[en] Diffusion kurtosis imaging (DKI) is a promising extension of diffusion tensor imaging, giving new insights into the white matter microstructure and providing new biomarkers. Given the rapidly increasing number of studies, DKI has a potential to establish itself as a valuable tool in brain diagnostics. However, to become a routine procedure, DKI still needs to be improved in terms of robustness, reliability, and reproducibility. As it requires acquisitions at higher diffusion31 weightings, results are more affected by noise than in diffusion tensor imaging. The lack of standard procedures for post-processing, especially for noise correction, might become a significant obstacle for the use of DKI in clinical routine limiting its application. We considered two noise correction schemes accounting for the noise properties of multichannel phased-array coils, in order to improve the data quality at signal-to-noise ratio (SNR) typical for DKI. The SNR dependence of estimated DKI metrics such as mean kurtosis (MK), mean diffusivity (MD) and fractional anisotropy (FA) is investigated for these noise correction approaches in Monte Carlo simulations and in in vivo human studies. The intra-subject reproducibility is investigated in a single subject study by varying the SNR level and SNR spatial distribution. Then the impact of the noise correction on inter-subject variability is evaluated in a homogeneous sample of 25 healthy volunteers. Results show a strong impact of noise correction on the MK estimate, while the estimation of FA and MD was affected to a lesser extent. Both intra- and inter-subject SNR
related variability of the MK estimate is considerably reduced after correction for the noise bias, providing more accurate and reproducible measures. In this work, we have proposed a straightforward method that improves accuracy of DKI metrics. This should contribute to standardization of DKI applications in clinical studies and making valuable inferences in group analysis and longitudinal studies.
Disciplines :
Radiology, nuclear medicine & imaging
Author, co-author :
André, Elodie ; Université de Liège - ULiège > Centre de recherches du cyclotron
Grinberg, Farida; Forschungszentrum Juelich GmbH > Institute of Neuroscience and Medicine
Farrher, Ezequiel; Forschungszentrum Juelich GmbH > Institute of Neuroscience and Medicine
Maximov, Ivan I.; Forschungszentrum Juelich GmbH > Institute of Neuroscience and Medicine
Shah, N. Jon; Forschungszentrum Juelich GmbH > Institute of Neuroscience and Medicine
Meyer, Christelle ; Université de Liège - ULiège > Centre de recherches du cyclotron
Jaspar, Mathieu ; Université de Liège - ULiège > Centre de recherches du cyclotron
Muto, Vincenzo ; Université de Liège - ULiège > Centre de recherches du cyclotron
Phillips, Christophe ; Université de Liège - ULiège > Centre de recherches du cyclotron
Balteau, Evelyne ; Université de Liège - ULiège > Centre de recherches du cyclotron
Language :
English
Title :
Influence of noise correction on intra- and inter-subject variability of quantitative metrics in diffusion kurtosis imaging
Publication date :
April 2014
Journal title :
PLoS ONE
eISSN :
1932-6203
Publisher :
Public Library of Science, San Franscisco, United States - California
Le Bihan D, Breton E, Lallemand D, Grenier P, Cabanis E, et al. (1986) MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 161: 401-407. (Pubitemid 17173295)
Basser PJ, Mattiello J, LeBihan D (1994) Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson B 103: 247-254.
Le Bihan D, Johansen-Berg H (2012) Diffusion MRI at 25: exploring brain tissue structure and function. Neuroimage 61: 324-341.
Assaf Y, Cohen Y (1998) Non-mono-exponential attenuation of water and N-acetyl aspartate signals due to diffusion in brain tissue. J Magn Reson 131: 69-85. (Pubitemid 128450537)
Niendorf T, Dijkhuizen RM, Norris DG, van Lookeren Campagne M, Nicolay K (1996) Biexponential diffusion attenuation in various states of brain tissue: implications for diffusion-weighted imaging. Magn Reson Med 36: 847-857. (Pubitemid 26396812)
Mulkern RV, Gudbjartsson H, Westin CF, Zengingonul HP, Gartner W, et al. (1999) Multi-component apparent diffusion coefficients in human brain. NMR Biomed 12: 51-62. (Pubitemid 29135410)
Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed 15: 435-455.
