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      In patients with mild disability NMOSD: is the alteration in the cortical morphological or functional network topological properties more significant

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          Abstract

          Objective

          To assess the alteration of individual brain morphological and functional network topological properties and their clinical significance in patients with neuromyelitis optica spectrum disorder (NMOSD).

          Materials and methods

          Eighteen patients with NMOSD and twenty-two healthy controls (HCs) were included. The clinical assessment of NMOSD patients involved evaluations of disability status, cognitive function, and fatigue impact. For each participant, brain images, including high-resolution T1-weighted images for individual morphological brain networks (MBNs) and resting-state functional MR images for functional brain networks (FBNs) were obtained. Topological properties were calculated and compared for both MBNs and FBNs. Then, partial correlation analysis was performed to investigate the relationships between the altered network properties and clinical variables. Finally, the altered network topological properties were used to classify NMOSD patients from HCs and to analyses time- to-progression of the patients.

          Results

          The average Expanded Disability Status Scale score of NMOSD patients was 1.05 (range from 0 to 2), indicating mild disability. Compared to HCs, NMOSD patients exhibited a higher normalized characteristic path length (λ) in their MBNs (P = 0.0118, FDR corrected) but showed no significant differences in the global properties of FBNs (p: 0.405-0.488). Network-based statistical analysis revealed that MBNs had more significantly altered connections (P< 0.01, NBS corrected) than FBNs. Altered nodal properties of MBNs were correlated with disease duration or fatigue scores (P< 0.05/6 with Bonferroni correction). Using the altered nodal properties of MBNs, the accuracy of classification of NMOSD patients versus HCs was 96.4%, with a sensitivity of 93.3% and a specificity of 100%. This accuracy was better than that achieved using the altered nodal properties of FBNs. Nodal properties of MBN significantly predicted Expanded Disability Status Scale worsening in patients with NMOSD.

          Conclusion

          The results indicated that patients with mild disability NMOSD exhibited compensatory increases in local network properties to maintain overall stability. Furthermore, the alterations in the morphological network nodal properties of NMOSD patients not only had better relevance for clinical assessments compared with functional network nodal properties, but also exhibited predictive values of EDSS worsening.

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          Most cited references41

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          Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain.

          An anatomical parcellation of the spatially normalized single-subject high-resolution T1 volume provided by the Montreal Neurological Institute (MNI) (D. L. Collins et al., 1998, Trans. Med. Imag. 17, 463-468) was performed. The MNI single-subject main sulci were first delineated and further used as landmarks for the 3D definition of 45 anatomical volumes of interest (AVOI) in each hemisphere. This procedure was performed using a dedicated software which allowed a 3D following of the sulci course on the edited brain. Regions of interest were then drawn manually with the same software every 2 mm on the axial slices of the high-resolution MNI single subject. The 90 AVOI were reconstructed and assigned a label. Using this parcellation method, three procedures to perform the automated anatomical labeling of functional studies are proposed: (1) labeling of an extremum defined by a set of coordinates, (2) percentage of voxels belonging to each of the AVOI intersected by a sphere centered by a set of coordinates, and (3) percentage of voxels belonging to each of the AVOI intersected by an activated cluster. An interface with the Statistical Parametric Mapping package (SPM, J. Ashburner and K. J. Friston, 1999, Hum. Brain Mapp. 7, 254-266) is provided as a freeware to researchers of the neuroimaging community. We believe that this tool is an improvement for the macroscopical labeling of activated area compared to labeling assessed using the Talairach atlas brain in which deformations are well known. However, this tool does not alleviate the need for more sophisticated labeling strategies based on anatomical or cytoarchitectonic probabilistic maps.
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            International consensus diagnostic criteria for neuromyelitis optica spectrum disorders

            Neuromyelitis optica (NMO) is an inflammatory CNS syndrome distinct from multiple sclerosis (MS) that is associated with serum aquaporin-4 immunoglobulin G antibodies (AQP4-IgG). Prior NMO diagnostic criteria required optic nerve and spinal cord involvement but more restricted or more extensive CNS involvement may occur. The International Panel for NMO Diagnosis (IPND) was convened to develop revised diagnostic criteria using systematic literature reviews and electronic surveys to facilitate consensus. The new nomenclature defines the unifying term NMO spectrum disorders (NMOSD), which is stratified further by serologic testing (NMOSD with or without AQP4-IgG). The core clinical characteristics required for patients with NMOSD with AQP4-IgG include clinical syndromes or MRI findings related to optic nerve, spinal cord, area postrema, other brainstem, diencephalic, or cerebral presentations. More stringent clinical criteria, with additional neuroimaging findings, are required for diagnosis of NMOSD without AQP4-IgG or when serologic testing is unavailable. The IPND also proposed validation strategies and achieved consensus on pediatric NMOSD diagnosis and the concepts of monophasic NMOSD and opticospinal MS.
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              GRETNA: a graph theoretical network analysis toolbox for imaging connectomics

