Quanti fi cation of microscopic diffusion anisotropy disentangles effects of orientation dispersion from microstructure : Applications in healthy volunteers and in brain tumors

(2015). Quantification of microscopic diffusion anisotropy disentangles effects of orientation dispersion from microstructure: Applications in healthy volunteers and in brain tumors. NeuroImage, 104, 241-252. General rights Copyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights. • Users may download and print one copy of any publication from the public portal for the purpose of private study or research. • You may not further distribute the material or use it for any profit-making activity or commercial gain • You may freely distribute the URL identifying the publication in the public portal ? Take down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. a b s t r a c t a r t i c l e i n f o Keywords: Diffusion weighted imaging Microscopic anisotropy Microscopic fractional anisotropy Order parameter Magic angle spinning of the q-vector The anisotropy of water diffusion in brain tissue is affected by both disease and development. This change can be detected using diffusion MRI and is often quantified by the fractional anisotropy (FA) derived from diffusion ten-sor imaging (DTI). Although FA is sensitive to anisotropic cell structures, such as axons, it is also sensitive to their orientation dispersion. This is a major limitation to the use of FA as a biomarker for " tissue integrity " , especially in regions of complex microarchitecture. In this work, we seek to circumvent this limitation by disentangling the effects of microscopic diffusion anisotropy from the orientation dispersion. The microscopic fractional anisotropy (μFA) and the order parameter (OP) were calculated from the contrast between signal prepared with directional and isotropic diffusion encoding, where the latter was achieved by magic angle spinning of the q-vector (qMAS). These parameters were quantified in healthy volunteers and in two patients ; one patient with meningioma and one with glioblastoma. Finally, we used simulations to elucidate the relation between FA and μFA in various micro-architectures. Generally, μFA was high in the white matter and low in the gray matter. In the white matter, the largest differences between μFA and FA were found in crossing white matter and in interfaces between …

[1]  J. E. Tanner,et al.  Spin diffusion measurements : spin echoes in the presence of a time-dependent field gradient , 1965 .

[2]  P. Basser,et al.  MR diffusion tensor spectroscopy and imaging. , 1994, Biophysical journal.

[3]  A. Song,et al.  Optimized isotropic diffusion weighting , 1995, Magnetic resonance in medicine.

[4]  Mitra,et al.  Multiple wave-vector extensions of the NMR pulsed-field-gradient spin-echo diffusion measurement. , 1995, Physical review. B, Condensed matter.

[5]  P. Basser,et al.  Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. , 1996, Journal of magnetic resonance. Series B.

[6]  J. Pauly,et al.  Isotropic diffusion‐weighted and spiral‐navigated interleaved EPI for routine imaging of acute stroke , 1997, Magnetic resonance in medicine.

[7]  M. Horsfield,et al.  Optimal strategies for measuring diffusion in anisotropic systems by magnetic resonance imaging , 1999, Magnetic resonance in medicine.

[8]  D. Parker,et al.  Analysis of partial volume effects in diffusion‐tensor MRI , 2001, Magnetic resonance in medicine.

[9]  R. Kikinis,et al.  Diffusion tensor imaging and its application to neuropsychiatric disorders. , 2002, Harvard review of psychiatry.

[10]  Carl-Fredrik Westin,et al.  Processing and visualization for diffusion tensor MRI , 2002, Medical Image Anal..

[11]  E. Larsson,et al.  Diffusion tensor MRI post mortem demonstrated cerebral white matter pathology , 2004, Journal of Neurology.

[12]  J. Sijbers,et al.  Maximum likelihood estimation of signal amplitude and noise variance from MR data , 2004, Magnetic resonance in medicine.

[13]  J. Helpern,et al.  Diffusional kurtosis imaging: The quantification of non‐gaussian water diffusion by means of magnetic resonance imaging , 2005, Magnetic resonance in medicine.

[14]  O. Ciccarelli,et al.  Diffusion MRI in multiple sclerosis , 2005, Neurology.

