Cargando…

The different damage patterns of short-, middle- and long-range connections between patients with relapse-remitting multiple sclerosis and neuromyelitis optica spectrum disorder

OBJECTIVE: To investigate the differences in short-, middle- and long-range connections between patients with relapse-remitting multiple sclerosis (RRMS) and neuromyelitis optica spectrum disorder (NMOSD), and their correlation with brain tissue volume, structural and functional network parameters....

Descripción completa

Detalles Bibliográficos
Autores principales: Chen, Xiaoya, Peng, Yuling, Zheng, Qiao, Luo, Dan, Han, Yongliang, Luo, Qi, Zhu, Qiyuan, Luo, Tianyou, Li, Yongmei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9755727/
https://www.ncbi.nlm.nih.gov/pubmed/36532033
http://dx.doi.org/10.3389/fimmu.2022.1007335
_version_ 1784851481155862528
author Chen, Xiaoya
Peng, Yuling
Zheng, Qiao
Luo, Dan
Han, Yongliang
Luo, Qi
Zhu, Qiyuan
Luo, Tianyou
Li, Yongmei
author_facet Chen, Xiaoya
Peng, Yuling
Zheng, Qiao
Luo, Dan
Han, Yongliang
Luo, Qi
Zhu, Qiyuan
Luo, Tianyou
Li, Yongmei
author_sort Chen, Xiaoya
collection PubMed
description OBJECTIVE: To investigate the differences in short-, middle- and long-range connections between patients with relapse-remitting multiple sclerosis (RRMS) and neuromyelitis optica spectrum disorder (NMOSD), and their correlation with brain tissue volume, structural and functional network parameters. METHODS: A total of 51 RRMS, 42 NMOSD and 56 health controls (HC) were recruited. Of these 25 RRMS (median: 1.37 years) and 20 NMOSD (median: 1.25 years) patients were also studied at follow-up. The whole-brain fiber connection was divided into three groups according to the trisected lengths of the tract in HC group, including short-, middle- and long-range connections. The brain tissue features (including total brain tissue and deep grey matter volumes) and parameters of DTI and functional networks (including the shortest path, clustering coefficient, local efficiency and global efficiency) were calculated. The differences in fiber number (FN) and average fractional anisotropy (FA) were compared between RRMS and NMOSD by the One-way ANOVA and post hoc tests. The correlation between the FN or FA and the brain tissue volume, DTI and functional network parameters were further analyzed by Pearson analysis. RESULTS: Compared to HC and NMOSD, the total number of fibers in RRMS was decreased, including the reduced FN of middle- and long-range connections, but increased FN of short-range connections. Compared to HC, the FA of three fibers in RRMS and NMOSD were reduced significantly, and the decrease of FA in RRMS was greater than in NMOSD. There were correlations between the FN of short-, and long-range connections and the atrophy of whole brain tissue in two diseases and structural network topological parameters in RRMS. Additionally, there was no significant difference of FN and FA in short-, middle- and long-range connections between the baseline and follow-up in two diseases. CONCLUSIONS: RRMS and NMOSD patients have different patterns of fiber connection damage. The FN of different lengths in RRMS and NMOSD patients may be associated with brain atrophy. The FN and FA of different lengths may explain the decreased efficiency of the structural network in RRMS patients. In the short-term follow-up, neither has worsened damage of different fibers in two diseases.
format Online
Article
Text
id pubmed-9755727
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-97557272022-12-17 The different damage patterns of short-, middle- and long-range connections between patients with relapse-remitting multiple sclerosis and neuromyelitis optica spectrum disorder Chen, Xiaoya Peng, Yuling Zheng, Qiao Luo, Dan Han, Yongliang Luo, Qi Zhu, Qiyuan Luo, Tianyou Li, Yongmei Front Immunol Immunology OBJECTIVE: To investigate the differences in short-, middle- and long-range connections between patients with relapse-remitting multiple sclerosis (RRMS) and neuromyelitis optica spectrum disorder (NMOSD), and their correlation with brain tissue volume, structural and functional network parameters. METHODS: A total of 51 RRMS, 42 NMOSD and 56 health controls (HC) were recruited. Of these 25 RRMS (median: 1.37 years) and 20 NMOSD (median: 1.25 years) patients were also studied at follow-up. The whole-brain fiber connection was divided into three groups according to the trisected lengths of the tract in HC group, including short-, middle- and long-range connections. The brain tissue features (including total brain tissue and deep grey matter volumes) and parameters of DTI and functional networks (including the shortest path, clustering coefficient, local efficiency and global efficiency) were calculated. The differences in fiber number (FN) and average fractional anisotropy (FA) were compared between RRMS and NMOSD by the One-way ANOVA and post hoc tests. The correlation between the FN or FA and the brain tissue volume, DTI and functional network parameters were further analyzed by Pearson analysis. RESULTS: Compared to HC and NMOSD, the total number of fibers in RRMS was decreased, including the reduced FN of middle- and long-range connections, but increased FN of short-range connections. Compared to HC, the FA of three fibers in RRMS and NMOSD were reduced significantly, and the decrease of FA in RRMS was greater than in NMOSD. There were correlations between the FN of short-, and long-range connections and the atrophy of