Denoising of diffusion MRI using random matrix theory

Jelle Veraart, Dmitry S Novikov, Daan Christiaens, Benjamin Ades-Aron, Jan Sijbers, Els Fieremans, Jelle Veraart, Dmitry S Novikov, Daan Christiaens, Benjamin Ades-Aron, Jan Sijbers, Els Fieremans

Abstract

We introduce and evaluate a post-processing technique for fast denoising of diffusion-weighted MR images. By exploiting the intrinsic redundancy in diffusion MRI using universal properties of the eigenspectrum of random covariance matrices, we remove noise-only principal components, thereby enabling signal-to-noise ratio enhancements. This yields parameter maps of improved quality for visual, quantitative, and statistical interpretation. By studying statistics of residuals, we demonstrate that the technique suppresses local signal fluctuations that solely originate from thermal noise rather than from other sources such as anatomical detail. Furthermore, we achieve improved precision in the estimation of diffusion parameters and fiber orientations in the human brain without compromising the accuracy and spatial resolution.

Keywords: Accuracy; Marchenko-Pastur distribution; PCA; Precision.

Copyright © 2016 Elsevier Inc. All rights reserved.

Figures

Figure 1
Figure 1
(left) The upper edge λ+ of the Marchenko-Pastur distribution, a universal signature of noise in sample covariance matrices, distinguishes between noise- and significant signal-carrying principal components. (right) Validitiy of Eq. [8] as function of p nullified eigenvalues (color encoding). if p > M̃, suppressed signal leaks into the residuals and, as such, the variability of the residual map, σ̃2, start to deviate from σ2 − ℘σ with σ2 being the noise variance and ℘σ the noise variance accumulated in the p omitted eignvalues. Simulated data (cf. Data) with M = 90 and N = 250 was used to generate the graphs.
Figure 2
Figure 2
The bias [%] in the estimation of the noise-free signal is shown as function of N for different values for M and SNR (top row: SNR=25, bottom row: SNR=50). After Rician correction, the maximal error reduced to ~ 0.01%. The remaining noise standard deviation, normalized by σP^, converges to 1/M (dashed line).
Figure 3
Figure 3
The 95% confidence intervals of the mean error (με, [%]) in the estimation of the noise-free signal for the different diffusion encoding schemes show that MPPCA lacks a significant bias in single- and n-shell protocols. The remaining noise standard deviation, normalized by σ, is significantly higher for the multi-shell protocols if M is kept constant (blue). This observation indicates that more principal components are needed to approximate the diffusion weighted signal as function of the b-value in a linear basis if M is spread across a few shells and, as such, P increases. Nonetheless, MPPCA boosts SNR without compromising the accuracy for all evaluated protocols. Moreover, analyzing multiple shells (M = n × 90; red) simultaneously when the number of directions per shell is fixed improves the performance of MPPCA because the increase in M is generally larger than the associated increase in P.
Figure 4
Figure 4
(top row) A randomly chosen DW image after denoising the simulated whole brain data with M=30, 60, and 90 using MPPCA for SNR=25 and 50. (middle row) The corresponding error maps, computed as the difference between the denoised images, corrected for Rician noise bias, and the noise-free ground truth data, do not show anatomical features. (bottom row) Scatter plots show the noise-free simulated data (S ) against the corresponding noisy data points ( ; red) and against the corresponding denoised and Rician corrected data points ( ; green)
Figure 5
Figure 5
Denoised diffusion-weighted images for different b-values. Although the noise reduction is clearly visible in all denoising techniques, ANLM and TGV introduce image blur and/or reconstruction artifacts.
Figure 6
Figure 6
(left panel) The σ-normalized residual maps between the denoised diffusion-weighted images from Fig. 5 and the original data. (right panel) The presence of anatomical structure in ANLM and TGV anatomical maps indicates interference of the denoising algorithm with the “signal”. The effect becomes more visible after averaging the residual maps of the Mb>0 = 60 images per b value.
Figure 7
Figure 7
The logarithm of the distribution of normalized residuals p(r) as a function of r2 for different b-values, Mb>0, and methods as observed (*) and best fitting normal distribution (solid line). The standard normal distribution is shown for reference (black line). ANLM and TGV clearly over-do the denoising (i.e. standard deviation >1) by interfering with the underlying signal.
Figure 8
Figure 8
k-space energy density as function of the distance to the k-space center. ANLM and TGV have a low-pass filtering effect resulting in spatial resolution loss. MPPCA overshoots the predicted k-space density (black), i.e. Ref = Original - NΩ;σ2. This observation indicated incomplete noise suppression.
Figure 9
Figure 9
Denoised single DW images for different methods and b-values and the corresponding residuals maps for MPPCA.
Figure 10
Figure 10
Effect of denoising on the variability in the estimated MD [μm2/ms] and FA as function of the denoising method and the number of measurements M
Figure 11
Figure 11
Effect of denoising on the bias in the estimation of MD [μm2/ms] and FA. MD and FA maps, derived from a concatenation of the 3 repetitions of all DW data up to b = 1msm2, are shown for reference.
Figure 12
Figure 12
The effect of denoising on the angular precision, probed by a coherence metric κ, and the angular accuracy of the primary and secondary diffusion directions are shown as function of the number of measurements M and the denoising technique.
Figure 13
Figure 13
Effect of denoising on the fiber ODF for a voxel with a three-fiber crossing (crosshair). Studying the three repetitions of the Mb=2.5 = 60 data subsets separately shows that MPPCA consistently improves the estimation of the third peak. Other methods show low coherence of the third direction and often a spurious fourth peak.
Figure 14
Figure 14
Overlay of all tractograms derived from a single repetition of the Mb=2.5 = 60 data subset before and after denoising with the different techniques. Tractography was seeded in the corpus callosum. The cores of the major fiber bundles overlap well (white color). However, changing noise characteristics and possibly signal suppression introduced by ANLM and TGV have very different local and global effects on the tractogram that are often indistinguishable from anatomy (arrows) because of their plausible appearance.

