Jenny Chen1, Benjamin Ades-aron1, Hong-Hsi Lee2, Durga Kullakanda1, Saurabh Maithani1, Dmitry S. Novikov1, Jelle Veraart1, and Els Fieremans1
1Department of Radiology, NYU School of Medicine, New York, NY, United States, 2Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Boston, MA, United States
Synopsis
Diffusion
MRI (dMRI) is affected by noise and by artifacts such as Gibbs ringing and distortions.
Using software phantoms as ground-truth, this study compares diffusion tensor
imaging (DTI) and diffusional kurtosis imaging (DKI) parameter estimates to
assess accuracy of various denoising and Gibbs removal methods, two key
components of dMRI pipelines. An optimized Diffusion parameter EStImation with
Gibbs and NoisE Removal (DESIGNER) pipeline is proposed, with non-local patch
MP-PCA denoising and Removal of Partial-fourier induced Gibbs Ringing (RPG),
that yields more accurate metrics, fewer outlier voxels in phantoms and more
robust DTI/DKI maps in patient data.
Introduction
dMRI
are corrupted by the effect of thermal noise and various imaging artifacts such
as Gibbs ringing and distortions. To improve reproducibility and data fidelity,
various dMRI pre-processing pipelines [1,2,3,4,5] are proposed that differ in
artifacts they choose to address and/or the algorithmic methods, which
potentially may lead to conflicting findings in clinical dMRI studies [6,7]. Here,
we introduce DESIGNER 2.0 (Dv2), based on previously validated DESIGNER
[1] pipeline, that additionally (1) corrects for Gibbs ringing due to partial
Fourier (PF) acquisitions, which is common in clinical (research) settings,
and (2) removes noise more effectively. We systematically evaluate accuracy and
precision of these new steps using in-vivo dMRI and phantoms for ground-truth
comparison. Methods
We evaluated the accuracy and precision of Dv2 by comparing to (i) a minimal
preprocessing pipeline (1; HCP) and (ii) the original implementation of
DESIGNER (Dv1) using clinical data and simulation.
DESIGNER 2.0 is a revision of Dv1
that integrates the latest denoise and Gibbs removal development: (a) MP-PCA
nonlocal-patch denoising, which selects similar voxels within a local-patch to
reconstruct denoised voxel signals, with eigenvalue shrinkage [8] and (b) Removal
of Partial-fourier induced Gibbs Ringing (RPG) [9].
Clinical Data: dMRI
data (5 b=0 images AP, 1 b=0 image PA for distortion correction [10,11], b=250
s/mm2 – 4 directions, b=1000 s/mm2 – 20 directions,
b=2000 s/mm2 – 60 directions, TE=70ms, TR=3.7s, 50 slices,
resolution=1.7x1.7x3mm3, 6/8 PF) was retrospectively analyzed of a
47-year-old female who underwent MRI on a Magnetom Prisma 3T.
Simulation I: An HCP
phantom [2] was modified by generating B0 and DKI tensor (weighted linear least
square (WLLS) fit [12]) using the diffusion vectors matching the dMRI protocol
above, and adjusting the resolution (72 slices, resolution=2.5x2.5x2.5mm3).
Then, 50 sets of noisy phantoms with SNR ranging from 10 to 100 were created by
adding Rician noise. Each noisy phantom was processed with HCP (no denoising),
local denoising [13,14] (Dv1), or non-local denoising with eigenvalue shrinkage
(Dv2), as well as pre-processed with only Rician correction [15], local
denoising with eigenvalue shrinkage, and non-local denoising without eigenvalue
shrinkage.
Simulation
II: HCP
data is acquired with PF on, hence the HCP phantom cannot evaluate PF-induced Gibbs
removal methods. Instead, Gibbs ringing was introduced by k-space truncation
and PF 6/8 in the horizontal direction using the Shepp-Logan phantom. The Gibbs
phantom was either not corrected (HCP), corrected with Subvoxel-shifts (SuShi)
method [16] (Dv1), or with RPG degibbs (Dv2). Additionally, the subject's MRI
was processed with SuShi method and RPG degibbs (along with eddy and EPI
correction) to see effect of degibbs on realistic anatomical structures.
