Eric Seth Michael1, Franciszek Hennel1, and Klaas Paul Pruessmann1
1Institute for Biomedical Engineering, ETH Zurich and University of Zurich, Zurich, Switzerland
Synopsis
Multi-shot techniques for
diffusion MRI are desirable because of the associated improvement potential in
image resolution but are inhibited by phase variability across interleaves,
which results from subject motion and causes ghosting. Here, an EPI-based acquisition
strategy is devised which diminishes the ghosting pattern by employing a
modified interleaving scheme and mitigates motion sensitivity by nulling the
first- and second-order moments of the diffusion-sensitizing gradient waveforms.
This solution yielded unperturbed, high-resolution images in in vivo human
brain scans and clear improvements in image quality compared to acquisitions
incorporating standard interleaving and uncompensated diffusion sensitization.
Introduction
Diffusion-weighted imaging (DWI) is
a powerful diagnostic tool but is predominantly combined with single-shot EPI
acquisitions, thereby limiting the attainable resolution. Segmented
acquisitions can provide improved resolution but are hindered by motion-induced
shot-to-shot phase variability, which leads to ghosting in reconstructed images
when neglected.1 One promising approach for
resolving this issue is to suppress phase variations by utilizing diffusion-sensitizing
gradient sequences with nulled moments (i.e., motion-compensation); this method
yielded high quality images for interleaved spiral acquisitions.2 Translation of this approach
to EPI, however, may be nontrivial because interleaved EPI acquisitions suffer trains
of ghosts for standard interleaving (i.e., when all interleaved k-space
trajectories begin at the same corner of k-space) even in the absence of phase
fluctuations.3 That said, ghosting can be
reduced by employing a modified interleaving scheme (particularly, for acquisitions
with an odd number of interleaves) in which even and odd interleaves begin at opposite
corners of k-space, thereby returning the sampling pattern to that of
single-shot EPI.4
In light of these considerations,
the aim of this work is to evaluate the feasibility of multi-shot DW-EPI in
conjunction with second-order motion-compensated diffusion gradients and the
modified EPI interleaving scheme.Methods
Scanning was performed using a 3T
Philips Achieva system (Philips Healthcare, Best, the Netherlands) with a
high-performance gradient insert that could reach gradient amplitudes up to 100
mT/m and slew rates up to 1200 mT/m/ms at 100% duty cycle.5
To capture the dependence of imaging performance on the interleaving scheme, a
stationary silicon oil phantom was scanned using pulsed gradient spin-echo
(PGSE) sequences, which are uncompensated, combined with three-shot EPI
readouts with standard and modified interleaving schemes, which are depicted in
Figure 1. Subsequently, to examine the utility of motion-compensated diffusion
gradients in conjunction with modified interleaving, two healthy adult
volunteers were scanned using the modified three-shot EPI acquisitions combined
with pulsed gradients and velocity- and acceleration-compensated oscillating
diffusion gradients2 derived from improved oscillating
gradient spin-echo (OGSE) waveforms.6 Figure 2 depicts the two gradient
shapes as well as nulled higher-order moments of the oscillating gradients,
which corresponds to the desired motion compensation. Identical imaging
parameters were used across all acquisitions: 1.5 mm in-plane resolution, 10
slices, 3 mm slice thickness, 2 mm slice gap, b = 800 s/mm2, two b =
0 acquisitions and 3 DWI directions (each aligned with a Cartesian coordinate
axis) with 2 repetitions each, and TR/TE = 4000/103 ms.