References

    1. Ahmed A, Hu YF, Noras JM. Noise variance estimation for spectrum sensing in cognitive radio networks. AASRI Procedia. 2014;9:37–43.
    1. Aja-Fernández S, Tristán-Vega A, Hoge WS. Statistical noise analysis in GRAPPA using a parametrized noncentral Chi approximation model. Magnetic Resonance in Medicine. 2011;65(4):1195–1206.
    1. Basser PJ, Mattiello J, LeBihan D. MR diffusion tensor spectroscopy and imaging. Biophysical journal. 1994;66(1):259–267.
    1. Basser PJ, Pajevic S. Statistical artifacts in diffusion tensor MRI (DT-MRI) caused by background noise. Magnetic Resonance in Medicine. 2000;44(1):41–50.
    1. Blackledge MD, Leach MO, Collins DJ, Koh DM. Computed diffusion-weighted mr imaging may improve tumor detection. Radiology. 2011;261(2):573–581.
    1. Block KT, Uecker M, Frahm J. Suppression of MRI truncation artifacts using total variation constrained data extrapolation. International journal of biomedical imaging 2008
    1. Buades A, Coll B, Morel J-M. A non-local algorithm for image denoising. Computer Vision and Pattern Recognition. IEEE Computer Society Conference on; IEEE; 2005. pp. 60–65.
    1. Chang LC, Jones DK, Pierpaoli C. RESTORE: robust estimation of tensors by outlier rejection. Magnetic Resonance in Medicine. 2005;53(5):1088–1095.
    1. Coupé P, Yger P, Barillot C. Medical Image Computing and Computer-Assisted Intervention–MICCAI 2006. Springer; 2006. Fast non local means denoising for 3D MR images; pp. 33–40.
    1. Deledalle C-A, Salmon J, Dalalyan AS, et al. Image denoising with patch based PCA: local versus global. BMVC. 2011:1–10.
    1. Dhollander T, Veraart J, Van Hecke W, Maes F, Sunaert S, Sijbers J, Suetens P. Medical Image Computing and Computer-Assisted Intervention–MICCAI 2011. Springer; 2011. Feasibility and advantages of diffusion weighted imaging atlas construction in q-space; pp. 166–173.
    1. Ding Y, Chung YC, Simonetti OP. A method to assess spatially variant noise in dynamic MR image series. Magnetic Resonance in Medicine. 2010;63(3):782–789.
    1. Efron B. Bootstrap methods: another look at the jackknife. Springer; 1992.
    1. Foi A. Noise estimation and removal in mr imaging: The variance-stabilization approach. Biomedical Imaging: From Nano to Macro, 2011 IEEE International Symposium on; IEEE; 2011. pp. 1809–1814.
    1. Glasser MF, Sotiropoulos SN, Wilson JA, Coalson TS, Fischl B, Andersson JL, Xu J, Jbabdi S, Webster M, Polimeni JR, et al. The minimal preprocessing pipelines for the Human Connectome Project. Neuroimage. 2013;80:105–124.
    1. Gudbjartsson H, Patz S. The Rician distribution of noisy MRI data. Magnetic Resonance in Medicine. 1995;34(6):910–914.
    1. Hansen B, Lund TE, Sangill R, Jespersen SN. Experimentally and computationally fast method for estimation of a mean kurtosis. Magnetic resonance in medicine. 2013;69(6):1754–1760.
    1. Hansen B, Lund TE, Sangill R, Stubbe E, Finsterbusch J, Jespersen SN. Experimental considerations for fast kurtosis imaging. Magnetic resonance in medicine 2015
    1. Hotelling H. Analysis of a complex of statistical variables into principal components. Journal of educational psychology. 1933;24(6):417.
    1. Jahani J, Johnson G, Kiselev VG, Novikov DS. Random matrix theory-based noise reduction for dynamic imaging: Application to DCE-MRI. Proceedings 21th Scientific Meeting, International Society for Magnetic Resonance in Medicine; Salt Lake City, USA. 2013. p. 3073.
