The Role of Double Inversion Recovery Imaging in Acute Ischemic Stroke
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pISSN 2384-1095 iMRI 2019;23:210-219 https://doi.org/10.13104/imri.2019.23.3.210 eISSN 2384-1109 The Role of Double Inversion Recovery Imaging in Acute Ischemic Stroke Na Young Choi, Soonchan Park, Chung Min Lee, Chang-Woo Ryu, Geon-Ho Jahng Department of Radiology, Kyung Hee University Hospital at Gangdong, College of Medicine, Kyung Hee University, Seoul, Korea Magnetic resonance imaging Purpose: The purpose of this study was to investigate if double inversion recovery (DIR) imaging can have a role in the evaluation of brain ischemia, compared with diffusion-weighted imaging (DWI) and fluid-attenuated inversion recovery (FLAIR) imaging. Original Article Materials and Methods: Sixty-seven patients within 48 hours of onset, underwent MRI scans with FLAIR, DWI with b-value of 0 (B0) and 1000 s/mm2, and DIR sequences. Patients were categorized into four groups: within three hours, three to six hours, six to 24 hours, and 24 to 48 hours after onset. Lesion-to-normal ratio (LNR) Received: March 4, 2019 value was calculated and compared among all sequences within each group, by the Revised: May 24, 2019 Friedman test and conducted among all groups, for each sequence by the Kruskal- Accepted: June 10, 2019 Wallis test. In qualitative assessment, signal intensity changes of DIR, B0, and FLAIR Correspondence to: based on similarity with DWI and image quality of each sequence, were graded on a Geon-Ho Jahng, Ph.D. 3-point scale, respectively. Scores for detectability of lesions were compared by the Department of Radiology, Kyung McNemar’s test. Hee University Hospital at Results: LNR values from DWI were higher than DIR, but not statistically significant Gangdong, College of Medicine, Kyung Hee University, #892 in all groups (P > 0.05). LNR values of DIR were significantly higher than FLAIR within Dongnam-ro, Gangdong-gu, 24 hours of onset (P < 0.05). LNR values were significantly different between, before, Seoul 05278, Korea. and after six hours onset time for DIR (P = 0.016), B0 (P = 0.008), and FLAIR (P = 0.018) Tel. +82-2-440-6187 but not for DWI (P = 0.051). Qualitative analysis demonstrated that detectability of Fax. +82-2-440-6932 DIR was higher, compared to that of FLAIR within 4.5 hours and six hours of onset (P [email protected] E-mail: < 0.05). Also, the DWI quality score was lower than that of DIR, particularly relative to infratentorial lesions. Conclusion: DIR provides higher detectability of hyperacute brain ischemia than B0 and FLAIR, and does not suffer from susceptibility artifact, unlike DWI. So, DIR can be This is an Open Access article distributed used to replace evaluation of the FLAIR-DWI mismatch. under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/ Keywords: Double inversion recovery; Acute ischemic stroke; by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and Magnetic resonance imaging; Diffusion MRI; Brain infarction reproduction in any medium, provided the original work is properly cited. INTRODUCTION Copyright © 2019 Korean Society In the acute phase of brain ischemia, the best strategy to demonstrate restricted of Magnetic Resonance in water motion related to cytotoxic edema, is diffusion-weighted imaging (DWI) with Medicine (KSMRM) magnetic resonance imaging (MRI) (1-3). However, single-shot echo-planar imaging (EPI)-based DWI is limited in detecting acute ischemic stroke in some areas of the brain, because of a magnetic susceptibility artifact and a low spatial resolution (4). Also, it is 210 www.i-mri.org https://doi.org/10.13104/imri.2019.23.3.210 an intrinsically low signal-to-noise ratio sequence, caused excluded. In the end, 67 patients (41 men and 26 women; by a large diffusion-encoding gradient. mean age = 66.7; range = age 31 to 86), were enrolled Fluid-attenuated inversion-recovery (FLAIR) and T2- in the study. Patients’ medical history and demographic weighted (T2W) images, as well as conventional T2- information such as age, sex, and duration from symptom based MRI methods, are usually limited in detecting acute onset were obtained. Patients were stratified into four ischemic stroke during the hyperacute phase (2, 3, 5-7), groups based on time after onset of stroke symptoms: because of insufficient sensitivity to detect cytotoxic edema Group I (onset ≤ 3 hours), Group II (3 < onset ≤ 6), Group in the acute phase of infarction (8-10). Additionally, in III (6 < onset ≤ 24), and Group IV (24 < onset ≤ 48). FLAIR, imaging contrast between white and gray matter is Table 1 lists patients’ demographic information. The local usually more or less poor, because transverse magnetization Institutional Review Board approved a waiver of consent for is highly decayed with a lengthy repetition time (TR) and this retrospective study. lengthy echo time (TE). Previous studies reported FLAIR could estimate the age of stroke in patients with unclear MRI Scanning Protocol stroke onset time, by evaluation mismatch of the ischemic Images were acquired with a 3.0 Tesla MRI scanner (Philips lesion compared to DWI (11, 12). Medical System, Achieva, Best, the Netherlands) using a Double inversion recovery (DIR) MRI sequence is a dedicated 8-element phased array sensitivity-encoding method to suppress signals from cerebral spinal fluid (CSF) (SENSE) head coil. Imaging protocols included contiguous and white matter in the brain simultaneously, by applying axial sections of DWI, FLAIR, and DIR. Imaging parameters two inversion pulses with two different inversion times (TI). for the FLAIR sequence were TR/TE/TI =11000/140/2800 ms, This allows the DIR to increase image contrast between slice thickness = 5 mm, field of view (FOV) = 189 × 240 gray and white matter (13, 14). So, a brain lesion can be mm2, and matrix size = 256 × 240, and turbo spin-echo (TSE) distinguished from normal tissue with a DIR image due to factor = 30. Acquisition time for FLAIR was 130 seconds. the difference in T1 relaxation time, because DIR imaging Imaging parameters for the DWI sequence were TR/TE = contrast depends on T1 relaxation time. Although DIR 3540/72 ms, slice thickness = 5 mm, FOV = 230 × 230 mm2, imaging has been applied to brain diseases such as multiple matrix size = 192 × 192, and b-values = 0, and 1000 s/mm2. sclerosis or epilepsy (13, 15-18) and Alzheimer’s (19), no The DIR sequence consisted of two radio frequency (RF) study has evaluated the role of DIR imaging in detecting 180° inversion pulses, preceding TSE imaging acquisition (19, acute ischemic brain lesions. 21). The two TI for the DIR sequence was TI1/TI2 = 2600/360 Since a DIR sequence shows high lesion conspicuity in ms wherein TI1 was the time interval from the first to the gray and white matter compared with FLAIR or T2W images second 180° inversion pulses, and TI2 was the time interval (20), the DIR image may provide better detectability of from the second 180° inversion pulse, to the 90° excitation hyperacute ischemic stroke than FLAIR. So, the purpose of pulse. To set the two TIs, we used the null point for the CSF this study was to evaluate if DIR can detect acute ischemic signal (TI1 = 2650 ms, CSF T1 = 4300 ms), and for white stroke, and to compare lesion contrast of DIR images to that matter (TI2 = 360 ms, WM T1 = 830 ms) in the human brain, of DWI and FLAIR. in a 3 Tesla MRI system (22, 23). Effective TE that was time of sampling the center of k-space, with respect to excitation pulse was 100 ms. Additional imaging parameter were: TR MATERIALS AND METHODS = 8000 ms, slice thickness = 5 mm, echo-spacing = 8.3 ms, echo-train length = 11, acquisition matrix = 256 × 256, Patient Selection reconstruction matrix = 512 × 512, FOV = 180 × 180 mm, From September 2006 to May 2008, a total of 101 matrix size = 356 × 256 mm, number of slices = 25, slice patients underwent MRI scanning with DWI, FLAIR and thickness = 3 mm, gap between slices = 0.3 mm, TSE factor DIR sequences due to ischemic symptoms. Among them, = 44, SENSE factor = 2, and number of averages = 1. Scan we included consecutive patients (n = 76) with ischemic time for the DIR sequence was 140 seconds. The excitation symptoms within 48 hours’ symptom onset time, and with 90° RF pulse was preceded by a fat saturation pulse, and an diffusion restriction lesions. Patients who had other brain inferiorly placed saturation slab to minimize flow artifacts. diseases (n = 1; moyamoya disease), or with hemorrhagic infarction (n = 5) and severe motion artifacts (n = 3) were www.i-mri.org 211 DIR MRI in Ischemic Stroke | Na Young Choi, et al. Imaging Analysis from infarcted and contra-lateral normal brain areas, To identify pathological lesions, images were interpreted volumetric region-of-interests (ROIs) were defined on DWI, by a neuroradiologist (CWR) with 15 years’ experience. at the infarction area and its contra-lateral normal area When multiple diffusion restriction lesions were present in a over several slices using MRIcro software (http://people. patient, the largest lesion was selected for further imaging cas.sc.edu/rorden/mricro/index.html). Mean values of signal analysis. Diffusion restrictive lesions were classified based intensities of DIR, FLAIR, B0, and DWI for each patient were on location and size. According to the location, lesions obtained from the ROIs. were classified as supratentorial or infratentorial lesions. To explore imaging contrast between normal areas and According to size, lesions were classified as small (less than infracted lesions for each sequence, lesion-to-normal ratio 2 cm), medium (2 cm to 4 cm) or large (greater than 4 cm) (LNR) value was calculated as the difference of signal infarcts, based on maximum length of infarction.