Reliability of Longitudinal Brain Volume Loss Measurements between 2 Sites in Patients with Multiple Sclerosis: Comparison of 7 Quantification Techniques

BACKGROUND AND PURPOSE: Brain volume loss is currently a MR imaging marker of neurodegeneration in MS. Available quantification algorithms perform either direct (segmentation-based techniques) or indirect (registration-based techniques) measurements. Because there is no reference standard technique, the assessment of their accuracy and reliability remains a difficult goal. Therefore, the purpose of this work was to assess the robustness of 7 different postprocessing algorithms applied to images acquired from different MR imaging systems. MATERIALS AND METHODS: Nine patients with MS were followed longitudinally over 1 year (3 time points) on two 1.5T MR imaging systems. Brain volume change measures were assessed using 7 segmentation algorithms: a segmentation-classification algorithm, FreeSurfer, BBSI, KN-BSI, SIENA, SIENAX, and JI algorithm. RESULTS: Intersite variability showed that segmentation-based techniques and SIENAX provided large and heterogeneous values of brain volume changes. A Bland-Altman analysis showed a mean difference of 1.8%, 0.07%, and 0.79% between the 2 sites, and a wide length agreement interval of 11.66%, 7.92%, and 11.94% for the segmentation-classification algorithm, FreeSurfer, and SIENAX, respectively. In contrast, registration-based algorithms showed better reproducibility, with a low mean difference of 0.45% for BBSI, KN-BSI and JI, and a mean length agreement interval of 1.55%. If SIENA obtained a lower mean difference of 0.12%, its agreement interval of 3.29% was wider. CONCLUSIONS: If brain atrophy estimation remains an open issue, future investigations of the accuracy and reliability of the brain volume quantification algorithms are needed to measure the slow and small brain volume changes occurring in MS.

[1]  Nick C. Fox,et al.  Accuracy assessment of global and local atrophy measurement techniques with realistic simulated longitudinal Alzheimer's disease images , 2008, NeuroImage.

[2]  Alan C. Evans,et al.  A nonparametric method for automatic correction of intensity nonuniformity in MRI data , 1998, IEEE Transactions on Medical Imaging.

[3]  B. Lewis,et al.  Methylprednisolone effect on brain volume and enhancing lesions in MS before and during IFN&bgr;-1b , 2002, Neurology.

[4]  Nick C. Fox,et al.  Phenomenological Model of Diffuse Global and Regional Atrophy Using Finite-Element Methods , 2006, IEEE Transactions on Medical Imaging.

[5]  R. Henry,et al.  Measurement of Whole‐Brain Atrophy in Multiple Sclerosis , 2004, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[6]  Massimo Filippi,et al.  Quantitative volumetric analysis of brain magnetic resonance imaging from patients with multiple sclerosis , 1998, Journal of the Neurological Sciences.

[7]  Jerry L Prince,et al.  A computerized approach for morphological analysis of the corpus callosum. , 1996, Journal of computer assisted tomography.

[8]  Michael Weiner,et al.  Tensor-based morphometry as a neuroimaging biomarker for Alzheimer's disease: An MRI study of 676 AD, MCI, and normal subjects , 2008, NeuroImage.

[9]  Anders M. Dale,et al.  MRI-derived measurements of human subcortical, ventricular and intracranial brain volumes: Reliability effects of scan sessions, acquisition sequences, data analyses, scanner upgrade, scanner vendors and field strengths , 2009, NeuroImage.

[10]  F. Jolesz,et al.  MRI contrast uptake in new lesions in relapsing-remitting MS followed at weekly intervals , 2003, Neurology.

[11]  Alan C. Evans,et al.  Growth patterns in the developing brain detected by using continuum mechanical tensor maps , 2000, Nature.

[12]  Mehul P. Sampat,et al.  Disease modeling in multiple sclerosis: Assessment and quantification of sources of variability in brain parenchymal fraction measurements , 2010, NeuroImage.

[13]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[14]  Katrin Amunts,et al.  Detection of structural changes of the human brain in longitudinally acquired MR images by deformation field morphometry: Methodological analysis, validation and application , 2008, NeuroImage.

[15]  Anders M. Dale,et al.  Reliability of MRI-derived measurements of human cerebral cortical thickness: The effects of field strength, scanner upgrade and manufacturer , 2006, NeuroImage.

[16]  M. A. Horsfield,et al.  Whole-brain atrophy in multiple sclerosis measured by two segmentation processes from various MRI sequences , 2003, Journal of the Neurological Sciences.

[17]  Neil Gordon,et al.  Apparent Cerebral Atrophy in Patients on Treatment with Steroids , 1980, Developmental medicine and child neurology.

[18]  Y. Chen,et al.  Image registration via level-set motion: Applications to atlas-based segmentation , 2003, Medical Image Anal..

[19]  A. Dale,et al.  Whole Brain Segmentation Automated Labeling of Neuroanatomical Structures in the Human Brain , 2002, Neuron.

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

[21]  W. Heindel,et al.  Dehydration confounds the assessment of brain atrophy , 2005, Neurology.

