrics 124:14471456, 2009

  • 11

    Metry DW, Haggstrom AN, Drolet BA, Baselga E, Chamlin S, Garzon M, et al.: A prospective study of PHACE syndrome in infantile hemangiomas: demographic features, clinical findings, and complications. Am J Med Genet A 140:975986, 2006

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

    Sathishkumar D, George R, Irodi A, Thomas M: PHACES syndrome with moyamoya vasculopathy—a case report. Dermatol Online J 19:19271, 2013

  • 13

    Scott RM, Smith ER: Introduction: moyamoya disease. Neurosurg Focus 26(4):E1, 2009

  • 14

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

  • 15

    Scott RM, Smith JL, Robertson RL, Madsen JR, Soriano SG, Rockoff MA: Long-term outcome in children with moyamoya syndrome after cranial revascularization by pial synangiosis. J Neurosurg 100 (2 Suppl Pediatrics ):142149, 2004

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Smith ER, McClain CD, Heeney M, Scott RM: Pial synangiosis in patients with moyamoya syndrome and sickle cell anemia: perioperative management and surgical outcome. Neurosurg Focus 26(4):E10, 2009

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

    Smith ER, Scott RM: Progression of disease in unilateral moyamoya syndrome. Neurosurg Focus 24(2):E17, 2008

  • 18

    Tortora D, Severino M, Accogli A, Martinetti C, Vercellino N, Capra V, et al.: Moyamoya vasculopathy in PHACE syndrome: six new cases and review of the literature. World Neurosurg 108:291302, 2017

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

Image from Roland and Smyth (pp 411–421).

  • Lateral vertebral artery injection (left) and common carotid artery injection (right) angiograms obtained in a patient with a basilar artery anomaly and characteristic narrowing of the petrous segment of the internal carotid artery.

  • Operative photographs demonstrating aspects of pial synangiosis. A: Initial wide, stellate dural opening. B: Arachnoidal opening throughout operative field. C: Synangiosis with 10–0 nylon. D: Conclusion of synangiosis, with dural leaflets reflected back into area of arachnoidal opening, without dural closure. Figure is available in color online only.

  • 1

    Drolet BA, Dohil M, Golomb MR, Wells R, Murowski L, Tamburro J, et al.: Early stroke and cerebral vasculopathy in children with facial hemangiomas and PHACE association. Pediatrics 117:959964, 2006

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Hess CP, Fullerton HJ, Metry DW, Drolet BA, Siegel DH, Auguste KI, et al.: Cervical and intracranial arterial anomalies in 70 patients with PHACE syndrome. AJNR Am J Neuroradiol 31:19801986, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Heyer GL: PHACE(S) syndrome. Handb Clin Neurol 132:169183, 2015

  • 4

    Heyer GL, Millar WS, Ghatan S, Garzon MC: The neurologic aspects of PHACE: case report and review of the literature. Pediatr Neurol 35:419424, 2006

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

    Jack AS, Chow MM, Fiorillo L, Chibuk T, Yager JY, Mehta V: Bilateral pial synangiosis in a child with PHACE syndrome. J Neurosurg Pediatr 17:7075, 2016

  • 6

    Kelly ME, Bell-Stephens TE, Marks MP, Do HM, Steinberg GK: Progression of unilateral moyamoya disease: a clinical series. Cerebrovasc Dis 22:109115, 2006

  • 7

    Koss M, Scott RM, Irons MB, Smith ER, Ullrich NJ: Moyamoya syndrome associated with neurofibromatosis Type 1: perioperative and long-term outcome after surgical revascularization. J Neurosurg Pediatr 11:417425, 2013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Matsushima T, Inoue T, Katsuta T, Natori Y, Suzuki S, Ikezaki K, et al.: An indirect revascularization method in the surgical treatment of moyamoya disease—various kinds of indirect procedures and a multiple combined indirect procedure. Neurol Med Chir (Tokyo) 38 Suppl:297302, 1998

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Matsushima Y: [Indirect anastomoses for moyamoya disease.] No Shinkei Geka 26:769786, 1998 (Jpn)

  • 10

    Metry D, Heyer G, Hess C, Garzon M, Haggstrom A, Frommelt P, et al.: Consensus Statement on Diagnostic Criteria for PHACE Syndrome. Pediatrics 124:14471456, 2009

  • 11

    Metry DW, Haggstrom AN, Drolet BA, Baselga E, Chamlin S, Garzon M, et al.: A prospective study of PHACE syndrome in infantile hemangiomas: demographic features, clinical findings, and complications. Am J Med Genet A 140:975986, 2006

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

    Sathishkumar D, George R, Irodi A, Thomas M: PHACES syndrome with moyamoya vasculopathy—a case report. Dermatol Online J 19:19271, 2013

  • 13

    Scott RM, Smith ER: Introduction: moyamoya disease. Neurosurg Focus 26(4):E1, 2009

  • 14

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

  • 15

    Scott RM, Smith JL, Robertson RL, Madsen JR, Soriano SG, Rockoff MA: Long-term outcome in children with moyamoya syndrome after cranial revascularization by pial synangiosis. J Neurosurg 100 (2 Suppl Pediatrics ):142149, 2004

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Smith ER, McClain CD, Heeney M, Scott RM: Pial synangiosis in patients with moyamoya syndrome and sickle cell anemia: perioperative management and surgical outcome. Neurosurg Focus 26(4):E10, 2009

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

    Smith ER, Scott RM: Progression of disease in unilateral moyamoya syndrome. Neurosurg Focus 24(2):E17, 2008

  • 18

    Tortora D, Severino M, Accogli A, Martinetti C, Vercellino N, Capra V, et al.: Moyamoya vasculopathy in PHACE syndrome: six new cases and review of the literature. World Neurosurg 108:291302, 2017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

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