    1. Jelescu IO, Veraart J, Fieremans E, Novikov DS. Degeneracy in model parameter estimation for multi-compartmental diffusion in neuronal tissue. NMR in Biomedicine. 2016;29(1):33–47.
    1. Jeurissen B, Leemans A, Jones DK, Tournier JD, Sijbers J. Probabilistic fiber tracking using the residual bootstrap with constrained spherical deconvolution. Human brain mapping. 2011;32(3):461–479.
    1. Jeurissen B, Leemans A, Tournier JD, Jones DK, Sijbers J. Investigating the prevalence of complex fiber configurations in white matter tissue with diffusion magnetic resonance imaging. Human brain mapping. 2013;34(11):2747–2766.
    1. Johnson JB. Thermal agitation of electricity in conductors. Physical review. 1928;32(1):97.
    1. Johnstone IM. High dimensional statistical inference and random matrices. 2006 arXiv preprint math/0611589.
    1. Jones D, Horsfield M, Simmons A. Optimal strategies for measuring diffusion in anisotropic systems by magnetic resonance imaging. Magnetic Resonance in Medicine. 1999:42.
    1. Jones DK. Determining and visualizing uncertainty in estimates of fiber orientation from diffusion tensor MRI. Magnetic Resonance in Medicine. 2003;49(1):7–12.
    1. Jones DK. Diffusion MRI: Theory, methods, and applications. Oxford University Press; 2010a.
    1. Jones DK. Precision and accuracy in diffusion tensor magnetic resonance imaging. Topics in Magnetic Resonance Imaging. 2010b;21(2):87–99.
    1. Jones DK, Basser PJ. “Squashing peanuts and smashing pumpkins”: How noise distorts diffusion-weighted MR data. Magnetic Resonance in Medicine. 2004;52(5):979–993.
    1. Keil B, Blau JN, Biber S, Hoecht P, Tountcheva V, Setsompop K, Triantafyllou C, Wald LL. A 64-channel 3T array coil for accelerated brain MRI. Magnetic Resonance in Medicine. 2013;70(1):248–258.
    1. Kellner E, Dhital B, Kiselev VG, Reisert M. Gibbs-ringing artifact removal based on local subvoxel-shifts. Magnetic Resonance in Medicine. 2015 doi: 10.1002/mrm.26054.
    1. Knoll F, Bredies K, Pock T, Stollberger R. Second order total generalized variation (TGV) for MRI. Magnetic Resonance in Medicine. 2011;65(2):480–491.
    1. Koay CG, Basser PJ. Analytically exact correction scheme for signal extraction from noisy magnitude MR signals. Journal of Magnetic Resonance. 2006;179(2):317–322.
    1. Laloux L, Cizeau P, Bouchaud JP, Potters M. Noise dressing of financial correlation matrices. Physical review letters. 1999;83(7):1467.
    1. Manjón JV, Carbonell-Caballero J, Lull JJ, García-Martí G, Martí-Bonmatí L, Robles M. MRI denoising using non-local means. Medical image analysis. 2008;12(4):514–523.
    1. Manjón JV, Coupé P, Buades A. MRI noise estimation and denoising using non-local PCA. Medical image analysis. 2015;22(1):35–47.
    1. Manjón JV, Coupé P, Concha L, Buades A, Collins DL, Robles M. Diffusion weighted image denoising using overcomplete local PCA. PloS one. 2013;8(9):e73021.
    1. Manjón JV, Coupé P, Martí-Bonmatí L, Collins DL, Robles M. Adaptive non-local means denoising of MR images with spatially varying noise levels. Journal of Magnetic Resonance Imaging. 2010;31(1):192–203.
    1. Marchenko VA, Pastur LA. Distribution of eigenvalues for some sets of random matrices. Matematicheskii Sbornik. 1967;114(4):507–536.
    1. Nyquist H. Thermal agitation of electric charge in conductors. Physical review. 1928;32(1):110.
