Intracranial Arteriovenous Shunting: Detection with Arterial Spin-Labeling and Susceptibility-Weighted Imaging Combined

Patients and Brain Imaging

This study was approved by the Rothschild Foundation Hospital institutional review board, and written informed consent was obtained from all subjects. From September 1, 2011, to August 31, 2015, 104 consecutive patients (45 females and 59 males; mean age, 48.3 years; range, 11–81 years) underwent DSA for a known (n = 26) or suspected (n = 78) AVS. Known AVS included brain AVM previously treated by embolization and/or radiosurgery. In this patient group, DSA was performed to evaluate nidus reduction or detect a potential residual shunting. DAVF or brain AVM was suspected in patients with brain hematoma (according to clinical status, patient age, medical history, and location of hemorrhage), pulsatile tinnitus, and suggestive findings on brain MR imaging/CT. In these patients, DSA was performed to confirm AVS and to analyze its location and angioarchitecture.

DSA was performed on a flat panel biplane system (Allura; Philips Healthcare, Best, the Netherlands) and included a selective injection in both the internal and external carotid arteries and vertebral arteries with at least 2 intracranial views (frontal and sagittal). When necessary, 3D rotational angiography with MIP reconstructions and additional oblique views was performed. Each angiogram was acquired at 2 frames per second with a 1024 × 1024 matrix size and a 20-cm or 27-cm FOV.

In all 104 consecutive patients, we systematically performed 3T MR imaging (Discovery MR750; GE Healthcare, Milwaukee, Wisconsin) once per patient as required by the institutional review board and within the 3 weeks following DSA. Patients were excluded from the study on the basis of at least 1 of the following conditions: 1) The time interval between MR imaging and DSA was >4 weeks; 2) an endovascular or a radiosurgical procedure was performed in the interval between MR imaging and DSA; and 3) image artifacts prevented accurate analysis of the MR images. Among the 104 consecutive patients, 12 were excluded from the study because of major artifacts on MR imaging. Finally, the study group consisted of 92 patients (40 females and 52 males; mean age, 47.4 years; range, 11–81 years) with a mean time interval between MR imaging and DSA of 13 days (range, 2–21 days). A flow chart illustrating the patient characteristics is shown in Fig 1.

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Fig 1.

Flow chart illustrating patient selection.

The conventional MR imaging protocol included 2D diffusion-weighted imaging, 2D gradient-echo T2*, 3D FLAIR, 3D TOF MRA, 4D contrast-enhanced MRA (TR, 2.6 ms; TE, 1.1 ms; temporal resolution, 1 second; voxel size, 1 × 1 × 1 mm) directly followed by a 3D high-resolution contrast-enhanced MRA (TR, 3.6 ms; TE, 1.5 ms; voxel size, 0.6 × 0.6 × 0.6 mm), and postcontrast 3D gradient-echo T1WI sequences (voxel size, 1 × 1 × 1 mm). In addition, SWI (TR, 40 ms; TE, 25 ms; voxel size, 1 × 1 × 2 mm) and ASL (3D FSE; pseudocontinuous; postlabel delay, 1525 ms; section thickness, 4 mm) were performed in each subject before gadolinium administration.

4D contrast-enhanced MRA covered a half-brain that was chosen according to DSA results to optimize temporal and spatial resolution. Intravenous gadobutrol (Gadovist; Bayer Schering Pharma, Berlin, Germany) was administered at a concentration of 0.1 mmol/kg during the acquisition of 4D contrast-enhanced MRA.

Image Analysis

DSA examinations were interpreted by 2 interventional neuroradiologists (X.L., J.-P.P.) together, with >20 years of experience. They reviewed the DSA images of all 92 patients to determine the presence or absence of AVS. In case of AVS, they assigned the vascular malformation as DAVF or AVM. A lesion was considered consistent with a DAVF if meningeal arterial feeders and a fistulous point on the dura mater were identified. A lesion was considered consistent with AVM if arterial feeders and a complex AVS (nidus) located in the brain were identified. Developmental venous anomaly was also located by using DSA, if present.

MR images were first anonymized and randomly mixed. Two experienced neuroradiologists with 14 (R.B.) and 10 (J.H.) years of experience, blinded to the results of DSA and clinical data, independently reviewed all the MR imaging datasets for the presence of AVS. Four independent readings took place 2 weeks apart to avoid recall bias with the following sequences available: 1) ASL alone, 2) SWI alone, 3) ASL/SWI, and 4) the “conventional MR imaging protocol,” including diffusion-weighted imaging, T2*, 3D FLAIR, TOF MRA, 4D and 3D contrast-enhanced MRA, and postcontrast 3D T1WI MR imaging. Criteria for the presence of AVS on MR images were defined as follows:

With ASL, the presence of an intracranial venous hypersignal within the dural sinuses or cortical veins.

With SWI, a hyperintense venous structure and/or direct visualization of the nidus/fistulous point.

With 4D contrast-enhanced MRA, visualization of the venous drainage at the arterial phase.

With TOF and 3D contrast-enhanced MRA, enlarged and dilated serpiginous vessels and/or direct visualization of the fistulous point/nidus.

For each patient, all the MR images were assessed by using a dedicated workstation (Advantage Windows Workstation; GE Healthcare) with multiplanar reformations available. With SWI, axial 10-mm-thick maximum intensity projections were systematically reconstructed as well as raw data and CBF color maps of ASL. With 4D contrast-enhanced MRA, a time-resolved MIP sagittal view was available as well as each of the 3D MRA volumes generated. When assessing combined MR images, the readers had the ability to merge MR images from different sequences, with or without manual thresholding, by using the available fusion software (3D synchroview, Advantage Windows Workstation; GE Healthcare). Discrepancies between readers were resolved by consensus by using a panel, including an additional board-certified neuroradiologist (X.L.). In each patient, signal abnormalities previously detected on MR images by the blinded readers were correlated with the presence or absence of AVS on DSA. Medical records were also systematically reviewed for acute ICH and previous surgical or endovascular AVS treatments.

Statistical Analysis

Statistical analysis was performed by using SAS software, Version 9.3 (SAS Institute, Cary, North Carolina). Interobserver and intermodality agreement was calculated by using the Cohen κ test. κ values were interpreted as follows: κ value of 0 indicates poor agreement; κ values of 0.01–0.20 indicate minor agreement; κ values of 0.21–0.40, fair agreement; κ values of 0.41–0.60, moderate agreement; κ values of 0.61–0.80, good agreement; and κ values of 0.81–1, excellent agreement. For each of the 4 independent readings, we calculated standard diagnostic accuracy parameters (ie, sensitivity, specificity, and positive and negative predictive values) for the detection of AVS in the whole cohort (n = 92), by using DSA as a reference standard. Diagnostic accuracy was also determined by calculating the area under the receiver operating curve (AUC), which equals 0.5 and 1 for models with random and perfect discrimination, respectively. In addition, sensitivity and specificity were calculated in the 2 subgroups: the patients with ICH (n = 24) and those previously treated for AVS (n = 24). The McNemar test was used to compare measures of diagnostic accuracy. The confidence intervals were calculated by using normal based approximation and were truncated to avoid values of >1.