More Than the Sum of Its Parts: Disrupted Core Periphery of Multiplex Brain Networks in Multiple Sclerosis.

Autor:	Pontillo G; Queen Square Multiple Sclerosis Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, University College London, London, UK.; MS Center Amsterdam, Radiology and Nuclear Medicine, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, Amsterdam UMC Location VUmc, Amsterdam, The Netherlands.; Departments of Advanced Biomedical Sciences and Electrical Engineering and Information Technology, University of Naples 'Federico II', Naples, Italy., Prados F; Queen Square Multiple Sclerosis Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, University College London, London, UK.; Centre for Medical Image Computing, Department of Medical Physics and Biomedical Engineering, University College London, London, UK.; E-Health Center, Universitat Oberta de Catalunya, Barcelona, Spain., Wink AM; MS Center Amsterdam, Radiology and Nuclear Medicine, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, Amsterdam UMC Location VUmc, Amsterdam, The Netherlands., Kanber B; Queen Square Multiple Sclerosis Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, University College London, London, UK.; Centre for Medical Image Computing, Department of Medical Physics and Biomedical Engineering, University College London, London, UK., Bisecco A; Department of Advanced Medical and Surgical Sciences, University of Campania 'Luigi Vanvitelli', Naples, Italy., Broeders TAA; MS Center Amsterdam, Anatomy and Neurosciences, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, Amsterdam UMC Location VUmc, Amsterdam, The Netherlands., Brunetti A; Departments of Advanced Biomedical Sciences and Electrical Engineering and Information Technology, University of Naples 'Federico II', Naples, Italy., Cagol A; Translational Imaging in Neurology (ThINK) Basel, Department of Biomedical Engineering, Faculty of Medicine, University Hospital Basel and University of Basel, Basel, Switzerland.; Department of Neurology, University Hospital Basel, Switzerland.; Research Center for Clinical Neuroimmunology and Neuroscience Basel (RC2NB), university Hospital Basel and University of Basel, Basel, Switzerland., Calabrese M; Department of Neurosciences, Biomedicine and Movement Sciences, University of Verona, Verona, Italy., Castellaro M; Department of Neurosciences, Biomedicine and Movement Sciences, University of Verona, Verona, Italy.; Department of Information Engineering, University of Padova, Padova, Italy., Cocozza S; Departments of Advanced Biomedical Sciences and Electrical Engineering and Information Technology, University of Naples 'Federico II', Naples, Italy., Colato E; Queen Square Multiple Sclerosis Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, University College London, London, UK., Collorone S; Queen Square Multiple Sclerosis Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, University College London, London, UK., Cortese R; Department of Medicine, Surgery and Neuroscience, University of Siena, Siena, Italy., De Stefano N; Department of Medicine, Surgery and Neuroscience, University of Siena, Siena, Italy., Douw L; MS Center Amsterdam, Anatomy and Neurosciences, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, Amsterdam UMC Location VUmc, Amsterdam, The Netherlands., Enzinger C; Department of Neurology, Medical University of Graz, Graz, Austria., Filippi M; Neuroimaging Research Unit, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy.; Neurology Unit, IRCCS San Raffaele Scientific Institute, Milan, Italy.; Neurorehabilitation Unit, IRCCS San Raffaele Scientific Institute, Milan, Italy.; Neurophysiology Service, IRCCS San Raffaele Scientific Institute, Milan, Italy.; Vita-Salute San Raffaele University, Milan, Italy., Foster MA; Queen Square Multiple Sclerosis Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, University College London, London, UK., Gallo A; Department of Advanced Medical and Surgical Sciences, University of Campania 'Luigi Vanvitelli', Naples, Italy., Gonzalez-Escamilla G; Movement Disorders, Neurostimulation and Neuroimaging, University Medicine Mainz, Mainz, Germany., Granziera C; Translational Imaging in Neurology (ThINK) Basel, Department of Biomedical Engineering, Faculty of Medicine, University Hospital Basel and University of Basel, Basel, Switzerland.; Department of Neurology, University Hospital Basel, Switzerland.; Research Center for Clinical Neuroimmunology and Neuroscience Basel (RC2NB), university Hospital Basel and University of Basel, Basel, Switzerland., Groppa S; Movement Disorders, Neurostimulation and Neuroimaging, University Medicine Mainz, Mainz, Germany., Harbo HF; Department of Neurology, Oslo University Hospital, Oslo, Norway., Høgestøl EA; Department of Neurology, Oslo University Hospital, Oslo, Norway.; Department of Psychology, University of Oslo, Oslo, Norway., Llufriu S; Center of Neuroimmunology. Laboratory of Advanced Imaging in Neuroimmunological Diseases; Hospital Clinic Barcelona, Institut d'Investigacions Biomediques August pi i Sunyer (IDIBAPS) and Universitat de Barcelona, Barcelona, Spain., Lorenzini L; MS Center Amsterdam, Radiology and Nuclear Medicine, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, Amsterdam UMC Location VUmc, Amsterdam, The Netherlands., Martinez-Heras E; Center of Neuroimmunology. Laboratory of Advanced Imaging in Neuroimmunological Diseases; Hospital Clinic Barcelona, Institut d'Investigacions Biomediques August pi i Sunyer (IDIBAPS) and