Yang Ji1,2, Congyu Liao3, William Scott Hoge4, Berkin Bilgic5, Yogesh Rathi1,4, and Lipeng Ning1
1Department of Psychiatry, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, United States, 2Wellcome Centre for Integrative Neuroimaging, FMRIB Division, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom, 3Department of Radiology, Stanford University, Stanford, CA, United States, 4Department of Radiology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, United States, 5Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Boston, MA, United States
Synopsis
Combined diffusion-relaxometry has demonstrated promising capability to noninvasively
probe tissue microstructure by joint modeling of relaxation coefficients and
diffusivity. Our recent work has introduced a sequence based on the
time-division multiplexing technique to accelerate the acquisition of
relaxation-diffusion MRI. In this work, we further developed the TDM-EPI
sequence by integrating ky-shifted k-space sampling strategies for data
acquired at different TEs. Moreover, we implemented and compared several reconstruction
methods to integrate complementary k-space samples to joint estimate images at
different TEs. The results showed that the joint reconstruction approach can
improve image quality and reduce artifact compared with conventional
reconstruction methods.
Introduction
Joint modeling of diffusion MRI (dMRI) with multiple echo-times (TEs),
i.e., combined diffusion-relaxometry, has demonstrated promising capability to
improve tissue microstructure estimation compared with standard single-TE dMRI1-5. However, the
prolonged scan time and relative low SNR for dMRI with long TE are limitations for
the application of the diffusion-relaxometry technique in neuroimaging
research. To overcome the limitations, our recent work6 has introduced a time-division
multiplexing echo-planar imaging (TDM-EPI) technique to accelerate the scan of
diffusion-relaxometry, which can simultaneously acquire dMRI with multiple TEs to
achieve ~3X acceleration while maintaining almost identical SNR and signal
intensity compared with the standard method. In this work, we aim to further
improve the image quality by combining novel acquisition schemes in TDM-EPI and
advanced reconstruction algorithms. On the acquisition side, we introduce a modified
TDM-EPI sequence with complementary k-space sampling, in which each echo has a
relative Δ ky shift for k-space sampling. On the reconstruction side, we implement
and compare different algorithms that jointly reconstruct multi-TE diffusion-weighted
images by integrating complementary k-space samplings to improve the capability
of parallel imaging.Methods
Data acquisition:
Figure1 shows the proposed TDM-EPI sequence diagram where the relative
shift of the k-space sampling along ky direction for the echoes at
three different TE are +Δky ,0 and –Δky,
respectively. The proposed sequence was implemented on a 3T MAGNETOM Prisma
scanner to acquire multi-TE dMRI data from a healthy volunteer. To avoid double
diffusion encoding effect7, echo-shifting gradient was
applied adaptively perpendicular to the diffusion gradient and the shift factor
kshift=9.1rad/mm following results from our previous work6. The scan parameters for the diffusion
experiments were as follows: TR =3000ms, FOV=210×210mm2, PF=6/8,
2.0 mm isotropic resolution, TE = (79 ms, 109 ms and 139 ms). Diffusion-weighted
images were acquired along 30 gradient directions at b = 500, 750, 1500, 2250,
and 3000 s/mm2 together with 10 nondiffusion-weighted (b = 0 s/mm2)
images.
Images reconstruction:
Joint GRAPPA methods:
To exploit different sampling patterns across multi-TE,
joint-GRAPPA was proposed for jointly reconstructing the multi-TE images8. The strategy of Joint-GRAPPA is
illustrated in Figure 2A, in which the missing point are estimated not only
from the nearby sampled points within the k-space but also from staggered
points in other k-space with different TE. However, due to the shot-to-shot
phase variations between the acquisitions with different TE, a joint
reconstruction without a prior phase correction may cause ghosting artifact and
signal cancelling. A phase-matching method (Figure 2B) was adopted for alleviating
such artifacts from the phase inconsistent9. To further improve the
performance of paralleling imaging, virtual coils concept is incorporated into
the joint-GRAPPA reconstruction (Figure 2B).
Joint low-rank regularization methods:
The second set
of methods exploit consistency between multi-contrast data using low-rank
regularization following the MUSSELS method10,11. The MUSSELS method was
initially used in multi-shot diffusion weighted imaging to effectively recovery
artifact-free images from under-sampled data by generalizing the SENSE method.
In this method, images are reconstructed as the solution to the following
problem:
$$I_{t}=argmin\sum_t\parallel F_{t}CI_{t}-K_{t}\parallel_2^2+\lambda\parallel H(I_{t})\parallel_{*}$$
where t is the index of TE ,Ft is the
undersampled Fourier operator, C is the coil sensitivity, It is the image-space
data with the tth TE, Kt
is the measured k-space data, and $$$\parallel H(I_{t})\parallel_{*}$$$is structured low-rank constraint. The
virtual-coil based method (VC-MUSSELS) augments the image It with
its complex conjugate, i.e.,$$$\left(\begin{array}{c}I_{t}\\ I_t^*\end{array}\right)$$$, in the low-rank regularization term9,12. The joint MUSSELS (J-MUSSELS) method uses the low-rank
regularization for images at different TEs. The JVC-MUSSELS method uses the
low-rank regularization for images from all three TEs and their complex
conjugate.