              Recent studies have suggested that the brain’s structural and functional networks (i.e., connectomics) can be constructed by various imaging technologies (e.g., EEG/MEG; structural, diffusion and functional MRI) and further characterized by graph theory. Given the huge complexity of network construction, analysis and statistics, toolboxes incorporating these functions are largely lacking. Here, we developed the GRaph thEoreTical Network Analysis (GRETNA) toolbox for imaging connectomics. The GRETNA contains several key features as follows: (i) an open-source, Matlab-based, cross-platform (Windows and UNIX OS) package with a graphical user interface (GUI); (ii) allowing topological analyses of global and local network properties with parallel computing ability, independent of imaging modality and species; (iii) providing flexible manipulations in several key steps during network construction and analysis, which include network node definition, network connectivity processing, network type selection and choice of thresholding procedure; (iv) allowing statistical comparisons of global, nodal and connectional network metrics and assessments of relationship between these network metrics and clinical or behavioral variables of interest; and (v) including functionality in image preprocessing and network construction based on resting-state functional MRI (R-fMRI) data. After applying the GRETNA to a publicly released R-fMRI dataset of 54 healthy young adults, we demonstrated that human brain functional networks exhibit efficient small-world, assortative, hierarchical and modular organizations and possess highly connected hubs and that these findings are robust against different analytical strategies. With these efforts, we anticipate that GRETNA will accelerate imaging connectomics in an easy, quick and flexible manner. GRETNA is freely available on the NITRC website. 1
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                Author and article information

                Contributors
                URI : https://loop.frontiersin.org/people/2589069Role: Role: Role: Role: Role:
                URI : https://loop.frontiersin.org/people/2643548Role: Role: Role: Role:
                URI : https://loop.frontiersin.org/people/2171771Role: Role: Role:
                URI : https://loop.frontiersin.org/people/2387285Role: Role: Role:
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                Journal
                Front Immunol
                Front Immunol
                Front. Immunol.
                Frontiers in Immunology
                Frontiers Media S.A.
                1664-3224
                05 February 2024
                2024
                : 15
                : 1345843
                Affiliations
                [1] 1 Department of Radiology, The First Affiliated Hospital, Jiangxi Medical College, Nanchang University , Nanchang, China
                [2] 2 Queen Mary College, Nanchang University , Nanchang, China
                [3] 3 Department of Biomedical Engineering, College of Engineering, Peking University , Beijing, China
                [4] 4 Spin Imaging Technology Co., Ltd , Nanjing, China
                [5] 5 Neuroimaging Laboratory, Jiangxi Medical Imaging Research Institute , Nanchang, China
                Author notes

                Edited by: Cong-Cong Wang, Shandong Provincial Qianfoshan Hospital, China

                Reviewed by: Adil Maarouf, Assistance Publique Hôpitaux de Marseille, France

                Shengjun Wang, Shandong University, China

                *Correspondence: Fuqing Zhou, ndyfy02301@ 123456ncu.edu.cn

                †These authors have contributed equally to this work and share first authorship

                Article
                10.3389/fimmu.2024.1345843
                10875087
                38375481
                76afd726-9c1e-4488-99b0-bad5173ad534
                Copyright © 2024 Ma, Zhu, Liang, Wu, Wang, Li, Qian, Cheung and Zhou

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 28 November 2023
                : 15 January 2024
                Page count
                Figures: 6, Tables: 2, Equations: 0, References: 41, Pages: 12, Words: 5393
                Funding
                The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This study was supported by the National Natural Science Foundation of China (82160331, 81771808), Jiangxi Province Double Thousand Talent Plan (jxsq2023201039), and the Innovation and Entrepreneurship Training Program for College Students of Jiangxi province (202310403075). This project is implemented by the Jiangxi Clinical Research Center for Medical Imaging (20223BCG74001).
                Categories
                Immunology
                Original Research
                Custom metadata
                Multiple Sclerosis and Neuroimmunology

                Immunology
                brain connectomics,neuromyelitis optica spectrum disorder,individual morphological brain network,functional brain networks,topological properties

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