[15]  A. Pfefferbaum,et al.  Diffusion tensor imaging and aging , 2006, Neuroscience & Biobehavioral Reviews.

[16]  Y. Assaf,et al.  Diffusion Tensor Imaging (DTI)-based White Matter Mapping in Brain Research: A Review , 2007, Journal of Molecular Neuroscience.

[17]  T. Nishimura,et al.  Diffusion Anisotropy Measurement of Brain White Matter Is Affected by Voxel Size: Underestimation Occurs in Areas with Crossing Fibers , 2007, American Journal of Neuroradiology.

[18]  H. Kashimura,et al.  Prediction of meningioma consistency using fractional anisotropy value measured by magnetic resonance imaging. , 2007, Journal of neurosurgery.

[19]  大内 宏之 Diffusion anisotropy measurement of brain white matter is affected by voxel size : underestimation occurs in areas with crossing fibers , 2007 .

[20]  Alexander Leemans,et al.  Microstructural maturation of the human brain from childhood to adulthood , 2008, NeuroImage.

[21]  S. Ng,et al.  Differentiation Between Classic and Atypical Meningiomas with Use of Diffusion Tensor Imaging , 2008, American Journal of Neuroradiology.

[22]  D. Alexander A general framework for experiment design in diffusion MRI and its application in measuring direct tissue‐microstructure features , 2008, Magnetic resonance in medicine.

[23]  W. Kaiser,et al.  Diffusion tensor imaging: the normal evolution of ADC, RA, FA, and eigenvalues studied in multiple anatomical regions of the brain , 2009, Neuroradiology.

[24]  Timothy Edward John Behrens,et al.  Training induces changes in white matter architecture , 2009, Nature Neuroscience.

[25]  F. Ståhlberg,et al.  On the effects of a varied diffusion time in vivo: is the diffusion in white matter restricted? , 2009, Magnetic resonance imaging.

[26]  M. Koch,et al.  A tensor model and measures of microscopic anisotropy for double-wave-vector diffusion-weighting experiments with long mixing times. , 2010, Journal of magnetic resonance.

[27]  E. Larsson,et al.  Alzheimer's disease (AD) and executive dysfunction. A case-control study on the significance of frontal white matter changes detected by diffusion tensor imaging (DTI). , 2010, Archives of gerontology and geriatrics.

[28]  Sun Shu-xia Differentiation of fibroblastic meningiomas from other benign subtypes using diffusion tensor imaging , 2010 .

[29]  Jung-Lung Hsu,et al.  Microstructural white matter changes in normal aging: A diffusion tensor imaging study with higher-order polynomial regression models , 2010, NeuroImage.

[30]  Max A. Viergever,et al.  elastix: A Toolbox for Intensity-Based Medical Image Registration , 2010, IEEE Transactions on Medical Imaging.

[31]  Max A. Viergever,et al.  Partial volume effect as a hidden covariate in DTI analyses , 2011, NeuroImage.

[32]  Stephen M. Smith,et al.  DTI measures in crossing-fibre areas: Increased diffusion anisotropy reveals early white matter alteration in MCI and mild Alzheimer's disease , 2011, NeuroImage.

[33]  Hui Zhang,et al.  Axon diameter mapping in the presence of orientation dispersion with diffusion MRI , 2011, NeuroImage.

[34]  Gabriel Peyré,et al.  The Numerical Tours of Signal Processing , 2011, Comput. Sci. Eng..

[35]  Y. Cohen,et al.  Microscopic and compartment shape anisotropies in gray and white matter revealed by angular bipolar double‐PFG MR , 2011, Magnetic resonance in medicine.

[36]  Daniel C. Alexander,et al.  NODDI: Practical in vivo neurite orientation dispersion and density imaging of the human brain , 2012, NeuroImage.

[37]  Max A. Viergever,et al.  The influence of complex white matter architecture on the mean diffusivity in diffusion tensor MRI of the human brain , 2012, NeuroImage.

