Free-Water Imaging in White and Gray Matter in Parkinson’s Disease

This study aimed to discriminate between neuroinflammation and neuronal degeneration in the white matter (WM) and gray matter (GM) of patients with Parkinson’s disease (PD) using free-water (FW) imaging. Analysis using tract-based spatial statistics (TBSS) of 20 patients with PD and 20 healthy individuals revealed changes in FW imaging indices (i.e., reduced FW-corrected fractional anisotropy (FAT), increased FW-corrected mean, axial, and radial diffusivities (MDT, ADT, and RDT, respectively) and fractional volume of FW (FW) in somewhat more specific WM areas compared with the changes of DTI indices. The region-of-interest (ROI) analysis further supported these findings, whereby those with PD showed significantly lower FAT and higher MDT, ADT, and RDT (indices of neuronal degeneration) in anterior WM areas as well as higher FW (index of neuroinflammation) in posterior WM areas compared with the controls. Results of GM-based spatial statistics (GBSS) analysis revealed that patients with PD had significantly higher MDT, ADT, and FW than the controls, whereas ROI analysis showed significantly increased MDT and FW and a trend toward increased ADT in GM areas, corresponding to Braak stage IV. These findings support the hypothesis that neuroinflammation precedes neuronal degeneration in PD, whereas WM microstructural alterations precede changes in GM.

[1]  Ninon Burgos,et al.  New advances in the Clinica software platform for clinical neuroimaging studies , 2019 .

[2]  Fabio Sambataro,et al.  Progressive Decline in Gray and White Matter Integrity in de novo Parkinson’s Disease: An Analysis of Longitudinal Parkinson Progression Markers Initiative Diffusion Tensor Imaging Data , 2018, Front. Aging Neurosci..

[3]  S. Aoki,et al.  Neurite orientation dispersion and density imaging of the nigrostriatal pathway in Parkinson's disease: Retrograde degeneration observed by tract-profile analysis. , 2018, Parkinsonism & related disorders.

[4]  Joseph R. Patterson,et al.  Lewy body-like alpha-synuclein inclusions trigger reactive microgliosis prior to nigral degeneration , 2018, Journal of Neuroinflammation.

[5]  J. Hatazawa,et al.  Japanese multicenter database of healthy controls for [123I]FP-CIT SPECT , 2018, European Journal of Nuclear Medicine and Molecular Imaging.

[6]  I. Rektor,et al.  White matter alterations in Parkinson’s disease with normal cognition precede grey matter atrophy , 2018, PloS one.

[7]  Aldo Quattrone,et al.  Structural connectivity differences in motor network between tremor‐dominant and nontremor Parkinson's disease , 2017, Human brain mapping.

[8]  Ofer Pasternak,et al.  Free water improves detection of changes in the substantia nigra in parkinsonism: A multisite study , 2017, Movement disorders : official journal of the Movement Disorder Society.

[9]  O. Coulon,et al.  Diffusion tensor imaging in Parkinson's disease: Review and meta-analysis , 2017, NeuroImage: Clinical.

[10]  S. Aoki,et al.  Gray Matter Abnormalities in Idiopathic Parkinson's Disease: Evaluation by Diffusional Kurtosis Imaging and Neurite Orientation Dispersion and Density Imaging , 2017, Human brain mapping.

[11]  Peter Savadjiev,et al.  Characterizing white matter changes in chronic schizophrenia: A free-water imaging multi-site study , 2017, Schizophrenia Research.

[12]  L. Tan,et al.  White matter microstructural characteristics in newly diagnosed Parkinson’s disease: An unbiased whole-brain study , 2016, Scientific Reports.

[13]  Stamatios N. Sotiropoulos,et al.  An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging , 2016, NeuroImage.

[14]  R. Barker,et al.  Gray and white matter imaging: A biomarker for cognitive impairment in early Parkinson's disease? , 2016, Movement disorders : official journal of the Movement Disorder Society.

[15]  Jia-wei Zhou,et al.  Neuroinflammation in Parkinson’s disease and its potential as therapeutic target , 2015, Translational Neurodegeneration.

[16]  G. Deuschl,et al.  MDS clinical diagnostic criteria for Parkinson's disease , 2015, Movement disorders : official journal of the Movement Disorder Society.

[17]  Norbert Schuff,et al.  Diffusion tensor imaging of the nigrostriatal fibers in Parkinson's disease , 2015, Movement disorders : official journal of the Movement Disorder Society.

[18]  D. Vaillancourt,et al.  Increased free water in the substantia nigra of Parkinson's disease: a single-site and multi-site study , 2015, Neurobiology of Aging.

[19]  Carl-Fredrik Westin,et al.  The extent of diffusion MRI markers of neuroinflammation and white matter deterioration in chronic schizophrenia , 2015, Schizophrenia Research.

[20]  A. Recasens,et al.  Alpha-synuclein spreading in Parkinson’s disease , 2014, Front. Neuroanat..

