Correlation between reduction in microvascular transit time after superficial temporal artery–middle cerebral artery bypass surgery for moyamoya disease and the development of postoperative hyperperfusion syndrome

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Hyperperfusion syndrome (HPS) is a notable complication that causes various neurological symptoms after superficial temporal artery (STA)–middle cerebral artery (MCA) bypass surgery for moyamoya disease (MMD). The authors used intraoperative indocyanine green (ICG) videoangiography to measure the change in microvascular transit time (MVTT) after bypass surgery. An analysis was then conducted to identify the correlation between change in MVTT and presence of postoperative HPS.


This study included 105 hemispheres of 81 patients with MMD who underwent STA-MCA single bypass surgery between January 2010 and January 2015. Intraoperative ICG videoangiography was performed before and after bypass surgery. The MVTT was calculated from the ICG time intensity curve recorded in the pial arterioles and venules. Multivariate logistic regression analysis was conducted to test the effect of multiple variables, including the change in MVTT after bypass surgery, on postoperative HPS.


Postoperative HPS developed in 28 (26.7%) of the 105 hemispheres operated on. MVTT was reduced significantly after bypass surgery (prebypass 5.34 ± 2.00 sec vs postbypass 4.12 ± 1.60 sec; p < 0.001). The difference between prebypass and postbypass MVTT values, defined as ΔMVTT, was significantly greater in the HPS group than in the non-HPS group (2.55 ± 2.66 sec vs 0.75 ± 1.78 sec; p < 0.001). Receiver operating characteristic curve analysis revealed that the optimal cutoff point of ΔMVTT was 2.6 seconds (sensitivity 46.4% and specificity 85.7% as a predictor of postoperative HPS). A ΔMVTT > 2.6 seconds was an independent predictor of HPS in multivariate analysis (hazard ratio 4.88, 95% CI 1.76–13.57; p = 0.002).


MVTT in patients with MMD was reduced significantly after bypass surgery. Patients with a ΔMVTT > 2.6 seconds tended to develop postoperative HPS. Because ΔMVTT can be easily measured during surgery, it is a useful diagnostic tool for identifying patients at high risk for HPS after STA-MCA bypass surgery for MMD.

ABBREVIATIONS CBF = cerebral blood flow; CBV = cerebral blood volume; DWI = diffusion-weighted imaging; HPS = hyperperfusion syndrome; ICG-VA = indocyanine green videoangiography; ICH = intracerebral hemorrhage; MCA = middle cerebral artery; MMD = moyamoya disease; MRA = MR angiography; MVTT = microvascular transit time; PaCO2 = partial pressure of carbon dioxide in arterial blood; PaO2 = partial pressure of oxygen in arterial blood; ROC = receiver operating characteristic; ROI = region of interest; STA = superficial temporal artery; ΔMVTT = difference between prebypass and postbypass MVTT values.

Article Information

Correspondence Hiroharu Kataoka, Department of Neurosurgery, National Cerebral and Cardiovascular Center, 5-7-1 Fujishiro-dai, Suita, Osaka 565-8565, Japan. email:

Drs. Yang and Higashino contributed equally to this work.

INCLUDE WHEN CITING Published online May 12, 2017; DOI: 10.3171/2016.11.JNS162403.

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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    Method for measuring MVTT. A: Schematic drawing of the ICG time intensity curve. MVTT was calculated as venous T1/2 peak − arterial T1/2 peak. B: ROIs were identified on the recipient M4 segment, just distal to the anastomosis point (asterisk), and on the superficial middle cerebral vein (cross). An analysis of the ICG time intensity curve was performed on the same ROIs before and after bypass surgery. C: An example of the ICG time intensity curve. Because the peak intensity lasts for several seconds, the “time to peak” is difficult to define. Therefore, the “time to half-value of peak” (T1/2 peak) was used instead of “time to peak.” MVTT was calculated as venous T1/2 peak − arterial T1/2 peak.

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    Change in MVTT after bypass surgery. MVTT was reduced significantly after bypass surgery, in both the HPS and non-HPS groups.

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    Comparison between ΔMVTT of HPS and non-HPS groups. The ΔMVTT of the HPS group was significantly greater than that of the non-HPS group.

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    ROC curve analysis for development of HPS. The ROC curve revealed that the Youden index (sensitivity + specificity–1) reached the maximum (dotted vertical line) when the cutoff point for ΔMVTT was set at 2.6 seconds. At this value, the sensitivity and specificity for predicting HPS were 46.4% and 85.7%, respectively. Figure is available in color online only.

  • View in gallery

    Representative case. A and D: Color maps of FLOW 800 before (A) and after (D) bypass surgery. The asterisk and the cross indicate ROIs in the artery and in the vein, respectively. The arrow indicates the STA. B and E: Time intensity curves before (B) and after (E) bypass surgery. Prebypass and postbypass MVTTs were 7.7 seconds and 4.0 seconds, respectively. C and F: Preoperative (C) and postoperative (F) 123I-IMP SPECT. The CBF in the left cerebral hemisphere was reduced compared with that in the contralateral side before surgery (C). CBF around the site of the anastomosis (arrows) increased significantly on the 2nd day after surgery (F). The patient presented with motor aphasia on the same day as the SPECT procedure.


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