3D diffusion MRI with twin navigator-based GRASE and comparison with 2D EPI for tractography in the human brain.

PURPOSE: 3D pulse sequences enable high-resolution acquisition with a high SNR and ideal slice profiles, which, however, is particularly difficult for diffusion MRI (dMRI) due to the additional phase errors from diffusion encoding. METHODS: We proposed a twin navigator-based 3D diffusion-weighted gradient spin-echo (GRASE) sequence to correct the phase errors between shots and between odd and even spin echoes for human whole-brain acquisition. We then compared the SNR of 3D GRASE and 2D simultaneous multi-slice EPI within the same acquisition time. We further tested the performance of 2D versus 3D acquisition at equivalent SNR on fiber tracking and microstructural mapping, using the diffusion tensor and high-order fiber orientation density-based metrics. RESULTS: The proposed twin navigator approach removed multi-shot phase errors to some extent in the whole brain dMRI, and the 2D navigator performed better than the 1D navigator. Comparisons of SNR between the 2D simultaneous multi-slice EPI and 3D GRASE sequences demonstrated that the SNR of the GRASE sequence was 1.4-1.5-fold higher than the EPI sequence at an equivalent scan time. More importantly, we found a significantly higher fiber cross-section in the cerebrospinal tract, as well as richer subcortical fibers (U-fibers) using the 3D GRASE sequence compared to 2D EPI. CONCLUSION: The twin navigator-based 3D diffusion-weighted-GRASE sequence minimized the multishot phase error and effectively improved the SNR for whole-brain dMRI acquisition. We found differences in fiber tracking and microstructural mapping between 2D and 3D acquisitions, possibly due to the different slice profiles.

Inversion-Recovery-Prepared Oscillating Gradient Sequence Improves Diffusion-Time Dependency Measurements in the Human Brain.

BACKGROUND: Oscillating gradient diffusion MRI (dMRI) enables measurements at a short diffusion-time (td ), but it is challenging for clinical systems. Particularly, the low b-value and low resolution may give rise to cerebrospinal fluid (CSF) contamination. PURPOSE: To assess the effect of CSF partial volume on td -dMRI measurements and efficacy of inversion-recovery (IR) prepared oscillating and pulsed gradient dMRI sequence to improve td -dMRI measurements in the human brain. STUDY TYPE: Prospective. SUBJECTS: Ten normal volunteers and six glioma patients. FIELD STRENGTH/SEQUENCE: A 3 T; three-dimensional (3D) IR-prepared oscillating gradient-prepared gradient spin-echo (GRASE) and two-dimensional (2D) IR-prepared oscillating gradient echo-planar imaging (EPI) sequences. ASSESSMENT: We assessed the td -dependent patterns of apparent diffusion coefficient (ADC) in several gray and white matter structures, including the hippocampal subfields (head, body, and tail), cortical gray matter, thalamus, and posterior white matter in normal volunteers. Pulsed gradient (0 Hz) and oscillating gradients at frequencies of 20 Hz, 40 Hz, and 60 Hz dMRI were acquired with GRASE and EPI sequences with or without the IR module. We also tested the td -dependency patterns in glioma patients using the EPI sequence with or without the IR module. STATISTICAL TESTS: The differences in ADC across the different td s were compared by one-way ANOVA followed by post hoc pairwise t-tests with Bonferroni correction. RESULTS: In the healthy subjects, brain regions that were possibly contaminated by CSF signals, such as the hippocampus (head, body, and tail) and cortical gray matter, td -dependent ADC changes were only significant with the IR-prepared 2D and 3D sequences but not with the non-IR sequences. In brain glioblastomas patients, significantly higher td -dependence was observed in the tumor region with the IR module than that without IR (slope = 0.0196 µm2 /msec2 vs. 0.0034 µm2 /msec2 ). CONCLUSION: The IR-prepared sequence effectively suppressed the CSF partial volume effect and significantly improved the td -dependent measurements in the human brain. EVIDENCE LEVEL: 1 TECHNICAL EFFICACY: Stage 1.

Three-dimensional gradient and spin-echo readout for time-encoded pseudo-continuous arterial spin labeling: Influence of segmentation factor and flow compensation.