All scans were repeated using a
Dynamic Field Camera7 (Skope Magnetic Resonance
Technologies, Zurich, Switzerland) to monitor the spatiotemporal field dynamics
associated with the imaging gradients; third-order spherical harmonic models
were fitted to these data and were utilized in an algebraic reconstruction
algorithm,8 which also incorporated
off-resonance maps. Reconstructed images were smoothed with Hamming filters to
reduce Gibbs ringing, after which maps of mean diffusivity (MD) were computed
as the average diffusivity of the three diffusion gradient directions. Results
Figure 3 depicts phantom images acquired with standard
and modified interleaving schemes for b = 0 and for each diffusion gradient
direction; multiple ghosts are visible for standard interleaving but become highly
suppressed for the modified interleaving. The combination of the modified
scheme with pulsed and second-order motion-compensated diffusion gradients is
shown in Figure 4 for a slice of one volunteer, which depicts repetitions of diffusion-weighted
images for each gradient direction as well as mean diffusivity (MD) maps. In
the acceleration-compensated case, all diffusion-weighted images lack discernible
artifacts and yield a high quality MD map, whereas all but one uncompensated
image have some level of ghosting or signal dropout, which deteriorate the MD
map. Discussion
The reduction in the number of visible ghosts for
acquisitions with modified interleaving compared to those with standard
interleaving can be attributed to the favorable k-space sampling pattern of the
former,4 which yields only very faint ghosts
at FOV/2, like single-shot EPI. The suppression of this residual ghost is
likely a byproduct of the higher-order field model, without which stronger
ghosting would have occurred.
In the subsequent diffusion-weighted in vivo images, the
visible ghosting for the uncompensated diffusion gradients again only
appears at FOV/2, whereas the signal dropouts, which appear near CSF in the
ventricles and lead to falsely elevated MD values, do not appear patterned and
are likely caused by phase variability induced by pulsatile motion.9 In the motion-compensated case, for
which constant velocity and acceleration motion is not encoded into phase, the
repeated acquisitions do not contain discernible forms of either artifact,
thereby obviating the need for a reconstruction method dedicated to accounting
for shot-to-shot phase variability.1,10
Compensating for motion of increasing orders inherently
reduces the encoding efficiency and is responsible for the relatively long TEs.
However, more efficient methods for motion compensation exist;11 future work should investigate such
approaches with this implementation, which may enable a sufficient b-value/TE
combination for translation to a standard gradient system.Conclusion
This study demonstrates the feasibility of the multi-shot
DW-EPI implementation utilized here, which combined acceleration-compensated
diffusion sensitization and a modified interleaving scheme and provided images of
high quality without a reconstruction method dedicated to the typical issues of
interleaved DWI.Acknowledgements
No acknowledgement found.References
1. Chen
N-k, Guidon A, Chang H-C, Song AW. A robust multi-shot scan strategy for
high-resolution diffusion weighted MRI enabled by multiplexed
sensitivity-encoding (MUSE). Neuroimage. 2013;72:41-47.
2. Michael ES, Hennel F, Pruessmann KP.
Multi-shot diffusion MRI of the human brain with motion-compensated oscillating
gradients. In Proceedings of the 2021 ISMRM & SMRT Annual Meeting, 2021.
Abstract #1324.
3. McKinnon GC. Ultrafast interleaved
gradient-echo-planar imaging on a standard scanner. Magn Reson Med.
1993;30(5):609-616.
4. Hennel F. Image-based reduction of
artifacts in multishot echo-planar imaging. J Magn Reson. 1998;134(2):206-213.
5. Weiger
M, Overweg J, Rösler MB, et al. A high-performance gradient insert for
rapid and short-T2 imaging at full duty cycle. Magn Reson Med.
2018;79(6):3256-3266.
6. Hennel F, Michael ES, Pruessmann KP.
Improved gradient waveforms for oscillating gradient spin-echo (OGSE) diffusion
tensor imaging. NMR Biomed. 2021;34(2):e4434.
7. Dietrich BE, Brunner DO, Wilm BJ, et
al. A field camera for MR sequence monitoring and system analysis. Magn Reson
Med. 2016;75(4):1831-1840.
8. Wilm BJ, Barmet C, Pavan M, Pruessmann
KP. Higher order reconstruction for MRI in the presence of spatiotemporal field
perturbations. Magn Reson Med. 2011;65(6):1690-1701.
9. Miller KL, Pauly JM. Nonlinear phase
correction for navigated diffusion imaging. Magn Reson Med. 2003;50(2):343-353.
10. Mani M, Jacob M, Kelley D, Magnotta V.
Multi-shot sensitivity-encoded diffusion data recovery using structured
low-rank matrix completion (MUSSELS). Magn Reson Med. 2017;78(2):494-507.
11. Aliotta E, Wu HH, Ennis DB. Convex
optimized diffusion encoding (CODE) gradient waveforms for minimum echo time
and bulk motion–compensated diffusion-weighted MRI. Magn Reson Med.
2017;77(2):717-729.