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Abnormal topological organization in systemic lupus erythematosus: a resting-state functional magnetic resonance imaging analysis

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Abstract

Using resting-state functional magnetic resonance imaging and graph theory approaches to investigate the topological characteristics of functional networks and their potential correlations with clinical information in patients with systemic lupus erythematosus (SLE). A total of 41 patients and 35 volunteers were consecutively recruited. Detailed clinical data of all participants were recorded. All participants underwent a resting-state functional magnetic resonance imaging examination. Functional networks were constructed by a Pearson correlation matrix of 116 brain regions. The topological properties were analyzed by graph theory. Parametric tests were used to compare the topological properties between the groups. Partial correlation analysis was used to identify relationships between the abnormal topological properties and the clinical data. The nodal network metrics were abnormal in the SLE patients compared to the controls. Decreased nodal efficiency was identified in the right insula, bilateral putamen, and bilateral Heschl’s gyrus in the SLE patients. Decreased degree centrality was also found in the right amygdala and bilateral Heschl’s gyrus. In addition, the SLE patients showed decreased network functional connectivity (FC) between several regions, particularly between the basal ganglia and the cerebellum. Moreover, FC values between the right putamen and vermis 6 were positively correlated with Mini-Mental State Examination scores. The nodal efficiency and the degree centrality values in the left Heschl’s gyrus were both positively correlated with the course of the disease. The topological structure of the functional network was apparently abnormal in SLE patients. FC values between the right putamen and vermis 6 may serve as a neuroimaging marker for evaluating the progressive cognitive decline in SLE patients. Decreased synergy between the basal ganglia region and the cerebellum in the extrapyramidal system may be one cause of cognitive dysfunction in SLE patients.

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Abbreviations

FC:

functional connectivity

FDR:

False Discovery Rate

fMRI:

functional magnetic resonance imaging

HC:

healthy control

MMSE:

Mini-Mental State Examination

NAA:

N-acetylaspartate

Gamma:

normalized clustering coefficient

Lambda:

normalized characteristic path length

NPSLE:

neuropsychiatric systemic lupus erythematosus

SLE:

Systemic lupus erythematosus

Sigma:

small-worldness

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Funding

This study has received funding by National Natural Science Foundation of China (NSFC81571652); Science and technology project of Yangzhou (YZ2018059); “333 Project” of Jiangsu Province (BRA2017154). Yangzhou City Science and Education Strengthening Key Talents Project (ZDRC201873).

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Correspondence to Jing-Tao Wu.

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All authors declare that they have no conflict of interest.

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All the procedures involving human subjects were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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We confirm that informed consent was obtained from all the participants included in this study.

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Cao, ZY., Wang, N., Jia, JT. et al. Abnormal topological organization in systemic lupus erythematosus: a resting-state functional magnetic resonance imaging analysis. Brain Imaging and Behavior 15, 14–24 (2021). https://doi.org/10.1007/s11682-019-00228-y

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