Results
Figure 3A shows the diffusion weighted images of b=1000 s/mm2 at
three different TEs from the standard GRAPPA and three generalized methods. Compared
with the standard method, there are some significant ghosting artifacts and signal
canceling in the images from J-GRAPPA method which are caused by inconsistent
phases between measurements at different TEs. After the phase-matching
procedure, the JPM-GRAPPA method successfully removed the ghosting artifact and
improve the image quality. With the integration of the virtual-coil data, the JPMVC‐GRAPPA
method further improved the image quality especially for the long-TE data.
Figure 3B compares the images from standard SENSE, and the three low-rank
regularization-based methods. The virtual-coil based method improved the image
quality, especially at long TE, without using information from other TEs, which
is consistent with results shown in12. Though the J-MUSSELS method
also improves the image quality, it led to undesirable intensity loss at
deep-brain regions, which may be related to sub-optimal regularization
parameters. With the same parameter, the JVC-MUSSELS methods removed the
intensity loss and further improved the image quality.
Figure 4A and 4B compares the FA maps for the proposed methods. The
FA measures from the JPM-GRAPPA and JVC-MUSSELS methods have less noise than
other methods in the corresponding group.Discussion and Conclusion
We proposed a ky-shifted TDM-EPI with complementary k-space
sampling in this study. To improve the images qualities, we performed and
compared several reconstruction methods on the complementary k-space sampling
dataset. The results show that our proposed method with the joint reconstruction
obtained higher image quality, better SNR performance, and lower artifact level
than conventional method.Acknowledgements
This study was
supported in part by NIH grants R21MH116352, R21MH126396,
K01MH117346, R01MH119222, R01MH116173, R01MH125860.References
1. Slator
PJ, Palombo M, Miller KL, Westin CF, Laun F, Kim D, Haldar JP, Benjamini D,
Lemberskiy G, de Almeida Martins JP. Combined diffusion‐relaxometry
microstructure imaging: Current status and future prospects. Magn Reson Med 2021.
2. Kim D, Doyle EK, Wisnowski JL, Kim
JH, Haldar JP. Diffusion‐relaxation correlation spectroscopic
imaging: a multidimensional approach for probing microstructure. Magn Reson Med
2017;78(6):2236-2249.
3. Benjamini D, Basser PJ. Use of
marginal distributions constrained optimization (MADCO) for accelerated 2D MRI
relaxometry and diffusometry. J Magn Reson 2016;271:40-45.
4. Veraart J, Novikov DS, Fieremans E.
TE dependent Diffusion Imaging (TEdDI) distinguishes between compartmental T2
relaxation times. Neuroimage 2018;182:360-369.
5. Gong T, Tong Q, He H, Sun Y, Zhong J,
Zhang H. MTE-NODDI: Multi-TE NODDI for disentangling non-T2-weighted signal
fractions from compartment-specific T2 relaxation times. Neuroimage
2020:116906.
6. Ji Y, Gagoski B, Hoge WS, Rathi Y,
Ning L. Accelerated diffusion and relaxation‐diffusion MRI using time‐division
multiplexing EPI. Magn Reson Med 2021. doi: 10.1002/mrm.28894.
7. Ji Y, Paulsen J, Zhou IY, Lu D,
Machado P, Qiu B, Song YQ, Sun PZ. In vivo microscopic diffusional kurtosis
imaging with symmetrized double diffusion encoding EPI. Magn Reson Med
2019;81(1):533-541.
8. Bilgic B, Kim TH, Liao C, Manhard MK,
Wald LL, Haldar JP, Setsompop K. Improving parallel imaging by jointly
reconstructing multi‐contrast data. Magn Reson Med
2018;80(2):619-632.
9. Liao C, Manhard MK, Bilgic B, Tian Q,
Fan Q, Han S, Wang F, Park DJ, Witzel T, Zhong J. Phase-matched virtual coil
reconstruction for highly accelerated diffusion echo-planar imaging. Neuroimage
2019;194:291-302.
10. Haldar JP. Low-rank modeling of local $
k $-space neighborhoods (LORAKS) for constrained MRI. IEEE Trans Med Imaging
2013;33(3):668-681.
11. 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.
12. Bilgic B, Liao C, Manhard MK, Tian Q,
Chatnuntawech I, Iyer SS, Cauley SF, Feiweier T, Giri S, Hu Y. Robust
high-quality multi-shot EPI with low-rank prior and machine learning. 2019.