PURPOSE: To monitor the complete passage of the labeled blood through the vascular tree into tissue and improve the quantification of ASL maps, we evaluated the effect of 3D gradient and spin-echo (GRASE) readout segments on temporal SNR (tSNR) and image blurriness for time-encoded pseudo-continuous arterial spin labeling and the effect of flow-compensation gradients on the presence of intravascular signal. METHODS: Fifteen volunteers were scanned using time-encoded pCASL with 2D EPI and single-segment, two-segments, and three-segments 3D-GRASE readouts with first-order flow compensation (FC) gradients. Two-segments 3D-GRASE scans were acquired with 25%, 50%, 75%, and 100% of full first-order FC. Temporal SNR was assessed, and cerebral blood flow and arterial blood volume were quantified for all readout strategies. RESULTS: For single-segment 3D GRASE, tSNR was comparable to 2D EPI for perfusion signal but worse for the arterial signal. Two-segments and three-segments 3D GRASE resulted in higher tSNR than 2D EPI for perfusion and arterial signal. The arterial signal was not well visualized for 3D-GRASE data without FC. Visualization of the intravascular signal at postlabeling delays of 660 ms and 1060 ms was restored with FC. Adequate visualization of the intravascular signal was achieved from 75% of FC gradient strength at a postlabeling delay of 660 ms. For a postlabeling delay of 1060 ms, full-FC gradients were the best option to depict intravascular signal. CONCLUSION: Segmented GRASE provided higher effective tSNR compared with 2D-EPI and single-segment GRASE. Flow compensation with GRASE readout should be carefully controlled when applying for time-encoded pCASL to visualize intravascular signal.

Diffusion-prepared 3D gradient spin-echo sequence for improved oscillating gradient diffusion MRI.

PURPOSE: Oscillating gradient (OG) enables the access of short diffusion times for time-dependent diffusion MRI (dMRI); however, it poses several technical challenges for clinical use. This study proposes a 3D oscillating gradient-prepared gradient spin-echo (OGprep-GRASE) sequence to improve SNR and shorten acquisition time for OG dMRI on clinical scanners. METHODS: The 3D OGprep-GRASE sequence consisted of global saturation, diffusion encoding, fat saturation, and GRASE readout modules. Multiplexed sensitivity-encoding reconstruction was used to correct the phase errors between multiple shots. We compared the scan time and SNR of the proposed sequence and the conventional 2D-EPI sequence for OG dMRI at 30-90-mm slice coverage. We also examined the time-dependent diffusivity changes with OG dMRI acquired at frequencies of 50 Hz and 25 Hz and pulsed-gradient dMRI at diffusion times of 30 ms and 60 ms. RESULTS: The OGprep-GRASE sequence reduced the scan time by a factor of 1.38, and increased the SNR by 1.74-2.27 times compared with 2D EPI for relatively thick slice coverage (60-90 mm). The SNR gain led to improved diffusion-tensor reconstruction in the multishot protocols. Image distortion in 2D-EPI images was also reduced in GRASE images. Diffusivity measurements from the pulsed-gradient dMRI and OG dMRI showed clear diffusion-time dependency in the white matter and gray matter of the human brain, using both the GRASE and EPI sequences. CONCLUSION: The 3D OGprep-GRASE sequence improved scan time and SNR and reduced image distortion compared with the 2D multislice acquisition for OG dMRI on a 3T clinical system, which may facilitate the clinical translation of time-dependent dMRI.

Oxygen extraction fraction mapping with multi-parametric quantitative BOLD MRI: Reduced transverse relaxation bias using 3D-GraSE imaging.

