Rich-Club Organization: An Important Determinant of Functional Outcome After Acute Ischemic Stroke

Objective: To determine whether the rich-club organization, essential for information transport in the human connectome, is an important biomarker of functional outcome after acute ischemic stroke (AIS).Methods: Consecutive AIS patients (N = 344) with acute brain magnetic resonance imaging (MRI) (&a...

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Main Authors: Markus D. Schirmer, Sofia Ira Ktena, Marco J. Nardin, Kathleen L. Donahue, Anne-Katrin Giese, Mark R. Etherton, Ona Wu, Natalia S. Rost
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-09-01
Series:Frontiers in Neurology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fneur.2019.00956/full
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author Markus D. Schirmer
Markus D. Schirmer
Markus D. Schirmer
Sofia Ira Ktena
Marco J. Nardin
Kathleen L. Donahue
Anne-Katrin Giese
Mark R. Etherton
Ona Wu
Natalia S. Rost
author_facet Markus D. Schirmer
Markus D. Schirmer
Markus D. Schirmer
Sofia Ira Ktena
Marco J. Nardin
Kathleen L. Donahue
Anne-Katrin Giese
Mark R. Etherton
Ona Wu
Natalia S. Rost
author_sort Markus D. Schirmer
collection DOAJ
description Objective: To determine whether the rich-club organization, essential for information transport in the human connectome, is an important biomarker of functional outcome after acute ischemic stroke (AIS).Methods: Consecutive AIS patients (N = 344) with acute brain magnetic resonance imaging (MRI) (<48 h) were eligible for this study. Each patient underwent a clinical MRI protocol, which included diffusion weighted imaging (DWI). All DWIs were registered to a template on which rich-club regions have been defined. Using manual outlines of stroke lesions, we automatically counted the number of affected rich-club regions and assessed its effect on the National Institute of Health Stroke Scale (NIHSS) and modified Rankin Scale (mRS; obtained at 90 days post-stroke) scores through ordinal regression.Results: Of 344 patients (median age 65, inter-quartile range 54–76 years) with a median DWI lesion volume (DWIv) of 3cc, 64% were male. We established that an increase in number of rich-club regions affected by a stroke increases the odds of poor stroke outcome, measured by NIHSS (OR: 1.77, 95%CI 1.41–2.21) and mRS (OR: 1.38, 95%CI 1.11–1.73). Additionally, we demonstrated that the OR exceeds traditional markers, such as DWIv (ORNIHSS 1.08, 95%CI 1.06–1.11; ORmRS 1.05, 95%CI 1.03–1.07) and age (ORNIHSS 1.03, 95%CI 1.01–1.05; ORmRS 1.05, 95%CI 1.03–1.07).Conclusion: In this proof-of-concept study, the number of rich-club nodes affected by a stroke lesion presents a translational biomarker of stroke outcome, which can be readily assessed using standard clinical AIS imaging protocols and considered in functional outcome prediction models beyond traditional factors.
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spelling doaj.art-b0e558d42b7e4e399d51ba0cd98fb6692022-12-22T00:53:02ZengFrontiers Media S.A.Frontiers in Neurology1664-22952019-09-011010.3389/fneur.2019.00956479083Rich-Club Organization: An Important Determinant of Functional Outcome After Acute Ischemic StrokeMarkus D. Schirmer0Markus D. Schirmer1Markus D. Schirmer2Sofia Ira Ktena3Marco J. Nardin4Kathleen L. Donahue5Anne-Katrin Giese6Mark R. Etherton7Ona Wu8Natalia S. Rost9Department of Neurology, J. Philip Kistler Stroke Research Center, Harvard Medical School, Boston, MA, United StatesComputer Science and Artificial Intelligence Lab, Massachusetts Institute of Technology, Cambridge, MA, United StatesDepartment of Population Health Sciences, German Center for Neurodegenerative Diseases (DZNE), Bonn, GermanyBiomedical Image Analysis Group, Imperial College London, London, United KingdomDepartment of Neurology, J. Philip Kistler Stroke Research Center, Harvard Medical School, Boston, MA, United StatesDepartment of Neurology, J. Philip Kistler Stroke Research Center, Harvard Medical School, Boston, MA, United StatesDepartment of Neurology, J. Philip Kistler Stroke Research Center, Harvard Medical School, Boston, MA, United StatesDepartment of Neurology, J. Philip Kistler Stroke Research Center, Harvard Medical School, Boston, MA, United StatesDepartment of Radiology, Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Boston, MA, United StatesDepartment of Neurology, J. Philip Kistler Stroke Research Center, Harvard Medical School, Boston, MA, United StatesObjective: To determine whether the rich-club organization, essential for information transport in the human connectome, is an important biomarker of functional outcome after acute ischemic stroke (AIS).Methods: Consecutive AIS patients (N = 344) with acute brain magnetic resonance imaging (MRI) (<48 h) were eligible for this study. Each patient underwent a clinical MRI protocol, which included diffusion weighted imaging (DWI). All DWIs were registered to a template on which rich-club regions have been defined. Using manual outlines of stroke lesions, we automatically counted the number of affected rich-club regions and assessed its effect on the National Institute of Health Stroke Scale (NIHSS) and modified Rankin Scale (mRS; obtained at 90 days post-stroke) scores through ordinal regression.Results: Of 344 patients (median age 65, inter-quartile range 54–76 years) with a median DWI lesion volume (DWIv) of 3cc, 64% were male. We established that an increase in number of rich-club regions affected by a stroke increases the odds of poor stroke outcome, measured by NIHSS (OR: 1.77, 95%CI 1.41–2.21) and mRS (OR: 1.38, 95%CI 1.11–1.73). Additionally, we demonstrated that the OR exceeds traditional markers, such as DWIv (ORNIHSS 1.08, 95%CI 1.06–1.11; ORmRS 1.05, 95%CI 1.03–1.07) and age (ORNIHSS 1.03, 95%CI 1.01–1.05; ORmRS 1.05, 95%CI 1.03–1.07).Conclusion: In this proof-of-concept study, the number of rich-club nodes affected by a stroke lesion presents a translational biomarker of stroke outcome, which can be readily assessed using standard clinical AIS imaging protocols and considered in functional outcome prediction models beyond traditional factors.https://www.frontiersin.org/article/10.3389/fneur.2019.00956/fullacute ischemic strokeoutcomerich-clubnetwork topologylesion
spellingShingle Markus D. Schirmer
Markus D. Schirmer
Markus D. Schirmer
Sofia Ira Ktena
Marco J. Nardin
Kathleen L. Donahue
Anne-Katrin Giese
Mark R. Etherton
Ona Wu
Natalia S. Rost
Rich-Club Organization: An Important Determinant of Functional Outcome After Acute Ischemic Stroke
Frontiers in Neurology
acute ischemic stroke
outcome
rich-club
network topology
lesion
title Rich-Club Organization: An Important Determinant of Functional Outcome After Acute Ischemic Stroke
title_full Rich-Club Organization: An Important Determinant of Functional Outcome After Acute Ischemic Stroke
title_fullStr Rich-Club Organization: An Important Determinant of Functional Outcome After Acute Ischemic Stroke
title_full_unstemmed Rich-Club Organization: An Important Determinant of Functional Outcome After Acute Ischemic Stroke
title_short Rich-Club Organization: An Important Determinant of Functional Outcome After Acute Ischemic Stroke
title_sort rich club organization an important determinant of functional outcome after acute ischemic stroke
topic acute ischemic stroke
outcome
rich-club
network topology
lesion
url https://www.frontiersin.org/article/10.3389/fneur.2019.00956/full
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