[21]  A. Cerasa,et al.  Reduced thalamic volume in Parkinson disease with REM sleep behavior disorder: volumetric study. , 2014, Parkinsonism & related disorders.

[22]  M E Shenton,et al.  Gray matter alterations in early aging: A diffusion magnetic resonance imaging study , 2014, Human brain mapping.

[23]  M. Filippi,et al.  The topography of brain damage at different stages of Parkinson's disease , 2013, Human brain mapping.

[24]  L. Nyberg,et al.  Diffusion tensor imaging and correlations to Parkinson rating scales , 2013, Journal of Neurology.

[25]  Joseph V. Hajnal,et al.  Development of cortical microstructure in the preterm human brain , 2013, Proceedings of the National Academy of Sciences.

[26]  T. Anderson,et al.  White matter microstructure deteriorates across cognitive stages in Parkinson disease , 2013, Neurology.

[27]  J. Jankovic,et al.  How to identify tremor dominant and postural instability/gait difficulty groups with the movement disorder society unified Parkinson's disease rating scale: Comparison with the unified Parkinson's disease rating scale , 2013, Movement disorders : official journal of the Movement Disorder Society.

[28]  Klaus P. Ebmeier,et al.  Diffusion tensor imaging in parkinsonian syndromes , 2013, Neurology.

[29]  Poul Jennum,et al.  A single‐question screen for rapid eye movement sleep behavior disorder: A multicenter validation study , 2012, Movement disorders : official journal of the Movement Disorder Society.

[30]  O. Abe,et al.  Cognitive status correlates with white matter alteration in Parkinson's disease , 2012, Human brain mapping.

[31]  Derek K. Jones,et al.  How and how not to correct for CSF-contamination in diffusion MRI , 2012, NeuroImage.

[32]  M. Urashima,et al.  The odor stick identification test for Japanese differentiates Parkinson's disease from multiple system atrophy and progressive supra nuclear palsy , 2011, BMC neurology.

[33]  K. Trinkaus,et al.  Quantification of increased cellularity during inflammatory demyelination. , 2011, Brain : a journal of neurology.

[34]  R. Burke,et al.  Clinical progression in Parkinson disease and the neurobiology of axons , 2010, Annals of neurology.

[35]  H. Braak,et al.  A timeline for Parkinson's disease. , 2010, Parkinsonism & related disorders.

[36]  Joel S. Perlmutter,et al.  Assessment of Parkinson Disease Manifestations , 2009, Current protocols in neuroscience.

[37]  N. Intrator,et al.  Free water elimination and mapping from diffusion MRI , 2009, Magnetic resonance in medicine.

[38]  Moo K. Chung,et al.  A study of diffusion tensor imaging by tissue-specific, smoothing-compensated voxel-based analysis , 2009, NeuroImage.

[39]  H. Braak,et al.  Invited Article: Nervous system pathology in sporadic Parkinson disease , 2008, Neurology.

[40]  John Ashburner,et al.  A fast diffeomorphic image registration algorithm , 2007, NeuroImage.

[41]  S Fook-Chong,et al.  Case control study of diffusion tensor imaging in Parkinson’s disease , 2007, Journal of Neurology, Neurosurgery, and Psychiatry.

[42]  A. Alexander,et al.  Diffusion tensor imaging of the brain , 2007, Neurotherapeutics.

[43]  J. Helpern,et al.  Three‐dimensional characterization of non‐gaussian water diffusion in humans using diffusion kurtosis imaging , 2006, NMR in biomedicine.

[44]  I. McKeith,et al.  Pathophysiology of synuclein aggregation in Lewy body disease , 2006, Mechanisms of Ageing and Development.

[45]  E. Tolosa,et al.  Characteristics of idiopathic REM sleep behavior disorder and that associated with MSA and PD , 2005, Neurology.

[46]  Y Nakata,et al.  Early pathological changes in the parkinsonian brain demonstrated by diffusion tensor MRI , 2004, Journal of Neurology, Neurosurgery & Psychiatry.

[47]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[48]  H. Braak,et al.  Parkinson’s disease: the thalamic components of the limbic loop are severely impaired by α-synuclein immunopositive inclusion body pathology , 2002, Neurobiology of Aging.

[49]  Karl J. Friston,et al.  Voxel-Based Morphometry—The Methods , 2000, NeuroImage.

[50]  V. Lee,et al.  Modeling Lewy pathology propagation in Parkinson's disease. , 2014, Parkinsonism & related disorders.

[51]  D. Dickson,et al.  Evidence in favor of Braak staging of Parkinson's disease , 2010, Movement disorders : official journal of the Movement Disorder Society.

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

[53]  Thomas E. Nichols,et al.  A related paper has been accepted for publication in NeuroImage ) , 2005 .

[54]  Stephen M. Smith,et al.  Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm , 2001, IEEE Transactions on Medical Imaging.

[55]  Jacob Cohen.  QUANTITATIVE METHODS IN PSYCHOLOGY A Power Primer , 1992 .