Magnetic resonance imaging (MRI)-based quantification of the blood-oxygenation-level-dependent (BOLD) effect allows oxygen extraction fraction (OEF) mapping. The multi-parametric quantitative BOLD (mq-BOLD) technique facilitates relative OEF (rOEF) measurements with whole brain coverage in clinically applicable scan times. Mq-BOLD requires three separate scans of cerebral blood volume and transverse relaxation rates measured by gradient-echo (1/T2∗) and spin-echo (1/T2). Although the current method is of clinical merit in patients with stroke, glioma and internal carotid artery stenosis (ICAS), there are relaxation measurement artefacts that impede the sensitivity of mq-BOLD and artificially elevate reported rOEF values. We posited that T2-related biases caused by slice refocusing imperfections during rapid 2D-GraSE (Gradient and Spin Echo) imaging can be reduced by applying 3D-GraSE imaging sequences, because the latter requires no slice selective pulses. The removal of T2-related biases would decrease overestimated rOEF values measured by mq-BOLD. We characterized effects of T2-related bias in mq-BOLD by comparing the initially employed 2D-GraSE and two proposed 3D-GraSE sequences to multiple single spin-echo reference measurements, both in vitro and in vivo. A phantom and 25 participants, including young and elderly healthy controls as well as ICAS-patients, were scanned. We additionally proposed a procedure to reliably identify and exclude artefact affected voxels. In the phantom, 3D-GraSE derived T2 values had 57% lower deviation from the reference. For in vivo scans, the formerly overestimated rOEF was reduced by -27% (p â€‹< â€‹0.001). We obtained rOEF â€‹= â€‹0.51, which is much closer to literature values from positron emission tomography (PET) measurements. Furthermore, increased sensitivity to a focal rOEF elevation in an ICAS-patient was demonstrated. In summary, the application of 3D-GraSE improves the mq-BOLD-based rOEF quantification while maintaining clinically feasible scan times. Thus, mq-BOLD with non-slice selective T2 imaging is highly promising to improve clinical diagnostics of cerebrovascular diseases such as ICAS.

Improved velocity-selective-inversion arterial spin labeling for cerebral blood flow mapping with 3D acquisition.

PURPOSE: To further optimize the velocity-selective arterial spin labeling (VSASL) sequence utilizing a Fourier-transform based velocity-selective inversion (FT-VSI) pulse train, and to evaluate its utility for 3D mapping of cerebral blood flow (CBF) with a gradient- and spin-echo (GRASE) readout. METHODS: First, numerical simulations and phantom experiments were done to test the susceptibility to eddy currents and B1 field inhomogeneities for FT-VSI pulse trains with block and composite refocusing pulses. Second, the choices of the post-labeling delay (PLD) for FT-VSI prepared 3D VSASL were evaluated for the sensitivity to perfusion signal. The study was conducted among a young-age and a middle-age group at 3T. Both signal-to-noise ratio (SNR) and CBF were quantitatively compared with pseudo-continuous ASL (PCASL). The optimized 3D VSI-ASL was also qualitatively compared with PCASL in a whole-brain coverage among two healthy volunteers and a brain tumor patient. RESULTS: The simulations and phantom test showed that composite refocusing pulses are more robust to both eddy-currents and B1 field inhomogeneities than block pulses. 3D VSASL images with FT-VSI preparation were acquired over a range of PLDs and PLD = 1.2 s was selected for its higher perfusion signal. FT-VSI labeling produced quantitative CBF maps with 27% higher SNR in gray matter compared to PCASL. 3D whole-brain CBF mapping using VSI-ASL were comparable to the corresponding PCASL results. CONCLUSION: FT-VSI with 3D-GRASE readout was successfully implemented and showed higher sensitivity to perfusion signal than PCASL for both young and middle-aged healthy volunteers.

3D MRI of whole-brain water permeability with intrinsic diffusivity encoding of arterial labeled spin (IDEALS).

This work proposes a novel MRI method - Intrinsic Diffusivity Encoding of Arterial Labeled Spin (IDEALS) - for the whole-brain mapping of water permeability in the human brain without an exogenous contrast agent. Quantitative separation of the intravascular and extravascular labeled water MRI signal was achieved in arterial spin labeling experiments with segmented 3D-GRASE acquisition by modulating the relative sensitivity between relaxation, true diffusion, and pseudodiffusion. The intrinsic diffusivity encoding in k-space created different broadening of the image-domain point spread functions for intravascular and extravascular labeled spins, from which blood-brain barrier (BBB) water extraction fraction (Ew) and water permeability surface area product (PSw) were estimated. The feasibility and sensitivity of this method was evaluated in healthy subjects at baseline and after caffeine challenge. The estimated baseline Ew and PSw maps showed contrast among gray matter (GM) and white matter (WM). GM Ew was significantly lower than that of WM (78.8% ±â€¯3.3% in GM vs. 83.9% ±â€¯4.6% in WM; p < 0.05) and GM PSw was significantly higher than that of WM (131.7 ±â€¯29.5 mL/100  g/min in GM vs. 76.2 ±â€¯18.4 mL/100  g/min in WM; p < 0.05). BBB Ew was significantly lower for females than males (74.9% ±â€¯3.7% for females vs. 81.3% ±â€¯3.3% for males in GM; 80.5% ±â€¯4.7% for females vs. 86.1 ±â€¯3.0 for males in WM; p < 0.05 for both), while significant PSw differences were only observed in WM (143.8 ±â€¯34.4 mL/100  g/min for females vs. 123.6 ±â€¯24.4 mL/100  g/min for males in GM; 91.6 ±â€¯15.0 mL/100  g/min for females vs. 65.9 ±â€¯12.5 mL/100  g/min for males in WM; p = 0.20 and p < 0.05 for GM and WM respectively). Significant correlations between Ew and CBF (r = -0.32, p < 0.05) and between PSw and CBF (r = 0.89, p < 0.05) were observed, consistent with 15O-H2O PET findings. After caffeine challenge, reduced CBF, Ew and PSw were observed, demonstrating the sensitivity of IDEALS approach.

