Decrease in Leptomeningeal Ivy Sign on Fluid-Attenuated Inversion Recovery Images after Cerebral Revascularization in Patients with Moyamoya Disease

Imaging Examinations

Imaging examinations, including MR imaging and MRA, were performed in each patient pre- and postoperatively. Ten of 22 patients underwent quantitative SPECT with ACZ challenge pre- and postoperatively. Then, the correlation between a decrease in the ivy sign in the surgically treated hemisphere after cerebral revascularization and postoperative hemodynamic status was examined in 10 patients.

MR Imaging and MRA

The routine MR imaging protocol for cerebral ischemic diseases includes FLAIR imaging. MR imaging was performed by using a 3T MR imaging unit (MAGNETOM Trio, A Tim System; Siemens, Erlangen, Germany) without variability. FLAIR imaging was performed by using a fast FLAIR sequence with a TR of 9000 ms, a TE_eff of 86 ms, a TI of 2500 ms, a 241-Hz/pixel bandwidth, and a flip angle of 150°. Image thickness, gap, and matrix for all sequences were 6.0 mm, 1.2 mm, and 384 × 372 pixels, respectively. 3D time-of-flight MRA was performed with a TR of 22 ms, a TE of 3.1 ms, a 250-Hz/pixel bandwidth, and a flip angle of 18°. Voxel size was 0.52 × 0.52 × 0.8 mm, and the acquisition matrix was 384 × 320 pixels.

An ivy sign on a FLAIR image was defined as a continuous linear or punctate leptomeningeal high signal intensity along the cortical sulci and subarachnoid space. Two neuroradiologists retrospectively reviewed MR images for ivy signs on FLAIR. A hemisphere was defined as ivy-positive when an ivy sign was observed in the MCA region (in any of the frontal, temporal, and parietal lobes). The degree of the ivy sign (ivy sign score) in the MCA region was classified into 3 grades (0–2): Grade zero indicated an absence of the ivy sign, grade 1 indicated that the ivy sign was seen on less than half of the cortical surface in the region, and grade 2 indicated that the ivy sign was seen on more than half of the cortical surface. The ivy sign was scored subjectively by reviewing all the FLAIR images traversing all the cerebral hemispheres. The average score for each region was defined as the ivy sign score for the individual hemisphere. The score of the ivy sign was compared pre- and postoperatively among patients with Moyamoya disease. Postoperative MR imaging was performed during the first 3 months after surgery and every 6 month after that.

Quantitative Estimation of CBF and VR

A SPECT Multispect 3 scanner (Siemens) and an ICON image processor (Siemens Medical Systems) were used, with a low-energy ultra-high-resolution fan-beam collimator (225 cpm/μCi). The conditions for acquisition were as follows: 20-minute acquisition (40 seconds/90 steps, 3° step; the step and shoot method), a matrix of 128 × 128 pixels (2.89 mm/pixel), and a rotation radius of 13.9 cm. A filtered back-projection method by using a Butterworth filter was used to reconstruct images from 20-minute data. A low-pass filter (cutoff, 0.3 cycles/cm; order, 5.0) was used as the 3D postfilter. Two SPECT images were summated to obtain a section thickness of 5.78 mm.

Ten patients underwent 2 SPECT sessions: a basal study and an ACZ-challenged study. Both rCBF and VR were quantified by autoradiographic processing of a single SPECT scan with a 1-point arterial blood sample (the IMP-ARG method).⁵ Patients were allowed to rest in a quiet dimly lit room and were injected with IV ¹²³I-IMP, 166.5 MBq. Ten minutes after starting ¹²³I-IMP infusion, an arterial blood sample was collected to calibrate the previously determined standard input function, and its whole-blood radioactivity concentration was counted by using a well counter that had been cross-calibrated with the SPECT scanner. After arterial blood sampling, a single SPECT scan was obtained at a midscan time of 10 minutes. Basal images were obtained 35 minutes after injecting the radiotracer. In 2-compartment ¹²³I-IMP analysis, the distribution volume (ie, the ratio of influx constant and efflux constant) was set to a constant value (41.2 mL/mL). rCBF maps were calculated pixel by pixel from single SPECT data, and the standard input function was calibrated with a 1-point arterial blood sample.⁵

Several days later (3–5 days), the patients were consecutively placed in an environment similar to that of the first session and were injected with 1-g IV ACZ (Diamox) during a 1-minute period. Fifteen minutes later, the patients were injected with ¹²³I-IMP and ACZ-challenged images were obtained in a manner similar to that followed in the basal study. An automated region-of-interest-setting method by using NEUROSTAT (http://128.95.65.28/∼Download) was performed without losing individual morphologic information in the SPECT images.^6,7 To objectively classify the severity of hemodynamic ischemia according to the JET study protocol of patients with intracranial occlusive disease,⁸ we performed a quantitative analysis by using 3D stereotactic surface projections analytical software (3D-SSP; Nihon Medi-physics, Tokyo, Japan) and stereotactic extraction estimation display software (SEE-JET; Nihon Medi-physics).⁹ This method provides 3D displays of VR, the severity of hemodynamic brain ischemia, and CBF at rest and after Diamox challenge.

The measurements obtained with SPECT are not actually quantitative because true quantitative assessment of CBF requires the application of the Fick principle, as originally applied with the use of nitrous oxide by Kety and Schmidt¹⁰ and currently applied with PET and the use of ¹⁵O-labeled CO₂ and water. rVR was defined as the ratio of the difference between Diamox-activated rCBF and resting rCBF to resting rCBF (Diamox-activated rCBF / resting rCBF − 1[×100]%). Resting rCBF and rVR of the MCA territory were evaluated in the hemispheres in all patients. The severity of hemodynamic brain ischemia was classified into 3 stages: stage 0 (resting CBF > 15 mL/100 g/min and VR > 30%), stage I (34 mL/100 g/min [80% of normal CBF] > resting CBF > 15 mL/100 g/min and 30% > VR > 10%), and stage II (34 mL/100 g/min > resting CBF > 15 mL/100 g/min and 10% > VR > −30%).^8,9 The stage II area was identical to the misery perfusion area. Finally, the proportion of stage II area to hemisphere and mean rVRs in MCA territories were compared pre- and postoperatively between surgically treated and contralateral (nonsurgically treated) hemispheres.

Statistical Analysis

Statistical analysis was performed by using the paired t test to analyze the variance between the decreased ivy sign and contralateral hemispheres. A Student t test was performed to analyze the difference between direct and indirect bypass procedures. The difference was considered significant at P < .05.