Noam Omer1, Neta Stern1, Tamar Blumenfeld-Katzir1, Chen Solomon1, Meirav Galun2, and Noam Ben-Eliezer1,3,4
1Biomedical Engineering, Tel Aviv University, Tel Aviv, Israel, 2Department of Computer Science and Applied Mathematics, Weizmann Institute of Science, Rehovot, Israel, 3Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel, 4Center for Advanced Imaging Innovation and Research (CAI2R), New-York University Langone Medical Center, New York, NY, United States
Synopsis
The common approach to myelin mapping relies on multi-T2
component (mcT2) analysis, where the signal from a single
voxel is separated into its underlying distribution of T2 values. This
approach is highly challenging due to the ill posedness of
extracting multiple free parameters from a single voxel data.
We present a new data-driven
paradigm, where the white matter is first analyzed to identify a finite set of multi-T2
distributions, which are then used to locally analyze the signal in each
voxel. Application on white matter tissue produced improved myelin quantifications, without a priory fixing the number of sub-voxel compartments.
Introduction
Multicomponent analysis of T2 values (mcT2) allows
probing sub-voxel information on microscopic water environments by assessing their
relative fraction and T2 relaxation times (T2). Typically,
mcT2 is applied to white matter (WM) tissue for
estimating the relative fraction of water that reside between the myelin sheaths1.
The ensuing myelin water fraction (MWF) correlates with myelin content2 and therefore used as a biomarker for studying neurodegenerative
diseases3-6. This analysis is based on separating the multi-echo spin-echo
(MESE) signal in each voxel into a distribution of T2 values7.
The MWF is then calculated as the relative energy between 10-40 ms, having
relatively short T2 compared to intra/extra-cellular water (40-200 ms)2 ($$$\scriptsize\color{blue} {Figure 1}$$$).
Conventional mcT2 fitting
procedures apply the regularized non-negative
least squares (rNNLS) algorithm8 and consider the voxel signal Svoxel as
a weighted combination of
multiple single-T2 signals:
$$S_{voxel}=\sum_{m=1}^{nT_{2}}w_{m}S_{m}^{T_{2}}$$
where $$$nT_2$$$ is the
number of single-T2 signals $$$S_{m}^{T_{2}}$$$ and $$$w_{m}$$$ is the weight of
the single-T2 signal. This mcT2 fitting task involves matrix
inversion which is ill-conditioned, and highly sensitive to noise and to the
choice of regularization weights7,9,-10, resulting in grainy MWF maps indicating
zero values in myelinated voxel at clinical signal-to-noise ratios (SNR)11.
Recently, a new data-driven paradigm
for mcT2 analysis12 was suggested as a reliable alternative approach13-14. This approach suggests applying a
pre-processing step, which first identifies a set of multicomponent combinations of single-T2
signals (i.e. mcT2 motifs) which best describe the WM segment
being analyzed, and using these as basis set, describing the signal at each
voxel:
$$S_{voxel}=\sum_{m=1}^{L}\omega_{m}S_{m}^{mcT_{2}}$$
where $$$\omega_{m}$$$ is the weight of
the mth mcT2
motif $$$S_{m}^{mcT_{2}}$$$.
In this study we demonstrate how
the adoption of this data-driven paradigm, prior to applying the conventional rNNLS
fitting, improves the quantification of MWF. To that end, we compare between MWF
maps that were obtained with and without the data-driven preprocessing step. Validations
are shown on a numerical phantom at varying SNR levels, and on human brain
data.Methods
Data-driven identification of mcT2 motifs
The data-driven algorithm was applied on the entire WM, using a
mask generated by FreeSurfer15 (eroded by one pixel). The algorithm was initialized
with a large dictionary containing
over than 3 million simulated mcT2 motifs14, covering the
physiological range of WM tissue parameters. All mcT2 motifs were
generated from a set of 64 single-T2 values logaritmic-spaced between 1-800 ms and weighted by fractions between 0...1 in jumps of 0.05. The
data-driven step identified a set of L=30 mcT2 motifs that were used as basis signal components for the
inversion.
MWF quantification was done using an in-house implementation
of the conventional rNNLS algorithm7,16 added with second-order
Tikhonov regularization weighted by λtik=0.01.
Conventional versus data-driven MWF mapping
Numerical validations: five
mcT2 motifs, modeling different WM microenvironments
with 1-3 sub-voxel compartments, were simulated for a range of MWFs 0-20% (T2=10-40
ms) and intra/extra-cellular water fractions of 80-100% (T2=50-80
ms) ($$$\scriptsize\color{blue} {Figure 2}$$$). Conventional rNNLS was applied on
the simulated data twice – with and without the data-drive-step. To test the accuracy of both approaches white Gaussian noise was
added at varying SNR levels: 60, 40 and 25. The natural variability of T2
values was also modeled by perturbing their values in a range of ±20% from the baseline
T2 values. Finally, MWF were
quantified per voxel by summing the area under the peak in the short T2
range (10-40 ms)2 and error
maps were calculated as the absolute difference between each map and the ground
truth MWF map.
