Advanced diffusion MRI and image texture analysis detect widespread brain structural differences between relapsing-remitting and secondary progressive multiple sclerosis

IntroductionDisease development in multiple sclerosis (MS) causes dramatic structural changes, but the exact changing patterns are unclear. Our objective is to investigate the differences in brain structure locally and spatially between relapsing-remitting MS (RRMS) and its advanced form, secondary...

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Main Authors: Olayinka Oladosu, Wei-Qiao Liu, Lenora Brown, Bruce G. Pike, Luanne M. Metz, Yunyan Zhang
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-08-01
Series:Frontiers in Human Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnhum.2022.944908/full
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author Olayinka Oladosu
Olayinka Oladosu
Wei-Qiao Liu
Wei-Qiao Liu
Lenora Brown
Lenora Brown
Bruce G. Pike
Bruce G. Pike
Bruce G. Pike
Luanne M. Metz
Luanne M. Metz
Yunyan Zhang
Yunyan Zhang
Yunyan Zhang
author_facet Olayinka Oladosu
Olayinka Oladosu
Wei-Qiao Liu
Wei-Qiao Liu
Lenora Brown
Lenora Brown
Bruce G. Pike
Bruce G. Pike
Bruce G. Pike
Luanne M. Metz
Luanne M. Metz
Yunyan Zhang
Yunyan Zhang
Yunyan Zhang
author_sort Olayinka Oladosu
collection DOAJ
description IntroductionDisease development in multiple sclerosis (MS) causes dramatic structural changes, but the exact changing patterns are unclear. Our objective is to investigate the differences in brain structure locally and spatially between relapsing-remitting MS (RRMS) and its advanced form, secondary progressive MS (SPMS), through advanced analysis of diffusion magnetic resonance imaging (MRI) and image texture.MethodsA total of 20 patients with RRMS and nine patients with SPMS from two datasets underwent 3T anatomical and diffusion tensor imaging (DTI). The DTI was harmonized, augmented, and then modeled, which generated six voxel- and sub-voxel-scale measures. Texture analysis focused on T2 and FLAIR MRI, which produced two phase-based measures, namely, phase congruency and weighted mean phase. Data analysis was 3-fold, i.e., histogram analysis of whole-brain normal appearing white matter (NAWM); region of interest (ROI) analysis of NAWM and lesions within three critical white matter tracts, namely, corpus callosum, corticospinal tract, and optic radiation; and along-tract statistics. Furthermore, by calculating the z-score of core-rim pathology within lesions based on diffusion measures, we developed a novel method to define chronic active lesions and compared them between cohorts.ResultsHistogram features from diffusion and all but one texture measure differentiated between RRMS and SPMS. Within-tract ROI analysis detected cohort differences in both NAWM and lesions of the corpus callosum body in three measures of neurite orientation and anisotropy. Along-tract statistics detected cohort differences from multiple measures, particularly lesion extent, which increased significantly in SPMS in posterior corpus callosum and optic radiations. The number of chronic active lesions were also significantly higher (by 5–20% over z-scores 0.5 and 1.0) in SPMS than RRMS based on diffusion anisotropy, neurite content, and diameter.ConclusionAdvanced diffusion MRI and texture analysis may be promising approaches for thorough understanding of brain structural changes from RRMS to SPMS, thereby providing new insight into disease development mechanisms in MS.
