Greater ultrasonographic changes in pediatric moyamoya patients compared with adults after indirect revascularization surgeries

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Pediatric and adult patients with moyamoya disease experience similar clinical benefits from indirect revascularization surgeries, but there are still debates about age-related angiographic differences of the collaterals established after surgery. The goal of this study was to assess age-related differences on ultrasonography before and after indirect revascularization surgeries in moyamoya patients, focusing on some ultrasonographic parameters known to be correlated with the collaterals supplied by the external carotid artery (ECA).


The authors prospectively included moyamoya patients (50 and 26 hemispheres in pediatric and adult patients, respectively) who would undergo indirect revascularization surgery. Before surgery and at 1, 3, and 6 months after surgery, the patients underwent ultrasonographic examinations. The ultrasonographic parameters included peak-systolic velocity (PSV), end-diastolic velocity (EDV), resistance index (RI), and flow volume (FV) measured in the ECA, superficial temporal artery (STA), and internal carotid artery on the operated side. The mean values, absolute changes, and percentage changes of these parameters were compared between the pediatric and adult patients. Logistic regression analysis was used to clarify the determinants affecting postoperative EDV changes in the STA.


Before surgery, the adult patients had mean higher EDV and lower RI in the STA and ECA than the pediatric group (all p < 0.05). After surgery, the pediatric patients had greater changes (absolute and percentage changes) in the PSV, EDV, RI, and FV in the STA and ECA (all p < 0.05). The factors affecting postoperative EDV changes in the STA at 6 months were age (p = 0.006) and size of the revascularization area (i.e., revascularization in more than the temporal region vs within the temporal region; p = 0.009). Pediatric patients who received revascularization procedures in more than the temporal region had higher velocities (PSV and EDV) in the STA than those who received revascularization within the temporal region (p < 0.05 at 1–6 months), but such differences were not observed in the adult group.


The greater changes of these parameters in the STA and ECA in pediatric patients than in adults after indirect revascularization surgeries indicated that pediatric patients might have a greater increase of collaterals postoperatively than adults. Pediatric patients who undergo revascularization in more than the temporal region might have more collaterals than those who undergo revascularization within the temporal region.

ABBREVIATIONS ECA = external carotid artery; EDAS = encephaloduroarteriosynangiosis; EDS = encephalodurosynangiosis; EDV = end-diastolic velocity; EMS = encephalomyosynangiosis; EPS = encephalopericraniosynangiosis; FV = flow volume; ICA = internal carotid artery; MMD = moyamoya disease; PSV = peak-systolic velocity; RI = resistance index; STA = superficial temporal artery.

Article Information

Correspondence Meng-Fai Kuo: National Taiwan University Hospital, Taipei, Taiwan.

INCLUDE WHEN CITING Published online August 31, 2018; DOI: 10.3171/2018.6.PEDS18151.

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

© AANS, except where prohibited by US copyright law.



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    Study protocol. After confirmation of MMD by cerebral angiography, patients underwent ultrasonographic examinations and MR perfusion (MRP) imaging. Indirect revascularization procedures were designed according to the hypoperfusion area on MR perfusion images. Ultrasonographic examinations, MR perfusion imaging, and angiographic studies were performed postoperatively. *All of the indirect revascularization procedures were combined with EDS.

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    Ultrasonographic flow patterns of the STAs in 2 representative cases before and after indirect revascularization surgeries. Upper: In a pediatric case, the STA showed a high-resistance flow pattern preoperatively. The STA changed to a low-resistance pattern starting as early as 1 month after surgery. At 1 month postoperatively, an increase in PSV (41.6 cm/sec to 89 cm/sec, 114% increase) and EDV (6.66 cm/sec to 32 cm/sec, 380% increase) and a decrease in RI (0.84 to 0.64, 24% decrease) were observed. Lower: In an adult case, the STA persistently showed a low-resistance flow pattern before and after surgery. At 3 months postoperatively, both velocity parameters increased (PSV, 81% increase; EDV, 290% increase), RI decreased 35%, and FV increased 247.8% compared with the baseline. All of the indirect revascularization procedures were combined with EDS. M = month; TAMV = time-averaged mean velocity; TAPV = time-averaged peak velocity. Figure is available in color online only.

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    Comparison of the mean serial ultrasonographic hemodynamic values between the pediatric and adult groups. Before surgery, the adult group had significantly higher EDVs in the STA and ECA (p < 0.0001 and p = 0.0002, respectively) and lower RI (both p < 0.0001) than the pediatric group. After surgery, the pediatric group had a higher PSV (at 3 months, p = 0.036) and a larger FV (at 3 months, p = 0.046) in the STA than the adult group. The EDV and RI in the STA between the 2 groups were similar. In the ICA, pediatric patients had significantly higher PSV, RI, and FV than adults preoperatively and postoperatively (all p < 0.05).

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    Comparison of mean absolute changes in serial ultrasonographic parameters between the pediatric and adult groups. Pediatric patients showed greater increases of PSV and EDV in the STA than adult patients at 3 months (ΔPSV at 3 months, p = 0.006; ΔEDV at 3 months, p = 0.012), a greater PSV increase in the ECA at 3 months (p = 0.025), and a greater RI decrease (p = 0.012) and a greater FV increase (p = 0.001) in the STA at 3 months.

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    Comparison of the mean percentage changes of serial ultrasonographic parameters between pediatric and adult groups. Pediatric patients had significantly larger percentage changes in the PSV, EDV, RI, and FV of the STA at 3 and 6 months postoperatively (all p < 0.05). The ECA had a similar trend to that of the STA.

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    Comparison of the mean flow velocities of the STA between different surgical procedures (based on the size of the revascularization region: more than the temporal region vs within the temporal region) in the pediatric and adult groups. In pediatric patients, the flow velocities and the changing velocities in those receiving revascularization in more than the temporal region were significantly higher than those within the temporal region at 1–6 months (all p < 0.05). In adult patients, there was no significant procedure-related difference in the flow velocities.



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