In
vivo MWF quantification: a volunteer brain scan was performed on a 3 Tesla whole-body
MRI scanner (Prisma, Siemens Healthineers) using a 20-channel head coil. Experimental
parameters were: FOV=200x210 cm, matrix size=216x180, Naverages=1, TR=3000 ms, TE={10, 20, ..., 200}, slice thickness=3 mm, acquisition-bandwidth=210 Hz/Px, GRAPPA factor=2. Conventional
rNNLS was applied on the data twice – with, and without the data-drive-step and MWF maps were produced from both approaches.Results
($$$\scriptsize\color{blue} {Figure 3}$$$) presents
maps of the MWF and
relative error for the numerical simulation at varying SNR levels. At
SNR = 60 the data-driven approach showed perfect reconstruction while the conventional
approach underestimated the lesioned voxels and the myelin water pool in the
three-compartment tissue. At SNR=40 both methods underestimated the two-compartment tissue and
misidentified the myelin water pool in one of the three-compartment tissue. At
SNR=25 both methods presented incorrect reconstruction.
($$$\scriptsize\color{blue} {Figure 4}$$$) compares maps that were obtained with and without
the data-driven step for in vivo brain data. Both maps show MWF values which coincide with values reported in the literature (0-25%)17. The
data-driven approached produced a smoother MWF pattern compared to the map
obtained with conventional approach, which exhibits a significant number of
voxels where the fitting process failed to identify any myelin.Discussion & Conclusions
This study demonstrates the
contribution of adopting a data-driven approach for conventional mcT2
analysis. mcT2 analysis involves fitting at least five free parameters to a three-compartment sub-voxel configuration [$$$\scriptsize{T_{2}^{C1}}$$$,
$$$\scriptsize{T_{2}^{C2}}$$$, $$$\scriptsize{T_{2}^{C3}}$$$, $$$\scriptsize{f^{C1}}$$$, $$$\scriptsize{f^{C2}}$$$, $$$\scriptsize{f^{C3}=1-f^{C2}-f^{C1}}$$$]. where $$$\scriptsize{T_{2}^{Ci}}$$$ denotes the
relative fractions of compartment $$$\scriptsize{Ci}$$$.The statistical power of this key pre-processing stage endows the mcT2 data-driven analysis with additional robustness which stabilizes the rNNLS algorithm and overcomes the ambiguity in the T2-space.Acknowledgements
ISF Grant 2009/17References
1. Mackay A, Whittall K, Adler J, et al. In vivo visualization of myelin
water in brain by magnetic resonance. Magn. Reson. Med. 1994;31:673–677.
2. Alonso-Ortiz E, Levesque I, Pike B. MRI-based myelin water imaging: A
technical review. Magn. Reson. Med. 2015;73(1):70–81.
3. Zhang J, Kolind, H, Laule C, MacKay A. Comparison of myelin water
fraction from multiecho T2 decay curve and steady-state methods. Magn. Reson.
Med. 2015;73(1):223–32.
4. McCreary CR. Bjarnason T, Skihar V, et al. Multiexponential T2 and
magnetization transfer MRI of demyelination and remyelination in murine spinal
cord. Neuroimage. 2009;45:1173–1182.
5. Harald M, Bossoni L, Connor J, et al. Iron, Myelin, and the Brain:
Neuroimaging Meets Neurobiology. Trends Neurosci. 2019;42:384–401.
6. Heath F, Hurley S, Johansen-Berg H, Sampaio-Baptista C. Advances in
noninvasive myelin imaging. Dev. Neurobiol. 2018;78:136–151.
7. Whittall K, MacKay A. Quantitative interpretation of NMR relaxation
data. J. Magn. Reson. 1989;84:134–152.
8. MacKay A, Whittall K, Adler J, et al. In vivo
visualization of myelin water in brain by magnetic resonance. Magn. Reson. Med.
1994;31(6):673–677.
9. Graham S, Stanchev P, Bronskill M. Criteria for analysis of
multicomponent tissue T2 relaxation data. Magn. Reson. Med. 1996;35(3):370–378.
10. Laule C, Vavasour I, Moore G, et al. Water content and myelin water
fraction in multiple sclerosis: A T2 relaxation study. J. Neurol. 2004(3);251:284–293.
11. Raj A, Pandya S, Shen X, et al. Multi-Compartment T2 Relaxometry Using
a Spatially Constrained Multi-Gaussian Model. PLoS One 2014;9(6):e98391.
doi: 10.1371/journal.pone.0098391
12 Omer N, Stern N, Ben-Eliezer N, et at. A novel multicomponent T analysis
for identification of sub-voxel compartments and quantification of myelin water
fraction. In Proceedings of the 28th Annual Meeting of ISMRM, Sydney, Australia,
2020. Abstract 6109.
13 Omer N, Stern N, Ben-Eliezer N, et at. Data driven algorithm for
multicomponent T2 analysis based on identification of spatially global sub-voxel
features. In Proceedings of the 29th Annual Meeting of ISMRM, Virtual
Conference, 2021.Abstract 3301.
14 Omer N, Stern N, Ben-Eliezer N, et at. In vivo validation of a data
driven algorithm for multicomponent T2 mapping on a mice model of
demyelination. In Proceedings of the 29th Annual Meeting of ISMRM, Virtual
Conference, 2021.Abstract 4064.
15. Fischl B, Salat D, Busa E, et al. Whole brain segmentation: automated
labeling of neuroanatomical structures in the human brain. Neuron. 2002;33(3):341–355.
16. Provencher W. A constrained regularization method for inverting data
represented by linear algebraic or integral equations. Comput. Phys. Commun. 1982;27(3):213–227.
17. Deoni S. Quantitative relaxometry of the brain. Top. Magn. Reson.
Imaging 2010;21(2) 101–13.