Patients
Twenty-two pediatric patients with moyamoya disease, nine boys and 13 girls, aged 7.6 ± 2.9 years (range, 4–15 years), underwent surgery at Yamaguchi University Hospital between 2007 and 2020. Patients with quasi-moyamoya disease or unilateral moyamoya disease were excluded. The patients were treated according to our protocol and guidelines for the diagnosis and treatment of moyamoya disease issued by the Research Committee of the Ministry of Health, Labor and Welfare, Japan [17]. Data, clinical findings, and neuroradiological findings of the patients were retrospectively analyzed.
Surgeries
Surgery was performed on patients with ischemic symptoms. Superficial temporal artery to middle cerebral artery (STA-MCA) anastomosis combined with encephalo-duro synangiosis (EDS) and encephalo-galeo synangiosis (EGS) was performed. When the MCA branches of the recipient were too small for anastomosis, encephalo-duro synangiosis (EDAS) combined with EDS and EGS was performed. The first operative side was determined based on the frequency of transient ischemic attack (TIA). If it occurred evenly bilaterally, the decision of the surgical side was made in the order of a smaller CRC side, more progression side of MCA stenosis, and then language-dominant hemisphere. The second-side surgery was performed when TIA appeared. The interval between the two surgeries was 6 months at the shortest and 3 years at the longest. Patients who had been asymptomatic for 3 years since the first surgery did not undergo second-side surgery.
Examinations
Before first-side surgery, all patients were examined, the Wechsler Intelligence Scale for children (WISC) III or IV was used for patients aged > 5 years, and the Tanaka−Binet Intelligence scale IV or V was used for patients aged < 5 years. The neurological outcome at the final follow-up, 1.5−13 years after the final surgery, was assessed using the Pediatric Cerebral Performance Category Scale (PCPCS) [18] for school-age patients. We modified the PCPCS for patients aged > 18 years (Table 1). Grades 1 and 2 were regarded as favorable outcomes, and grades 3 to 6 were unfavorable outcomes. MRI and angiography were performed as necessary.
Table 1
Outcome measures by Pediatric Cerebral Performance Category Scale (PCPCS) for patients aged < 18 years and modified PCPCS for patients aged > 18 years.
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PCPCS, < 18 y.o.
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Modified PCPCS, > 18 y.o.
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1
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regular school classroom
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university student, white collar worker
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2
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regular school classroom but grades perhaps not appropriate for age
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working school, blue collar worker, part-time worker
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3
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special education classroom
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unable to work, vocational training school
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4
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dependent on others for daily support
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dependent on others for daily support
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5
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any degree of coma without brain death
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any degree of coma without brain death
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6
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brain death
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brain death
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CBF measurement and patient groups
CBF was measured using 123I-iodoamphetamine single-photon emission computed tomography (IMP-SPECT). The range of interest (ROI) was set in the bilateral MCA territories. Using the dual table autoradiography method [19], resting CBF and acetazolamide challenge CBF were measured on the same day. CRC was calculated as the percentage increase in CBF from resting CBF to acetazolamide-challenged CBF. Although the normal range of CRC was defined as ≥ 30%, we considered 20% to be a sufficient level in the study. Patients aged < 13 years were sedated during the measurement using of CBF by intravenous administration of thiopental.
Resting CBF and CRC were measured three times: before the first-side surgery (preoperative CBF), before the second-side surgery (midterm CBF), and one year after the second-side surgery (final CBF) (Fig. 1). Patients who underwent surgery only on one side were examined twice for CBF measurement, and the second measurement was performed 3 years after surgery.
The patients were classified into four groups according to the results of the first-side surgery.
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Excellent group: bilateral CRC increased > 7% and TIA in neither hemisphere.
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Good group: bilateral CRC increased > 7%, and TIA remained in the unoperated hemisphere.
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Fair group: CRC increased > 7% only in the operated hemisphere.
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Poor group: CRC increased ≤ 7% in either hemisphere.
The number of patients included in the excellent, good, fair, and poor groups was six, six, four, and six, respectively.
Statistics
Differences between groups in the patient’s age, IQ, and CBF were analyzed with analysis of variance, and sex, paralysis, infarction, stenosis of the cerebral artery, surgical method, and outcomes were analyzed using the chi-square test. A p-value of less than 0.05 was considered statistically significant.
This retrospective study was approved by the Yamaguchi University Hospital Institutional Review Boards (H2020-095 and H2021-044).