[38]  M. Rudemo,et al.  The gamma distribution model for pulsed-field gradient NMR studies of molecular-weight distributions of polymers. , 2012, Journal of magnetic resonance.

[39]  F. Ståhlberg,et al.  The importance of axonal undulation in diffusion MR measurements: a Monte Carlo simulation study , 2012, NMR in biomedicine.

[40]  Lawrence L. Wald,et al.  Surface based analysis of diffusion orientation for identifying architectonic domains in the in vivo human cortex , 2013, NeuroImage.

[41]  J. Mårtensson,et al.  Diffusion Tensor Tractography versus Volumetric Imaging in the Diagnosis of Behavioral Variant Frontotemporal Dementia , 2013, PloS one.

[42]  S. Lasič,et al.  Isotropic diffusion weighting in PGSE NMR by magic-angle spinning of the q-vector. , 2013, Journal of magnetic resonance.

[43]  A. Leemans,et al.  Assessment of Global and Regional Diffusion Changes along White Matter Tracts in Parkinsonian Disorders by MR Tractography , 2013, PloS one.

[44]  Suvrit Sra,et al.  The multivariate Watson distribution: Maximum-likelihood estimation and other aspects , 2011, J. Multivar. Anal..

[45]  F. Ståhlberg,et al.  The role of tissue microstructure and water exchange in biophysical modelling of diffusion in white matter , 2013, Magnetic Resonance Materials in Physics, Biology and Medicine.

[46]  D. Topgaard Isotropic diffusion weighting in PGSE NMR: Numerical optimization of the q-MAS PGSE sequence , 2013 .

[47]  J. Finsterbusch,et al.  Double‐wave‐vector diffusion‐weighted imaging reveals microscopic diffusion anisotropy in the living human brain , 2013, Magnetic resonance in medicine.

[48]  C. Sønderby,et al.  Orientationally invariant metrics of apparent compartment eccentricity from double pulsed field gradient diffusion experiments , 2013, NMR in biomedicine.

[49]  Alexander Leemans,et al.  Variability in diffusion kurtosis imaging: Impact on study design, statistical power and interpretation , 2013, NeuroImage.

[50]  A. Song,et al.  Cortical Depth Dependence of the Diffusion Anisotropy in the Human Cortical Gray Matter In Vivo , 2014, PloS one.

[51]  G. Frisoni,et al.  Fractional anisotropy changes in Alzheimer's disease depend on the underlying fiber tract architecture: a multiparametric DTI study using joint independent component analysis. , 2014, Journal of Alzheimer's disease : JAD.

[52]  Derek K. Jones,et al.  Why diffusion tensor MRI does well only some of the time: Variance and covariance of white matter tissue microstructure attributes in the living human brain☆ , 2014, NeuroImage.

[53]  Carl-Fredrik Westin,et al.  Measurement Tensors in Diffusion MRI: Generalizing the Concept of Diffusion Encoding , 2014, MICCAI.

[54]  F. Szczepankiewicz,et al.  Microanisotropy imaging: quantification of microscopic diffusion anisotropy and orientational order parameter by diffusion MRI with magic-angle spinning of the q-vector , 2014, Front. Physics.

[55]  C. Sønderby,et al.  Commentary on “Microanisotropy imaging: quantification of microscopic diffusion anisotropy and orientation of order parameter by diffusion MRI with magic-angle spinning of the q-vector” , 2014, Front. Physics.

[56]  J. Helpern,et al.  Double-pulsed diffusional kurtosis imaging. , 2014, NMR in biomedicine.

[57]  J. Finsterbusch,et al.  Mapping measures of microscopic diffusion anisotropy in human brain white matter in vivo with double‐wave‐vector diffusion‐weighted imaging , 2015, Magnetic resonance in medicine.

[58]  Carl-Fredrik Westin,et al.  Quantification of microscopic diffusion anisotropy disentangles effects of orientation dispersion from microstructure: Applications in healthy volunteers and in brain tumors , 2015, NeuroImage.