Jensen JH, Helpern JA, Ramani A, Lu H, Kaczynski K (2005) Diffusional kurtosis imaging: the quantification of non-gaussian water diffusion by means of magnetic resonance imaging. Magn Reson Med 53: 1432-1440. (Pubitemid 40734665)
Liu C, Bammer R, Acar B, Moseley ME (2004) Characterizing non-Gaussian diffusion by using generalized diffusion tensors. Magn Reson Med 51: 924-937. (Pubitemid 38580604)
Jensen JH, Helpern JA (2010) MRI quantification of non-Gaussian water diffusion by kurtosis analysis. NMR Biomed 23: 698-710.
Fieremans E, Jensen JH, Helpern JA (2011) White matter characterization with diffusional kurtosis imaging. Neuroimage 58: 177-188.
Fieremans E, Novikov DS, Jensen JH, Helpern JA (2010) Monte Carlo study of a two-compartment exchange model of diffusion. NMR in Biomedicine 23: 711-724.
De Santis S, Assaf Y, Jones DK (2011) Using the biophysical CHARMED model to elucidate the underpinnings of contrast in diffusional kurtosis analysis of diffusion-weighted MRI. Magma 25: 267-276.
Helpern JA, Adisetiyo V, Falangola MF, Hu C, Di Martino A, et al. (2011) Preliminary evidence of altered gray and white matter microstructural development in the frontal lobe of adolescents with attention-deficit hyperactivity disorder: a diffusional kurtosis imaging study. J Magn Reson Imaging 33: 17-23.
Hui ES, Fieremans E, Jensen JH, Tabesh A, Feng W, et al. (2012) Stroke assessment with diffusional kurtosis imaging. Stroke 43: 2968-2973.
Grinberg F, Ciobanu L, Farrher E, Shah NJ (2012) Diffusion kurtosis imaging and log-normal distribution function imaging enhance the visualisation of lesions in animal stroke models. NMR Biomed 25: 1295-1304.
Van Cauter S, Veraart J, Sijbers J, Peeters RR, Himmelreich U, et al. (2012) Gliomas: diffusion kurtosis MR imaging in grading. Radiology 263: 492-501.
Gao Y, Zhang Y, Wong CS, Wu PM, Zhang Z, et al. (2012) Diffusion abnormalities in temporal lobes of children with temporal lobe epilepsy: a preliminary diffusional kurtosis imaging study and comparison with diffusion tensor imaging. NMR Biomed 25: 1369-1377.
Veenith TV, Carter E, Grossac J, Newcombe VF, Outtrim JG, et al. (2013) Inter subject variability and reproducibility of diffusion tensor imaging within and between different imaging sessions. PLoS One 8: e65941.
Müller H-P, Unrath A, Riecker A, Pinkhardt EH, Ludolph AC, et al. (2009) Intersubject variability in the analysis of diffusion tensor images at the group level: fractional anisotropy mapping and fiber tracking techniques. Magnetic Resonance Imaging 27: 324-334.
Kang X, Herron TJ, Turken U, Woods DL (2012) Diffusion properties of cortical and pericortical tissue: regional variations, reliability and methodological issues. Magnetic Resonance Imaging 30: 1111-1122.
Szczepankiewicz F, Latt J, Wirestam R, Leemans A, Sundgren P, et al. (2013) Variability in diffusion kurtosis imaging: Impact on study design, statistical power and interpretation. Neuroimage 76: 145-154.
Latt J, Nilsson M, Wirestam R, Stahlberg F, Karlsson N, et al. (2013) Regional values of diffusional kurtosis estimates in the healthy brain. J Magn Reson Imaging 37: 610-618.
Jones DK, Basser PJ (2004) "Squashing peanuts and smashing pumpkins": how noise distorts diffusion-weighted MR data. Magn Reson Med 52: 979-993. (Pubitemid 39453270)
Koay CG, Ozarslan E, Basser PJ (2009) A signal transformational framework for breaking the noise floor and its applications in MRI. J Magn Reson 197: 108-119.