[22]  Gianpaolo Donzelli,et al.  Catch-Up Growth in Short-at-Birth NICU Graduates , 2000, Hormone Research in Paediatrics.

[23]  David H. Miller,et al.  Early development of multiple sclerosis is associated with progressive grey matter atrophy in patients presenting with clinically isolated syndromes. , 2004, Brain : a journal of neurology.

[24]  P. Matthews,et al.  Normalized Accurate Measurement of Longitudinal Brain Change , 2001, Journal of computer assisted tomography.

[25]  Elizabeth Fisher,et al.  Brain atrophy and magnetization transfer ratio following methylprednisolone in multiple sclerosis: short-term changes and long-term implications , 2005, Multiple sclerosis.

[26]  D. Louis Collins,et al.  Gradient distortions in MRI: Characterizing and correcting for their effects on SIENA-generated measures of brain volume change , 2010, NeuroImage.

[27]  Michael Weiner,et al.  Robust atrophy rate measurement in Alzheimer's disease using multi-site serial MRI: Tissue-specific intensity normalization and parameter selection , 2010, NeuroImage.

[28]  R. Bakshi,et al.  Whole-brain atrophy in multiple sclerosis measured by automated versus semiautomated MR imaging segmentation. , 2004, AJNR. American journal of neuroradiology.

[29]  N Roberts,et al.  Automatic measurement of changes in brain volume on consecutive 3D MR images by segmentation propagation. , 2000, Magnetic resonance imaging.

[30]  A. Compston,et al.  Recommended diagnostic criteria for multiple sclerosis: Guidelines from the international panel on the diagnosis of multiple sclerosis , 2001, Annals of neurology.

[31]  Nick C Fox,et al.  Interactive algorithms for the segmentation and quantitation of 3-D MRI brain scans. , 1997, Computer methods and programs in biomedicine.

[32]  David H. Miller,et al.  Biomarkers and surrogate outcomes in neurodegenerative disease: Lessons from multiple sclerosis , 2004, NeuroRX.

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

[34]  Nick C. Fox,et al.  The boundary shift integral: an accurate and robust measure of cerebral volume changes from registered repeat MRI , 1997, IEEE Transactions on Medical Imaging.

[35]  Paul M. Thompson,et al.  Intensity non-uniformity correction using N3 on 3-T scanners with multichannel phased array coils , 2008, NeuroImage.

[36]  Anders M. Dale,et al.  Reliability in multi-site structural MRI studies: Effects of gradient non-linearity correction on phantom and human data , 2006, NeuroImage.

[37]  Arno Klein,et al.  Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration , 2009, NeuroImage.

[38]  E M Haacke,et al.  MR artifacts: a review. , 1986, AJR. American journal of roentgenology.

[39]  C. Guttmann,et al.  MR Imaging Intensity Modeling of Damage and Repair In Multiple Sclerosis: Relationship of Short-Term Lesion Recovery to Progression and Disability , 2007, American Journal of Neuroradiology.

[40]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[41]  Michael I. Miller,et al.  Deformable templates using large deformation kinematics , 1996, IEEE Trans. Image Process..

[42]  Swati Sharma,et al.  Evaluation of brain atrophy estimation algorithms using simulated ground-truth data , 2010, Medical Image Anal..

[43]  Daniel Rueckert,et al.  Cerebral atrophy measurements using Jacobian integration: Comparison with the boundary shift integral , 2006, NeuroImage.

[44]  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.

[45]  Jean-Claude Froment,et al.  Unsupervised and Adaptive Segmentation of Multispectral 3D Magnetic Resonance Images of Human Brain: A Generic Approach , 2001, MICCAI.

[46]  André J. W. van der Kouwe,et al.  Detection of cortical thickness correlates of cognitive performance: Reliability across MRI scan sessions, scanners, and field strengths , 2008, NeuroImage.

[47]  R. Herndon,et al.  A longitudinal study of brain atrophy in relapsing multiple sclerosis , 1999, Neurology.

[48]  Nick C Fox,et al.  Brain atrophy progression measured from registered serial MRI: Validation and application to alzheimer's disease , 1997, Journal of magnetic resonance imaging : JMRI.

[49]  Rohit Bakshi,et al.  A semiautomated measure of whole-brain atrophy in multiple sclerosis , 2003, Journal of the Neurological Sciences.

[50]  Christos Davatzikos,et al.  Simulation of tissue atrophy using a topology preserving transformation model , 2006, IEEE Transactions on Medical Imaging.

[51]  Marco Rovaris,et al.  Intercenter agreement of brain atrophy measurement in multiple sclerosis patients using manually‐edited SIENA and SIENAX , 2007, Journal of magnetic resonance imaging : JMRI.

[52]  C H Polman,et al.  Cerebral volume changes in multiple sclerosis patients treated with high-dose intravenous methylprednisolone , 2002, Multiple sclerosis.

[53]  Johan Montagnat,et al.  Automated Estimation of Brain Volume in Multiple Sclerosis with BICCR , 2001, IPMI.

[54]  Xingchang Wei,et al.  Has your patient's multiple sclerosis lesion burden or brain atrophy actually changed? , 2004, Multiple sclerosis.