Diffusion sensitivity of 3D-GRASE in arterial spin labeling perfusion.

PURPOSE: To evaluate the role of true diffusion and flow-related pseudodiffusion in cerebral blood flow (CBF) quantification using arterial spin labeling (ASL) with single-shot or segmented 3D gradient and spin echo (GRASE) readouts. THEORY: The extended phase graph (EPG) algorithm, originally designed to model the effects of T1 /T2 relaxation and true diffusion in MRI acquisitions utilizing multiple refocusing RF pulses, was augmented (aEPG). This augmentation accounted for flow-related pseudodiffusion attenuation of intravascular MRI signal in the k-space domain during 3D-GRASE acquisition, which leads to blur along the partition direction in the image domain. Blurring of ASL signal into neighboring voxels can lead to underestimation of CBF in small, high-flow structures such as cortical gray matter (GM). METHODS: The diffusion sensitivity of 3D-GRASE was evaluated through aEPG simulations and in vivo experiments in 13 healthy subjects. The CBF estimation bias for different postlabeling delays, crusher gradient strengths, and segmentation factors along the partition (PAR) and phase-encoding (PE) directions was numerically assessed by simulations and experimentally validated. RESULTS: In vivo experiments demonstrated systematic underestimation of mean GM CBF measured with segmented 3D-GRASE. The GM CBF underestimation depended on ASL preparation and imaging parameters; it reached up to 25% at low-segmentation schemes (1PAR × 2PE ) but was considerably lower at high-segmentation schemes (4PAR × 2PE or 8PAR × 2PE ). Theoretical predictions showed that conventional T1 /T2 relaxation and true diffusion may account for at most ∼25% of GM CBF estimation bias, whereas the pseudodiffusion effect constituted the major fraction in a typical ASL experiment. CONCLUSION: The pseudodiffusion effect leads to considerable estimation bias in ASL-based CBF quantification using 3D-GRASE readouts. This bias can be substantially reduced by increasing the segmentation factors. Magn Reson Med 80:736-747, 2018. Published 2018. This article is a U.S. Government work and is in the public domain in the USA.

Accelerated 3D-GRASE imaging improves quantitative multiple post labeling delay arterial spin labeling.

PURPOSE: To investigate the impact of accelerated, single-shot 3D-GRASE acquisition on quantitative arterial spin labeling (ASL) with multiple and single post-labeling delay (PLD) in terms of perfusion-weighted SNR per unit scan time (TSNRPW ) and quantification accuracy. METHODS: Five subjects were scanned on a 3T MRI scanner using the pseudo-continuous arterial spin labeling (PCASL) technique with a 3D-GRASE imaging sequence capable of parallel imaging acceleration. A 3-inversion pulse background suppression was simulated and implemented in the sequence. Three time-matched single PLD measurements, a segmented one without acceleration, 1 with conventional GRAPPA, and 1 with CAIPIRINHA sampling, were used to compare TSNRPW . Three time-matched multiple PLD measurements with the identical imaging parameters were additionally evaluated (no acceleration vs. CAIPIRINHA sampling vs. CAIPIRINHA sampling with doubled number of PLDs). Cerebral blood flow and arterial transit time fit uncertainties were compared and used as a quality measure. RESULTS: The single PLD measurements show an 11% TSNRPW increase using CAIPIRINHA sampling instead of GRAPPA sampling, while the non-accelerated scan exhibits 35% higher TSNRPW compared to the GRAPPA scan. However, taking advantage of the increased number of averages for multiple PLD acquisitions, a 14%/16% (gray matter) and 34%/36% (white matter) reduction of CBF fit uncertainty is observed with CAIPIRINHA sampling (6 PLDs/12 PLDs) compared to no acceleration. CONCLUSION: Accelerated single-shot 3D-GRASE with PCASL allows for smaller quantification uncertainties than time-matched segmented acquisitions. Corresponding single-shot acquisitions with acceptable blurring and no intra-volume motion render state-of-the-art ASL methods in a clinically feasible time possible.

