Yi Sui1, Arvin Forghanian-Arani1, Joshua D. Trzasko, 1, Matthew C. Murphy1, Phillip J. Rossman1, Kevin J. Glaser1, Kiaran P. McGee1, Armando Manduca2, Richard L. Ehman1, Philip A. Araoz1, and John III Huston1
1Radiology, Mayo Clinic, Rochester, MN, United States, 2Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, United States
Synopsis
This study demonstrates the technical feasibility of a
3D radially batched internal navigator echo magnetic resonance elastography
(TURBINE-MRE) technique in the brain. The highly efficient TURBINE-MRE approach
allows for a true 3D wave displacement field to be acquired over the entire human
brain volume in approximately 1.5 minutes.
Introduction
MR elastography (MRE) has been a useful
tool for studying changes in the mechanical properties of brain tissues due to neurodegenerative diseases or normal aging.1 In more recent studies, there are
increasing interests to investigate the dynamic changes of brain tissue properties related to cerebral arterial pulsation,2 and to detect fast neuronal activity using functional MR Elastography.3 A high spatial and temporal resolution MRE acquisition is desired for these applications, which is
challenging for the 2D Cartesian acquisitions typically used in MRE. Recently, a
3D hybrid radial-EPI readout scheme (TURBINE) was proposed.4,5 The radially rotating EPI blades can provide motion
robustness and higher temporal resolution when combined with a golden-angle scheme, a sliding window view-sharing technique,6 and advanced reconstruction.7 To date, the TURBINE technique has been successfully
applied to DWI4 and fMRI5 that only display
and process magnitude information. However, its ability to obtain stable and accurate phase images (essential for MRE) has not been demonstrated. In this preliminary
work, we developed a TURBINE-MRE sequence and demonstrated its feasibility in
a phantom and 6 volunteers as the first steps towards future advanced applications.Method
Pulse sequence: The proposed TURBINE-MRE sequence is based on a
spoiled gradient-echo MRE sequence with a modified EPI readout (Fig.1a). MRE
motion-encoding gradients (MEGs) were added before EPI readout to encode
MRE harmonic tissue motion into the image phase. The EPI readout axis, Gθ, rotated about the
phase-encoding axis in
successive TRs by a golden angle increment.
Phantom study: A gelatin brain phantom with stiff, spherical
inclusions was scanned on a compact 3T scanner (GE
Healthcare, Waukesha, WI)8,9 with a 32-channel head coil. The TURBINE-MRE data were acquired with a 2.5 mm isotropic resolution and 80 Hz vibration.
For comparison, a standard 2D, multislice, spin-echo EPI-MRE acquisition
was also performed.
In
vivo study: To verify the in-vivo feasibility of the technique, six healthy volunteers were scanned with the same setup as the phantom
study except a 60 Hz vibration was used to compensate for the wave damping in
the brain. In addition, we also
collected 2 mm isotropic data on three additional healthy volunteers to
demonstrated its capability of acquiring high spatial resolution MRE images. The
imaging parameters are summarized in the table in Figure 1.
Image Reconstruction: After
EPI phase correction on every EPI blade, Tikhonov-Regularized SENSE10,11 reconstruction of the multi-coil 3D
radial-Cartesian TURBINE data was then performed via a conjugate-gradient method using
NUFFT regridding12, a Tikhonov
regularization parameter λ=0.001 and 40 iterations. The coil sensitivity profiles were estimated
from a separate calibration scan using a gradient echo sequence.
To study the acceleration potential of TURBINE-MRE, a subset of the EPI blades (16, 32, 64 or 128 blades) was used for image
reconstruction and MRE inversion and compared against the full 192-blade result.
Regional brain stiffness analysis: MRE
stiffness maps were generated using a 3D direct inversion (DI) algorithm to
invert the wave-field as described elsewhere.13,14 The regional brain stiffness analysis
was done in a similar approach as described in the previous study.14 Briefly, six regional ROIs (Fig.3)
were generated from T1-weighted images, and then registered to the MRE magnitude
images and propagated to the stiffness maps. The median stiffness values in each
ROI were used for comparison. Pearson correlation was used to assess the agreement between EPI-MRE and TURBINE-MRE.Results
Figure 2 compares the phantom and the volunteer results
between EPI-MRE and TURBINE-MRE. The TURBINE-MRE magnitude images have low
contrast between tissues since the Ernst angle was chosen for the flip angle to maximize the
signal intensity rather than the contrast. Comparable wave and stiffness maps
were observed, but the 3D-TURBINE-MRE exhibited much less of the slice-to-slice
variation artifacts that are commonly seen in the 2D-EPI-MRE acquisitions.
Figure 3A illustrates the generated regional ROIs of a
representative volunteer, and Figure 3B
shows the scatter plot of the median regional stiffness measured from the six
volunteers. A strong linear correlation (r=0.943) was observed between the two
methods.