whole brain tissue in two diseases and structural network topological parameters in RRMS. Additionally, there was no significant difference of FN and FA in short-, middle- and long-range connections between the baseline and follow-up in two diseases. CONCLUSIONS: RRMS and NMOSD patients have different patterns of fiber connection damage. The FN of different lengths in RRMS and NMOSD patients may be associated with brain atrophy. The FN and FA of different lengths may explain the decreased efficiency of the structural network in RRMS patients. In the short-term follow-up, neither has worsened damage of different fibers in two diseases. Frontiers Media S.A. 2022-12-02 /pmc/articles/PMC9755727/ /pubmed/36532033 http://dx.doi.org/10.3389/fimmu.2022.1007335 Text en Copyright © 2022 Chen, Peng, Zheng, Luo, Han, Luo, Zhu, Luo and Li https://creativecommons.org/licenses/by/4.0/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.
spellingShingle Immunology
Chen, Xiaoya
Peng, Yuling
Zheng, Qiao
Luo, Dan
Han, Yongliang
Luo, Qi
Zhu, Qiyuan
Luo, Tianyou
Li, Yongmei
The different damage patterns of short-, middle- and long-range connections between patients with relapse-remitting multiple sclerosis and neuromyelitis optica spectrum disorder
title The different damage patterns of short-, middle- and long-range connections between patients with relapse-remitting multiple sclerosis and neuromyelitis optica spectrum disorder
title_full The different damage patterns of short-, middle- and long-range connections between patients with relapse-remitting multiple sclerosis and neuromyelitis optica spectrum disorder
title_fullStr The different damage patterns of short-, middle- and long-range connections between patients with relapse-remitting multiple sclerosis and neuromyelitis optica spectrum disorder
title_full_unstemmed The different damage patterns of short-, middle- and long-range connections between patients with relapse-remitting multiple sclerosis and neuromyelitis optica spectrum disorder
title_short The different damage patterns of short-, middle- and long-range connections between patients with relapse-remitting multiple sclerosis and neuromyelitis optica spectrum disorder
title_sort different damage patterns of short-, middle- and long-range connections between patients with relapse-remitting multiple sclerosis and neuromyelitis optica spectrum disorder
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9755727/
https://www.ncbi.nlm.nih.gov/pubmed/36532033
http://dx.doi.org/10.3389/fimmu.2022.1007335
work_keys_str_mv AT chenxiaoya thedifferentdamagepatternsofshortmiddleandlongrangeconnectionsbetweenpatientswithrelapseremittingmultiplesclerosisandneuromyelitisopticaspectrumdisorder
AT pengyuling thedifferentdamagepatternsofshortmiddleandlongrangeconnectionsbetweenpatientswithrelapseremittingmultiplesclerosisandneuromyelitisopticaspectrumdisorder
AT zhengqiao thedifferentdamagepatternsofshortmiddleandlongrangeconnectionsbetweenpatientswithrelapseremittingmultiplesclerosisandneuromyelitisopticaspectrumdisorder
AT luodan thedifferentdamagepatternsofshortmiddleandlongrangeconnectionsbetweenpatientswithrelapseremittingmultiplesclerosisandneuromyelitisopticaspectrumdisorder
AT hanyongliang thedifferentdamagepatternsofshortmiddleandlongrangeconnectionsbetweenpatientswithrelapseremittingmultiplesclerosisandneuromyelitisopticaspectrumdisorder
AT luoqi thedifferentdamagepatternsofshortmiddleandlongrangeconnectionsbetweenpatientswithrelapseremittingmultiplesclerosisandneuromyelitisopticaspectrumdisorder
AT zhuqiyuan thedifferentdamagepatternsofshortmiddleandlongrangeconnectionsbetweenpatientswithrelapseremittingmultiplesclerosisandneuromyelitisopticaspectrumdisorder
AT luotianyou thedifferentdamagepatternsofshortmiddleandlongrangeconnectionsbetweenpatientswithrelapseremittingmultiplesclerosisandneuromyelitisopticaspectrumdisorder
AT liyongmei thedifferentdamagepatternsofshortmiddleandlongrangeconnectionsbetweenpatientswithrelapseremittingmultiplesclerosisandneuromyelitisopticaspectrumdisorder
AT chenxiaoya differentdamagepatternsofshortmiddleandlongrangeconnectionsbetweenpatientswithrelapseremittingmultiplesclerosisandneuromyelitisopticaspectrumdisorder
AT pengyuling differentdamagepatternsofshortmiddleandlongrangeconnectionsbetweenpatientswithrelapseremittingmultiplesclerosisandneuromyelitisopticaspectrumdisorder
AT zhengqiao differentdamagepatternsofshortmiddleandlongrangeconnectionsbetweenpatientswithrelapseremittingmultiplesclerosisandneuromyelitisopticaspectrumdisorder
AT luodan differentdamagepatternsofshortmiddleandlongrangeconnectionsbetweenpatientswithrelapseremittingmultiplesclerosisandneuromyelitisopticaspectrumdisorder
AT hanyongliang differentdamagepatternsofshortmiddleandlongrangeconnectionsbetweenpatientswithrelapseremittingmultiplesclerosisandneuromyelitisopticaspectrumdisorder
AT luoqi differentdamagepatternsofshortmiddleandlongrangeconnectionsbetweenpatientswithrelapseremittingmultiplesclerosisandneuromyelitisopticaspectrumdisorder
AT zhuqiyuan differentdamagepatternsofshortmiddleandlongrangeconnectionsbetweenpatientswithrelapseremittingmultiplesclerosisandneuromyelitisopticaspectrumdisorder
AT luotianyou differentdamagepatternsofshortmiddleandlongrangeconnectionsbetweenpatientswithrelapseremittingmultiplesclerosisandneuromyelitisopticaspectrumdisorder
AT liyongmei differentdamagepatternsofshortmiddleandlongrangeconnectionsbetweenpatientswithrelapseremittingmultiplesclerosisandneuromyelitisopticaspectrumdisorder