Calibrated bold fMRI with an optimized ASL-BOLD dual-acquisition sequence.

Calibrated fMRI techniques estimate task-induced changes in the cerebral metabolic rate of oxygen (CMRO2) based on simultaneous measurements of cerebral blood flow (CBF) and blood-oxygen-level-dependent (BOLD) signal changes evoked by stimulation. To determine the calibration factor M (corresponding to the maximum possible BOLD signal increase), BOLD signal and CBF are measured in response to a gas breathing challenge (usually CO2 or O2). Here we describe an ASL dual-acquisition sequence that combines a background-suppressed 3D-GRASE readout with 2D multi-slice EPI. The concatenation of these two imaging sequences allowed separate optimization of the acquisition for CBF and BOLD data. The dual-acquisition sequence was validated by comparison to an ASL sequence with a dual-echo EPI readout, using a visual fMRI paradigm. Results showed a 3-fold increase in temporal signal-to-noise ratio (tSNR) of the ASL time-series data while BOLD tSNR was similar to that obtained with the dual-echo sequence. The longer TR of the proposed dual-acquisition sequence, however, resulted in slightly lower T-scores (by 30%) in the BOLD activation maps. Further, the potential of the dual-acquisition sequence for M-mapping on the basis of a hypercapnia gas breathing challenge and for quantification of CMRO2 changes in response to a motor activation task was assessed. In five subjects, an average gray matter M-value of 8.71±1.03 and fractional changes of CMRO2 of 12.5±5% were found. The new sequence remedies the deficiencies of prior combined BOLD-ASL acquisition strategies by substantially enhancing perfusion tSNR, which is essential for accurate BOLD calibration.

Variable flip angle 3D-GRASE for high resolution fMRI at 7 tesla.

PURPOSE: To evaluate the use of variable flip angle refocusing pulse trains in single-shot three-dimensional gradient and spin-echo (3D-GRASE) to reduce blurring and increase the spatial coverage for high spatial resolution T2 -weighted functional MRI at 7 Tesla. METHODS: Variable flip angle refocusing schemes in 3D-GRASE were calculated based on extended phase graph theory. The blurring along the slice (partition) direction was evaluated in simulations, as well as phantom and in vivo experiments. Furthermore, temporal stability and functional sensitivity at 0.8 mm isotropic resolution were assessed. RESULTS: Variable flip angle refocusing schemes yielded significantly reduced blurring compared with conventional refocusing schemes, with the full width at half maximum being approximately 30-40% narrower. Simultaneously, spatial coverage could be increased by 80%. The temporal signal-to-noise ratio was slightly reduced, but functional sensitivity was largely maintained due to increased functional contrast in the variable flip angle acquisitions. Signal-to-noise ratio and functional sensitivity were reduced more strongly in areas with insufficient radiofrequency transmission indicating higher sensitivity to experimental imperfections. CONCLUSION: Variable flip angle refocusing schemes increase usability of 3D-GRASE for high-resolution functional MRI by reducing blurring and allowing increased spatial coverage. Magn Reson Med 76:897-904, 2016. © 2015 Wiley Periodicals, Inc.

Comparison of 2D and 3D single-shot ASL perfusion fMRI sequences.