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spelling doaj.art-e0a80b69706840568fb3bfb505c107662022-12-22T02:51:16ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612022-08-011610.3389/fnhum.2022.944908944908Advanced diffusion MRI and image texture analysis detect widespread brain structural differences between relapsing-remitting and secondary progressive multiple sclerosisOlayinka Oladosu0Olayinka Oladosu1Wei-Qiao Liu2Wei-Qiao Liu3Lenora Brown4Lenora Brown5Bruce G. Pike6Bruce G. Pike7Bruce G. Pike8Luanne M. Metz9Luanne M. Metz10Yunyan Zhang11Yunyan Zhang12Yunyan Zhang13Department of Neuroscience, Faculty of Graduate Studies, University of Calgary, Calgary, AB, CanadaHotchkiss Brain Institute, University of Calgary, Calgary, AB, CanadaHotchkiss Brain Institute, University of Calgary, Calgary, AB, CanadaDepartment of Clinical Neurosciences, Cumming School of Medicine, University of Calgary, Calgary, AB, CanadaHotchkiss Brain Institute, University of Calgary, Calgary, AB, CanadaDepartment of Clinical Neurosciences, Cumming School of Medicine, University of Calgary, Calgary, AB, CanadaHotchkiss Brain Institute, University of Calgary, Calgary, AB, CanadaDepartment of Clinical Neurosciences, Cumming School of Medicine, University of Calgary, Calgary, AB, CanadaDepartment of Radiology, Cumming School of Medicine, University of Calgary, Calgary, AB, CanadaHotchkiss Brain Institute, University of Calgary, Calgary, AB, CanadaDepartment of Clinical Neurosciences, Cumming School of Medicine, University of Calgary, Calgary, AB, CanadaHotchkiss Brain Institute, University of Calgary, Calgary, AB, CanadaDepartment of Clinical Neurosciences, Cumming School of Medicine, University of Calgary, Calgary, AB, CanadaDepartment of Radiology, Cumming School of Medicine, University of Calgary, Calgary, AB, CanadaIntroductionDisease development in multiple sclerosis (MS) causes dramatic structural changes, but the exact changing patterns are unclear. Our objective is to investigate the differences in brain structure locally and spatially between relapsing-remitting MS (RRMS) and its advanced form, secondary progressive MS (SPMS), through advanced analysis of diffusion magnetic resonance imaging (MRI) and image texture.MethodsA total of 20 patients with RRMS and nine patients with SPMS from two datasets underwent 3T anatomical and diffusion tensor imaging (DTI). The DTI was harmonized, augmented, and then modeled, which generated six voxel- and sub-voxel-scale measures. Texture analysis focused on T2 and FLAIR MRI, which produced two phase-based measures, namely, phase congruency and weighted mean phase. Data analysis was 3-fold, i.e., histogram analysis of whole-brain normal appearing white matter (NAWM); region of interest (ROI) analysis of NAWM and lesions within three critical white matter tracts, namely, corpus callosum, corticospinal tract, and optic radiation; and along-tract statistics. Furthermore, by calculating the z-score of core-rim pathology within lesions based on diffusion measures, we developed a novel method to define chronic active lesions and compared them between cohorts.ResultsHistogram features from diffusion and all but one texture measure differentiated between RRMS and SPMS. Within-tract ROI analysis detected cohort differences in both NAWM and lesions of the corpus callosum body in three measures of neurite orientation and anisotropy. Along-tract statistics detected cohort differences from multiple measures, particularly lesion extent, which increased significantly in SPMS in posterior corpus callosum and optic radiations. The number of chronic active lesions were also significantly higher (by 5–20% over z-scores 0.5 and 1.0) in SPMS than RRMS based on diffusion anisotropy, neurite content, and diameter.ConclusionAdvanced diffusion MRI and texture analysis may be promising approaches for thorough understanding of brain structural changes from RRMS to SPMS, thereby providing new insight into disease development mechanisms in MS.https://www.frontiersin.org/articles/10.3389/fnhum.2022.944908/fullmultiple sclerosischronic active lesionssingle-shell high angular resolution diffusion imagingdiffusion tensor imagingalong-tract statisticsphase congruency
spellingShingle Olayinka Oladosu
Olayinka Oladosu
Wei-Qiao Liu
Wei-Qiao Liu
Lenora Brown
Lenora Brown
Bruce G. Pike
Bruce G. Pike
Bruce G. Pike
Luanne M. Metz
Luanne M. Metz
Yunyan Zhang
Yunyan Zhang
Yunyan Zhang
Advanced diffusion MRI and image texture analysis detect widespread brain structural differences between relapsing-remitting and secondary progressive multiple sclerosis
Frontiers in Human Neuroscience
multiple sclerosis
chronic active lesions
single-shell high angular resolution diffusion imaging
diffusion tensor imaging
along-tract statistics
phase congruency
title Advanced diffusion MRI and image texture analysis detect widespread brain structural differences between relapsing-remitting and secondary progressive multiple sclerosis
title_full Advanced diffusion MRI and image texture analysis detect widespread brain structural differences between relapsing-remitting and secondary progressive multiple sclerosis
title_fullStr Advanced diffusion MRI and image texture analysis detect widespread brain structural differences between relapsing-remitting and secondary progressive multiple sclerosis
title_full_unstemmed Advanced diffusion MRI and image texture analysis detect widespread brain structural differences between relapsing-remitting and secondary progressive multiple sclerosis
title_short Advanced diffusion MRI and image texture analysis detect widespread brain structural differences between relapsing-remitting and secondary progressive multiple sclerosis
title_sort advanced diffusion mri and image texture analysis detect widespread brain structural differences between relapsing remitting and secondary progressive multiple sclerosis
topic multiple sclerosis
chronic active lesions
single-shell high angular resolution diffusion imaging
diffusion tensor imaging
along-tract statistics
phase congruency
url https://www.frontiersin.org/articles/10.3389/fnhum.2022.944908/full
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