Figure 4 shows the relation between the stiffness
values obtained from 16, 32, 64, or 128 blades against that of all 192 blades. Using the current basic reconstruction setup, the stiffness
values were slightly underestimated at a small number of blades (e.g.
N=16 or 32). However, with as few as 64
blades (a 1:20 minutes scan), the stiffness estimation was almost
identical to that of 192 blades (r=0.999), demonstrating the high acceleration
capability of the TURBINE-MRE sequence.
Figure 5. shows the 2 mm isotropic high-resolution
TURBINE-MRE data. High-resolution wave and stiffness maps can be obtained within 6
minutes. Discussion and Conclusion
Using the basic Tikhonov-SENSE reconstruction, a 1:20 minute TURBINE-MRE scan can be achieved. It is encouraging to explore more advanced reconstruction setups (e.g. a wavelet-sparse FISTA model) to further
accelerate the sequence using fewer blades. The TURBINE-MRE sequence is also self-navigated,
therefore it can be suitable for imaging fast dynamic stiffness changes and/or
moving objects with further development. This phantom and in-vivo brain study
demonstrated the feasibility of TURBINE-MRE for acquiring true 3D, high-resolution MRE data in a highly efficient manner, which motivates further exploration of its use for other applications such as functional MRE, free-breathing liver and cardiac MRE.Acknowledgements
This work was supported by grants from the National
Institute of Health (R01 EB001981, R01 EB010065, R01 NS113760, NIBIB EB017197, and NIH U01 EB024450).References
1. Murphy
MC, Huston J, 3rd, Ehman RL. MR elastography of the brain and its application
in neurological diseases. Neuroimage 2017.
2. Schrank F, Warmuth C, Tzschatzsch H,
Kreft B, Hirsch S, Braun J, Elgeti T, Sack I. Cardiac-gated steady-state
multifrequency magnetic resonance elastography of the brain: Effect of cerebral
arterial pulsation on brain viscoelasticity. J Cereb Blood Flow Metab
2019:271678X19850936.
3. Patz S, Fovargue D, Schregel K,
Nazari N, Palotai M, Barbone PE, Fabry B, Hammers A, Holm S, Kozerke S,
Nordsletten D, Sinkus R. Imaging localized neuronal activity at fast time
scales through biomechanics. Sci Adv 2019;5(4).
4. McNab JA, Gallichan D, Miller KL. 3D
steady-state diffusion-weighted imaging with trajectory using radially batched
internal navigator echoes (TURBINE). Magn Reson Med 2010;63(1):235-242.
5. Graedel NN, McNab JA, Chiew M, Miller
KL. Motion correction for functional MRI with three-dimensional hybrid
radial-Cartesian EPI. Magn Reson Med 2016.
6. Jonathan SV, Vakil P, Jeong YI, Menon
RG, Ansari SA, Carroll TJ. RAZER: A Pulse Sequence for Whole-Brain Bolus
Tracking at High Frame Rates. Magnetic Resonance in Medicine
2014;71(6):2127-2138.
7. Feng L, Axel L, Chandarana H, Block
KT, Sodickson DK, Otazo R. XD-GRASP: Golden-angle radial MRI with
reconstruction of extra motion-state dimensions using compressed sensing. Magn
Reson Med 2016;75(2):775-788.
8. Weavers PT, Shu YH, Tao SZ, Huston J,
Lee SK, Graziani D, Mathieu JB, Trzasko JD, Foo TKF, Bernstein MA. Technical
Note: Compact three-tesla magnetic resonance imager with high-performance
gradients passes ACR image quality and acoustic noise tests. Medical Physics
2016;43(3):1259-1264.
9. Tan ET, Lee SK, Weavers PT, Graziani
D, Piel JE, Shu Y, Huston J, 3rd, Bernstein MA, Foo TK. High slew-rate
head-only gradient for improving distortion in echo planar imaging: Preliminary
experience. J Magn Reson Imaging 2016;44(3):653-664.
10. King K, Angelos L. SENSE image quality
improvement using matrix regularization. 2001. p 1771.
11. Pruessmann KP, Weiger M, Bornert P, Boesiger
P. Advances in sensitivity encoding with arbitrary k-space trajectories. Magn
Reson Med 2001;46(4):638-651.
12. Fessler JA, Sutton BP. Nonuniform fast
Fourier transforms using min-max interpolation. Ieee T Signal Proces
2003;51(2):560-574.
13 Manduca A, Oliphant TE, Dresner MA,
Mahowald JL, Kruse SA, Amromin E, Felmlee JP, Greenleaf JF, Ehman RL. Magnetic
resonance elastography: Non-invasive mapping of tissue elasticity. Medical
Image Analysis 2001;5(4):237-254.
14. Murphy MC, Huston J, 3rd, Jack CR, Jr.,
Glaser KJ, Senjem ML, Chen J, Manduca A, Felmlee JP, Ehman RL. Measuring the
characteristic topography of brain stiffness with magnetic resonance
elastography. PLoS One 2013;8(12):e81668.