Experiments: DTI (MD – mean diffusivity, RD – radial
diffusivity, AD – axial diffusivity, and FA – fractional anisotropy) and DKI
(MK – mean kurtosis, RK – radial kurtosis, AK – axial kurtosis) parameter maps
were estimated using WLLS fitting. For the phantoms, percent error or median
percentage error (MdPE) over median of 50 noise iterations were calculated against their
respective ground truth DTI/DKI maps. Average outlier percentage were computed
to quantify amount of “black voxels” remaining after denoising, where outliers
are defined as D, K<0 or FA>1. JHU white matter (WM) atlas labels [17] were
warped to the ground truth FA map and combined to form an overall WM region of
interest (ROI). Then, median value in the WM ROI was extracted from DTI/DKI MdPE
maps. For Gibbs phantom, mean percent error (MPE) was taken over manually
drawn ROIs. Results
Figure
2 plots the DTI/DKI MdPE of noisy HCP phantoms pre-processed with varying
denoise methods. Not denoising or Rician bias correcting alone result in the
highest bias, while nonlocal-patch denoising was most accurate.
Interestingly, while eigenvalue shrinkage causes bias, it results in fewest
outliers. Visual comparison of the maps (Figure 3) shows eigenvalue shrinkage
and nonlocal-patch maps are noticeably less noisy and with more "black voxels" removed. Figure 4a shows DTI/DKI-parameters in Gibbs phantom are least
accurate without any Gibbs correction and most accurate with RPG degibbs. Although SuShi
method removes some Gibbs ringing, RPG additionally removes Gibbs ringing due
to PF [9,16] (Figure 4b). PF-induced Gibbs ringing can also be seen in the subject’s (Figure 5) as a dark (MD) or bright (FA) band and black
voxels (MK) at the CC/CSF boundary (Figure 5). These artifacts are reduced the most
in maps with RPG while Dv2 results in least noisy maps and the fewest outliers.Discussion and Conclusion
Our
results suggest nonlocal denoising and RPG degibbs can improve
accuracy and precision, yielding more robust DTI/DKI maps. Of the denoising
methods, nonlocal-patch denoising outperforms local-patch denoising with the
lowest MdPE. Although eigenvalue shrinkage causes some bias in estimations, it also
removes the most outliers and gives the least noisy parametric maps, making it
the preferred method for voxel-based analysis. To correct for Gibbs ringing in
PF 6/8 datasets, RPG gives the smallest MPE and cleaner maps.
As
expected from the phantom results, comparing the three pipelines on subject data (Figure 5), Dv2, which involves RPG and nonlocal-patch denoising with eigenvalue
shrinkage, performed best, as the parametric maps show the least outlier and noise. Future
work will optimize estimation methods [12,18] to target remaining "black voxels" in kurtosis maps.Acknowledgements
Research was supported by the National Institute of Neurological Disorders and Stroke of the NIH under awards R01 NS088040 and R01 EB027075, and by the Hirschl foundation and was performed at the Center of Advanced Imaging Innovation and Research (CAI2R, www.cai2r.net), a Biomedical Technology Research Center supported by NIBIB with the award P41 EB017183.
References
- Glasser MF, Sotiropoulos SN, Wilson JA, Coalson
TS, Fischl B, Andersson JL, Xu J, Jbabdi S, Webster M, Polimeni JR, Van Essen
DC, Jenkinson M; WU-Minn HCP Consortium. The minimal preprocessing pipelines
for the Human Connectome Project. Neuroimage. 2013 Oct 15;80:105-24. doi:
10.1016/j.neuroimage.2013.04.127. Epub 2013 May 11. PMID: 23668970; PMCID:
PMC3720813.
- Ades-Aron, B., Veraart, J., Kochunov, P.,
McGuire, S., Sherman, P., Kellner, E., Novikov, D. S., & Fieremans, E.
(2018). Evaluation of the accuracy and precision of the diffusion parameter
EStImation with Gibbs and NoisE removal pipeline. NeuroImage, 183, 532–543. https://doi.org/10.1016/j.neuroimage.2018.07.066
- Pierpaoli C, Irfanoglu
LW,MO, Barnett A, Basser P, Chang L-C, Koay C, Pajevic S, Rohde G, Sarlls J,
and Wu M, 2010. TORTOISE: an integrated software package for processing of
diffusion MRI data ISMRM, Stockholm, Sweden.