    1. Orchard J, Ebrahimi M, Wong A. Efficient nonlocal-means denoising using the SVD. Image Processing, 2008. ICIP 2008. 15th IEEE International Conference on; IEEE; 2008. pp. 1732–1735.
    1. Perrone D, Aelterman J, Pižurica A, Jeurissen B, Philips W, Leemans A. The effect of Gibbs ringing artifacts on measures derived from diffusion MRI. NeuroImage. 2015;120:441–455.
    1. Poot DHJ, den Dekker AJ, Achten E, Verhoye M, Sijbers J. Optimal experimental design for diffusion kurtosis imaging. Medical Imaging, IEEE Transactions on. 2010;29(3):819–829.
    1. Rajan J, Jeurissen B, Verhoye M, Van Audekerke J, Sijbers J. Maximum likelihood estimation-based denoising of magnetic resonance images using restricted local neighborhoods. Physics in Medicine and biology. 2011;56(16):5221.
    1. Rajan J, Veraart J, Van Audekerke J, Verhoye M, Sijbers J. Nonlocal maximum likelihood estimation method for denoising multiplecoil magnetic resonance images. Magnetic Resonance imaging. 2012;30(10):1512–1518.
    1. Rudin LI, Osher S, Fatemi E. Nonlinear total variation based noise removal algorithms. Physica D: Nonlinear Phenomena. 1992;60(1):259–268.
    1. Sengupta AM, Mitra PP. Distributions of singular values for some random matrices. Physical Review E. 1999;60(3):3389.
    1. Setsompop K, Kimmlingen R, Eberlein E, Witzel T, Cohen-Adad J, McNab JA, Keil B, Tisdall MD, Hoecht P, Dietz P, et al. Pushing the limits of in vivo diffusion MRI for the Human Connectome Project. Neuroimage. 2013;80:220–233.
    1. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, et al. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage. 2004;23:S208–S219.
    1. Sotiropoulos SN, Jbabdi S, Xu J, et al. Advances in diffusion MRI acquisition and processing in the Human Connectome Project. Neuroimage. 2013;80:125–143.
    1. Tax CM, Jeurissen B, Vos SB, Viergever MA, Leemans A. Recursive calibration of the fiber response function for spherical deconvolution of diffusion mri data. Neuroimage. 2014;86:67–80.
    1. Tournier J, Calamante F, Connelly A, et al. MRtrix: diffusion tractography in crossing fiber regions. International Journal of Imaging Systems and Technology. 2012;22(1):53–66.
    1. Tournier JD, Calamante F, Connelly A. Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution. NeuroImage. 2007;35(4):1459–1472.
    1. Veraart J, Fieremans E, Jelescu IO, Knoll F, Novikov DS. Gibbs ringing in diffusion MRI. Magnetic Resonance in Medicine. 2015 doi: 10.1002/mrm.25866.
    1. Veraart J, Fieremans E, Novikov DS. Diffusion MRI noise mapping using random matrix theory. Magnetic Resonance in Medicine. 2016 doi: 10.1002/mrm.26059.
    1. Veraart J, Poot DHJ, Van Hecke W, Blockx I, Van der Linden A, Verhoye M, Sijbers J. More accurate estimation of diffusion tensor parameters using diffusion kurtosis imaging. Magnetic Resonance in Medicine. 2011a;65(1):138–145. URL .
    1. Veraart J, Rajan J, Peeters RR, Leemans A, Sunaert S, Sijbers J. Comprehensive framework for accurate diffusion MRI parameter estimation. Magnetic Resonance in Medicine. 2013a;70(4):972–984. URL .
    1. Veraart J, Sijbers J, Sunaert S, Leemans A, Jeurissen B. Weighted linear least squares estimation of diffusion MRI parameters: strengths, limitations, and pitfalls. NeuroImage. 2013b;81:335–346.
    1. Veraart J, Van Hecke W, Sijbers J. Constrained maximum likelihood estimation of the diffusion kurtosis tensor using a Rician noise model. Magnetic Resonance in Medicine. 2011b;66(3):678–686. URL .

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