Lower self-report fatigue in multiple sclerosis is associated with localized white matter tract disruption between amygdala, temporal pole, insula, and other connected structures.


Journal

Multiple sclerosis and related disorders
ISSN: 2211-0356
Titre abrégé: Mult Scler Relat Disord
Pays: Netherlands
ID NLM: 101580247

Informations de publication

Date de publication:
Jan 2019
Historique:
received: 28 09 2018
revised: 06 11 2018
accepted: 08 11 2018
pubmed: 20 11 2018
medline: 5 4 2019
entrez: 20 11 2018
Statut: ppublish

Résumé

Fatigue, a frequent and disabling symptom for people with multiple sclerosis (PwMS), inconsistently correlates with white matter (WM) pathology. Network-based analysis, accounting for the manner in which lesions disrupt networks of structurally connected gray matter (GM) regions, may provide additional insight. To identify patterns of WM tract disruption which explain self-reported fatigue severity in PwMS. 137 PwMS and 50 age- and sex-matched healthy controls (HC) underwent fatigue assessment and brain MRI. Lesion maps were applied to determine the severity of WM tract disruption between pairs of GM regions. Then, the Network-Based-Statistics tool was applied to identify structural networks whose disruption explained fatigue severity. To determine whether these networks explain unique variance above conventional MRI measures and depression, regressions were applied controlling for age, sex, brain volume, T2-lesion volume, and depression. Patient-perceived fatigue in PwMS was positively associated with overall lesion burden (β = 0.563, p-value < 0.001). In contrast, localized disruptions in WM tracts between regions including the amygdala, insula, hippocampus, putamen, temporal pole, caudal-middle-frontal gyrus, rostral-middle-frontal gyrus, inferior-parietal gyrus, and banks of the superior temporal sulcus were significantly negatively correlated with fatigue in PwMS (β = -0.586, p-value < 0.001). Average disruption within this specific, localized network explained significant additional variance in fatigue above what was otherwise explained by depression and conventional MRI measures of neuropathology (ΔR Although overall lesion burden correlates positively with fatigue in PwMS, localized WM damage between the amygdala, temporal pole, and other connected structures is associated with lower severity of patient-perceived fatigue.

Sections du résumé

BACKGROUND BACKGROUND
Fatigue, a frequent and disabling symptom for people with multiple sclerosis (PwMS), inconsistently correlates with white matter (WM) pathology. Network-based analysis, accounting for the manner in which lesions disrupt networks of structurally connected gray matter (GM) regions, may provide additional insight.
OBJECTIVE OBJECTIVE
To identify patterns of WM tract disruption which explain self-reported fatigue severity in PwMS.
METHODS METHODS
137 PwMS and 50 age- and sex-matched healthy controls (HC) underwent fatigue assessment and brain MRI. Lesion maps were applied to determine the severity of WM tract disruption between pairs of GM regions. Then, the Network-Based-Statistics tool was applied to identify structural networks whose disruption explained fatigue severity. To determine whether these networks explain unique variance above conventional MRI measures and depression, regressions were applied controlling for age, sex, brain volume, T2-lesion volume, and depression.
RESULTS RESULTS
Patient-perceived fatigue in PwMS was positively associated with overall lesion burden (β = 0.563, p-value < 0.001). In contrast, localized disruptions in WM tracts between regions including the amygdala, insula, hippocampus, putamen, temporal pole, caudal-middle-frontal gyrus, rostral-middle-frontal gyrus, inferior-parietal gyrus, and banks of the superior temporal sulcus were significantly negatively correlated with fatigue in PwMS (β = -0.586, p-value < 0.001). Average disruption within this specific, localized network explained significant additional variance in fatigue above what was otherwise explained by depression and conventional MRI measures of neuropathology (ΔR
CONCLUSION CONCLUSIONS
Although overall lesion burden correlates positively with fatigue in PwMS, localized WM damage between the amygdala, temporal pole, and other connected structures is associated with lower severity of patient-perceived fatigue.

Identifiants

pubmed: 30453198
pii: S2211-0348(18)30490-5
doi: 10.1016/j.msard.2018.11.005
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

298-304

Informations de copyright

Copyright © 2018. Published by Elsevier B.V.

Auteurs

Tom A Fuchs (TA)

Jacobs Multiple Sclerosis Center for Treatment and Research, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York (SUNY), Buffalo, NY, USA; Buffalo Neuroimaging Analysis Center, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York (SUNY), Buffalo, NY, USA.

Caila B Vaughn (CB)

Jacobs Multiple Sclerosis Center for Treatment and Research, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York (SUNY), Buffalo, NY, USA.

Ralph H B Benedict (RHB)

Jacobs Multiple Sclerosis Center for Treatment and Research, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York (SUNY), Buffalo, NY, USA.

Bianca Weinstock-Guttman (B)

Jacobs Multiple Sclerosis Center for Treatment and Research, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York (SUNY), Buffalo, NY, USA.

Sanjeevani Choudhery (S)

Jacobs Multiple Sclerosis Center for Treatment and Research, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York (SUNY), Buffalo, NY, USA; Buffalo Neuroimaging Analysis Center, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York (SUNY), Buffalo, NY, USA.

Keith Carolus (K)

Jacobs Multiple Sclerosis Center for Treatment and Research, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York (SUNY), Buffalo, NY, USA; Buffalo Neuroimaging Analysis Center, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York (SUNY), Buffalo, NY, USA.

Patrick Rooney (P)

Jacobs Multiple Sclerosis Center for Treatment and Research, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York (SUNY), Buffalo, NY, USA; Buffalo Neuroimaging Analysis Center, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York (SUNY), Buffalo, NY, USA.

Kira Ashton (K)

Jacobs Multiple Sclerosis Center for Treatment and Research, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York (SUNY), Buffalo, NY, USA; Buffalo Neuroimaging Analysis Center, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York (SUNY), Buffalo, NY, USA.

Deepa P Ramasamy (D)

Jacobs Multiple Sclerosis Center for Treatment and Research, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York (SUNY), Buffalo, NY, USA; Buffalo Neuroimaging Analysis Center, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York (SUNY), Buffalo, NY, USA.

Dejan Jakimovski (D)

Jacobs Multiple Sclerosis Center for Treatment and Research, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York (SUNY), Buffalo, NY, USA; Buffalo Neuroimaging Analysis Center, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York (SUNY), Buffalo, NY, USA.

Robert Zivadinov (R)

Jacobs Multiple Sclerosis Center for Treatment and Research, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York (SUNY), Buffalo, NY, USA; Buffalo Neuroimaging Analysis Center, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York (SUNY), Buffalo, NY, USA.

Michael G Dwyer (MG)

Jacobs Multiple Sclerosis Center for Treatment and Research, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York (SUNY), Buffalo, NY, USA; Buffalo Neuroimaging Analysis Center, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York (SUNY), Buffalo, NY, USA. Electronic address: mgdwyer@buffalo.edu.

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Classifications MeSH