- Cieslak, M.,
Cook, P.A., He, X. et al. QSIPrep: an integrative platform for preprocessing
and reconstructing diffusion MRI data. Nat Methods 18, 775–778 (2021). https://doi.org/10.1038/s41592-021-01185-5
- Maximov, II,
Alnæs, D, Westlye, LT. Towards an optimised processing pipeline for diffusion
magnetic resonance imaging data: Effects of artefact corrections on diffusion
metrics and their age associations in UK Biobank. Hum Brain Mapp. 2019; 40:
4146– 4162. https://doi.org/10.1002/hbm.24691
- Chen J,
Ades-aron B, et al., The effect of image pre-processing pipelines on age
associations of diffusion and kurtosis in white matter, International Society
for Magnetic Resonance in Medicine, 2021, Digital Poster (presentation May
2021)
- Z. Lu, W.
Huang and C. Guan, "A comparison of DTI pre-processing tools on a dataset
of chronic subcortical stroke rehabilitation patients," 2017 8th
International IEEE/EMBS Conference on Neural Engineering (NER), 2017, pp.
568-571, doi: 10.1109/NER.2017.8008415.
- M. Gavish and
D. L. Donoho, "Optimal Shrinkage of Singular Values," in IEEE
Transactions on Information Theory, vol. 63, no. 4, pp. 2137-2152, April 2017,
doi: 10.1109/TIT.2017.2653801.
- Lee HH,
Novikov DS, Fieremans E. Removal of partial Fourier-induced Gibbs (RPG) ringing
artifacts in MRI. Magn Reson Med. 2021 Nov;86(5):2733-2750. doi:
10.1002/mrm.28830. Epub 2021 Jul 5. PMID: 34227142.
- J.L.R. Andersson, S. Skare, J. Ashburner. How to
correct susceptibility distortions in spin-echo echo-planar images: application
to diffusion tensor imaging. NeuroImage, 20(2):870-888, 2003.
- S.M. Smith, M. Jenkinson, M.W. Woolrich, C.F.
Beckmann, T.E.J. Behrens, H. Johansen-Berg, P.R. Bannister, M. De Luca, I.
Drobnjak, D.E. Flitney, R. Niazy, J. Saunders, J. Vickers, Y. Zhang, N. De
Stefano, J.M. Brady, and P.M. Matthews. Advances in functional and structural
MR image analysis and implementation as FSL. NeuroImage, 23(S1):208-219, 2004.
- J. Veraart, J. Sijbers, S. Sunaert, A. Leemans,
B. Jeurissen, Weighted linear least squares estimation of diffusion MRI
parameters: strengths, limitations, and pitfalls. NeuroImage 81, 335-346
(2013).
- Cordero-Grande,
L.; Christiaens, D.; Hutter, J.; Price, A.N.; Hajnal, J.V. Complex
diffusion-weighted image estimation via matrix recovery under general noise
models. NeuroImage, 2019, 200, 391-404, doi: 10.1016/j.neuroimage.2019.06.039
4.
- Veraart, J.,
Novikov, D. S., Christiaens, D., Ades-Aron, B., Sijbers, J., & Fieremans,
E. (2016). Denoising of diffusion MRI using random matrix theory. NeuroImage,
142, 394–406. https://doi.org/10.1016/j.neuroimage.2016.08.016
5.
- Koay CG, Basser PJ, 2006. Analytically exact
correction scheme for signal extraction from noisy magnitude MR signals.
Journal of Magnetic Resonance 179, 317–322.
- Kellner E,
Dhital B, Kiselev VG, Reisert M. Gibbs-ringing artifact removal based on local
subvoxel-shifts. Magn Reson Med. 2016 Nov;76(5):1574-1581. doi:
10.1002/mrm.26054. Epub 2015 Nov 24. PMID: 26745823.
- Hua et al.,
Tract probability maps in stereotaxic spaces: analysis of white matter anatomy
and tract-specific quantification. NeuroImage, 39(1):336-347 (2008)
-
Henriques RN, Jespersen SN,
Jones DK, Veraart J. Toward more robust and reproducible diffusion kurtosis
imaging. Magn Reson Med. 2021 Sep;86(3):1600-1613. doi: 10.1002/mrm.28730. Epub
2021 Apr 8. PMID: 33829542; PMCID: PMC8199974.