Kristoffersen A (2012) Estimating non-Gaussian diffusion model parameters in the presence of physiological noise and Rician signal bias. J Magn Reson Imaging 35: 181-189.
Veraart J, Rajan J, Peeters RR, Leemans A, Sunaert S, et al. (2013) Comprehensive framework for accurate diffusion MRI parameter estimation. Magn Reson Med 70: 972-984.
Veraart J, Sijbers J, Sunaert S, Leemans A, Jeurissen B (2013) Weighted linear least squares estimation of diffusion MRI parameters: strengths, limitations, and pitfalls. Neuroimage 81: 335-346.
Veraart J, Van Hecke W, Sijbers J (2011) Constrained maximum likelihood estimation of the diffusion kurtosis tensor using a Rician noise model. Magn Reson Med 66: 678-686.
Henkelman RM (1985) Measurement of signal intensities in the presence of noise in MR images. Med Phys 12: 232-233.
Gudbjartsson H, Patz S (1995) The Rician distribution of noisy MRI data. Magn Reson Med 34: 910-914.
Deshmane A, Gulani V, Griswold MA, Seiberlich N (2012) Parallel MR imaging. J Magn Reson Imaging 36: 55-72.
Dietrich O, Raya JG, Reeder SB, Ingrisch M, Reiser MF, et al. (2008) Influence of multichannel combination, parallel imaging and other reconstruction techniques on MRI noise characteristics. Magn Reson Imaging 26: 754-762.
Constantinides CD, Atalar E, McVeigh ER (1997) Signal-to-noise measurements in magnitude images from NMR phased arrays. Magn Reson Med 38: 852-857. (Pubitemid 27467727)
Maximov I, Farrher E, Grinberg F, Shah NJ (2012) Spatially variable Rician noise in magnetic resonance imaging. Med Image Anal 16: 536-548.
Robson PM, Grant AK, Madhuranthakam AJ, Lattanzi R, Sodickson DK, et al. (2008) Comprehensive quantification of signal-to-noise ratio and g-factor for image-based and k-space-based parallel imaging reconstructions. Magn Reson Med 60: 895-907.
Landman BA, Bazin PL, Smith SA, Prince JL (2009) Robust estimation of spatially variable noise fields. Magn Reson Med 62: 500-509.
Miller AJ, Joseph PM (1993) The use of power images to perform quantitative analysis on low SNR MR images. Magn Reson Imaging 11: 1051-1056.
Manjon JV, Coupe P, Marti-Bonmati L, Collins DL, Robles M (2010) Adaptive non-local means denoising of MR images with spatially varying noise levels. J Magn Reson Imaging 31: 192-203.
Nowak RD (1999) Wavelet-based Rician noise removal for magnetic resonance imaging. IEEE Trans Image Process 8: 1408-1419.
Prah DE, Paulson ES, Nencka AS, Schmainda KM (2010) A simple method for rectified noise floor suppression: Phase-corrected real data reconstruction with application to diffusion-weighted imaging. Magn Reson Med 64: 418-429.
Wirestam R, Bibic A, Latt J, Brockstedt S, Stahlberg F (2006) Denoising of complex MRI data by wavelet-domain filtering: application to high-b-value diffusion-weighted imaging. Magn Reson Med 56: 1114-1120. (Pubitemid 44691354)
Andersson JL (2008) Maximum a posteriori estimation of diffusion tensor parameters using a Rician noise model: why, how and but. Neuroimage 42: 1340-1356.
Aja-Fernandez S, Tristan-Vega A, Alberola-Lopez C (2009) Noise estimation in single- and multiple-coil magnetic resonance data based on statistical models. Magn Reson Imaging 27: 1397-1409.
Lu H, Jensen JH, Ramani A, Helpern JA (2006) Three-dimensional characterization of non-gaussian water diffusion in humans using diffusion kurtosis imaging. NMR Biomed 19: 236-247.
Poot DH, den Dekker AJ, Achten E, Verhoye M, Sijbers J (2010) Optimal experimental design for diffusion kurtosis imaging. IEEE Trans Med Imaging 29: 819-829.