Universitat de Barcelona, Barcelona, Spain., Messina S; Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UK., Moccia M; Queen Square Multiple Sclerosis Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, University College London, London, UK.; Movement Disorders, Neurostimulation and Neuroimaging, University Medicine Mainz, Mainz, Germany., Nygaard GO; Department of Neurology, Oslo University Hospital, Oslo, Norway., Palace J; Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UK., Petracca M; Department of Neurosciences and Reproductive and Odontostomatological Sciences, University of Naples 'Federico II', Naples, Italy., Pinter D; Department of Neurology, Medical University of Graz, Graz, Austria., Rocca MA; Neuroimaging Research Unit, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy.; Neurology Unit, IRCCS San Raffaele Scientific Institute, Milan, Italy.; Vita-Salute San Raffaele University, Milan, Italy., Strijbis E; MS Center Amsterdam, Neurology, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, Amsterdam UMC Location VUmc, Amsterdam, The Netherlands., Toosy A; Queen Square Multiple Sclerosis Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, University College London, London, UK., Valsasina P; Neuroimaging Research Unit, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy., Vrenken H; MS Center Amsterdam, Radiology and Nuclear Medicine, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, Amsterdam UMC Location VUmc, Amsterdam, The Netherlands., Ciccarelli O; Queen Square Multiple Sclerosis Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, University College London, London, UK., Cole JH; Centre for Medical Image Computing, Department of Computer Science, University College London, London, UK.; Dementia Research Centre, UCL Queen Square Institute of Neurology, University College London, London, UK., Schoonheim MM; MS Center Amsterdam, Anatomy and Neurosciences, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, Amsterdam UMC Location VUmc, Amsterdam, The Netherlands., Barkhof F; Queen Square Multiple Sclerosis Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, University College London, London, UK.; MS Center Amsterdam, Radiology and Nuclear Medicine, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, Amsterdam UMC Location VUmc, Amsterdam, The Netherlands.; Centre for Medical Image Computing, Department of Medical Physics and Biomedical Engineering, University College London, London, UK.; Dementia Research Centre, UCL Queen Square Institute of Neurology, University College London, London, UK.
Jazyk:	angličtina
Zdroj:	Human brain mapping [Hum Brain Mapp] 2025 Jan; Vol. 46 (1), pp. e70107.
DOI:	10.1002/hbm.70107
Abstrakt:	Disruptions to brain networks, measured using structural (sMRI), diffusion (dMRI), or functional (fMRI) MRI, have been shown in people with multiple sclerosis (PwMS), highlighting the relevance of regions in the core of the connectome but yielding mixed results depending on the studied connectivity domain. Using a multilayer network approach, we integrated these three modalities to portray an enriched representation of the brain's core-periphery organization and explore its alterations in PwMS. In this retrospective cross-sectional study, we selected PwMS and healthy controls with complete multimodal brain MRI acquisitions from 13 European centers within the MAGNIMS network. Physical disability and cognition were assessed with the Expanded Disability Status Scale (EDSS) and the symbol digit modalities test (SDMT), respectively. SMRI, dMRI, and resting-state fMRI data were parcellated into 100 cortical and 14 subcortical regions to obtain networks of morphological covariance, structural connectivity, and functional connectivity. Connectivity matrices were merged in a multiplex, from which regional coreness-the probability of a node being part of the multiplex core-and coreness disruption index (κ)-the global weakening of the core-periphery structure-were computed. The associations of κ with disease status (PwMS vs. healthy controls), clinical phenotype, level of physical disability (EDSS ≥ 4 vs. EDSS < 4), and cognitive impairment (SDMT z-score < -1.5) were tested within a linear model framework. Using random forest permutation feature importance, we assessed the relative contribution of κ in the multiplex and single-layer domains, in addition to conventional MRI measures (brain and lesion volumes), in predicting disease status, physical disability, and cognitive impairment. We studied 1048 PwMS (695F, mean ± SD age: 43.3 ± 11.4 years) and 436 healthy controls (250F, mean ± SD age: 38.3 ± 11.8 years). PwMS showed significant disruption of the multiplex core-periphery organization (κ = -0.14, Hedges' g = 0.49, p < 0.001), correlating with clinical phenotype (F = 3.90, p = 0.009), EDSS (Hedges' g = 0.18, p = 0.01), and SDMT (Hedges' g = 0.30, p < 0.001). Multiplex κ was the only connectomic measure adding to conventional MRI in predicting disease status and cognitive impairment, while physical disability also depended on single-layer contributions. In conclusion, we show that multilayer networks represent a biologically and clinically meaningful framework to model multimodal MRI data, with disruption of the core-periphery structure emerging as a potential connectomic biomarker for disease severity and cognitive impairment in PwMS. (© 2024 The Author(s). Human Brain Mapping published by Wiley Periodicals LLC.)
Databáze:	MEDLINE
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