Arterial spin labeling (ASL) can be implemented by combining different labeling schemes and readout sequences. In this study, the performance of 2D and 3D single-shot pulsed-continuous ASL (pCASL) sequences was assessed in a group of young healthy volunteers undergoing a baseline perfusion and a functional study with a sensory-motor activation paradigm. The evaluated sequences were 2D echo-planar imaging (2D EPI), 3D single-shot fast spin-echo with in-plane spiral readout (3D FSE spiral), and 3D single-shot gradient-and-spin-echo (3D GRASE). The 3D sequences were implemented with and without the addition of an optimized background suppression (BS) scheme. Labeling efficiency, signal-to-noise ratio (SNR), and gray matter (GM) to white matter (WM) contrast ratio were assessed in baseline perfusion measurements. 3D acquisitions without BS yielded 2-fold increments in spatial SNR, but no change in temporal SNR. The addition of BS to the 3D sequences yielded a 3-fold temporal SNR increase compared to the unsuppressed sequences. 2D EPI provided better GM-to-WM contrast ratio than the 3D sequences. The analysis of functional data at the subject level showed a 3-fold increase in statistical power for the BS 3D sequences, although the improvement was attenuated at the group level. 3D without BS did not increase the maximum t-values, however, it yielded larger activation clusters than 2D. These results demonstrate that BS 3D single-shot imaging sequences improve the performance of pCASL in baseline and activation studies, particularly for individual subject analyses where the improvement in temporal SNR translates into markedly enhanced power for task activation detection.

Impact of susceptibility-induced distortion correction on perfusion imaging by pCASL with a segmented 3D GRASE readout.

PURPOSE: The consensus for the clinical implementation of arterial spin labeling (ASL) perfusion imaging recommends a segmented 3D Gradient and Spin-Echo (GRASE) readout for optimal signal-to-noise-ratio (SNR). The correction of the associated susceptibility-induced geometric distortions has been shown to improve diagnostic precision, but its impact on ASL data has not been systematically assessed and it is not consistently part of pre-processing pipelines. Here, we investigate the effects of susceptibility-induced distortion correction on perfusion imaging by pseudo-continuous ASL (pCASL) with a segmented 3D GRASE readout. METHODS: Data acquired from 28 women using pCASL with 3D GRASE at 3T was analyzed using three pre-processing options: without distortion correction, with distortion correction, and with spatial smoothing (without distortion correction) matched to control for blurring effects induced by distortion correction. Maps of temporal SNR (tSNR) and relative perfusion were analyzed in eight regions-of-interest (ROIs) across the brain. RESULTS: Distortion correction significantly affected tSNR and relative perfusion across the brain. Increases in tSNR were like those produced by matched spatial smoothing in most ROIs, indicating that they were likely due to blurring effects. However, that was not the case in the frontal and temporal lobes, where we also found increased relative perfusion with distortion correction even compared with matched spatial smoothing. These effects were found in both controls and patients, with no interactions with the participant group. CONCLUSION: Correction of susceptibility-induced distortions significantly impacts ASL perfusion imaging using a segmented 3D GRASE readout, and this step should therefore be considered in ASL pre-processing pipelines. This is of special importance in clinical studies, reporting perfusion across ROIs defined on relatively undistorted images and when conducting group analyses requiring the alignment of images across different subjects.

Sub-millimeter T2 weighted fMRI at 7 T: comparison of 3D-GRASE and 2D SE-EPI.

Functional magnetic resonance imaging (fMRI) allows studying human brain function non-invasively up to the spatial resolution of cortical columns and layers. Most fMRI acquisitions rely on the blood oxygenation level dependent (BOLD) contrast employing T(*) 2 weighted 2D multi-slice echo-planar imaging (EPI). At ultra-high magnetic field (i.e., 7 T and above), it has been shown experimentally and by simulation, that T2 weighted acquisitions yield a signal that is spatially more specific to the site of neuronal activity at the cost of functional sensitivity. This study compared two T2 weighted imaging sequences, inner-volume 3D Gradient-and-Spin-Echo (3D-GRASE) and 2D Spin-Echo EPI (SE-EPI), with evaluation of their imaging point-spread function (PSF), functional specificity, and functional sensitivity at sub-millimeter resolution. Simulations and measurements of the imaging PSF revealed that the strongest anisotropic blurring in 3D-GRASE (along the second phase-encoding direction) was about 60% higher than the strongest anisotropic blurring in 2D SE-EPI (along the phase-encoding direction). In a visual paradigm, the BOLD sensitivity of 3D-GRASE was found to be superior due to its higher temporal signal-to-noise ratio (tSNR). High resolution cortical depth profiles suggested that the contrast mechanisms are similar between the two sequences, however, 2D SE-EPI had a higher surface bias owing to the higher T(*) 2 contribution of the longer in-plane EPI echo-train for full field of view compared to the reduced field of view of zoomed 3D-GRASE.