Hansen B, Lund TE, Sangill R, Jespersen SN (2013) Experimentally and computationally fast method for estimation of a mean kurtosis. Magn Reson Med 69: 1754-1760.
Thompson MR, Venkatesan R, Kuppusamy K, Celik A, Lin W, et al. (1999) Increased-contrast, high-spatial-resolution, diffusion-weighted, spin-echo, echo-planar imaging. Radiology 210: 253-259.
Maggioni M, Katkovnik V, Egiazarian K, Foi A (2012) A Nonlocal Transform-Domain Filter for Volumetric Data Denoising and Reconstruction. IEEE Trans Image Process.
Leemans A, Jones DK (2009) The B-matrix must be rotated when correcting for subject motion in DTI data. Magn Reson Med 61: 1336-1349.
Hui ES, Cheung MM, Qi L, Wu EX (2008) Towards better MR characterization of neural tissues using directional diffusion kurtosis analysis. NeuroImage 42: 122-134.
Jenkinson M, Beckmann CF, Behrens TE, Woolrich MW, Smith SM (2012) Fsl. Neuroimage 62: 782-790.
Grinberg F, Farrher E, Kaffanke J, Oros-Peusquens AM, Shah NJ (2011) Non-Gaussian diffusion in human brain tissue at high b-factors as examined by a combined diffusion kurtosis and biexponential diffusion tensor analysis. Neuroimage 57: 1087-1102.
Grossman EJ, Ge Y, Jensen JH, Babb JS, Miles L, et al. (2012) Thalamus and Cognitive Impairment in Mild Traumatic Brain Injury: A Diffusional Kurtosis Imaging Study. J Neurotrauma 29: 2318-2327.
Falangola MF, Jensen JH, Babb JS, Hu C, Castellanos FX, et al. (2008) Age-related non-Gaussian diffusion patterns in the prefrontal brain. J Magn Reson Imaging 28: 1345-1350.
Wang JJ, Lin WY, Lu CS, Weng YH, Ng SH, et al. (2011) Parkinson disease: diagnostic utility of diffusion kurtosis imaging. Radiology 261: 210-217.
Raab P, Hattingen E, Franz K, Zanella FE, Lanfermann H (2010) Cerebral gliomas: diffusional kurtosis imaging analysis of microstructural differences. Radiology 254: 876-881.
Falangola MF, Jensen JH, Tabesh A, Hu C, Deardorff RL, et al. (2013) Non-Gaussian diffusion MRI assessment of brain microstructure in mild cognitive impairment and Alzheimer's disease. Magn Reson Imaging 31: 840-846.
Fieremans E, Benitez A, Jensen JH, Falangola MF, Tabesh A, et al. (2013) Novel white matter tract integrity metrics sensitive to Alzheimer disease progression. AJNR Am J Neuroradiol 34: 2105-2112.
Blockx I, Verhoye M, Van Audekerke J, Bergwerf I, Kane JX, et al. (2012) Identification and characterization of Huntington related pathology: an in vivo DKI imaging study. Neuroimage 63: 653-662.
Hutton C, Balteau E, Lutti A, Josephs O, Weiskopf N (2012) Modelling temporal stability of EPI time series using magnitude images acquired with multi-channel receiver coils. PLoS One 7: e52075.
Aja-Fernandez S, Tristan-Vega A (2012) Influence of noise correlation in multiple-coil statistical models with sum of squares reconstruction. Magn Reson Med 67: 580-585.
Koay CG, Basser PJ (2006) Analytically exact correction scheme for signal extraction from noisy magnitude MR signals. J Magn Reson 179: 317-322.
Maximov, II, Grinberg F, Shah NJ (2011) Robust tensor estimation in diffusion tensor imaging. J Magn Reson 213: 136-144.
Chung S, Courcot B, Sdika M, Moffat K, Rae C, et al. (2010) Bootstrap quantification of cardiac pulsation artifact in DTI. Neuroimage 49: 631-640.
Nunes RG, Jezzard P, Clare S (2005) Investigations on the efficiency of cardiac-gated methods for the acquisition of diffusion-weighted images. J Magn Reson 177: 102-110. (Pubitemid 41336669)