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Increased Peripheral Interleukin 10 Relate to White Matter Integrity in Schizophrenia

Background: Schizophrenia is characterized by the disruption of microstructural white matter (WM) integrity, while the pathogenesis remains unclear. Inflammation has been associated with the WM pathology in schizophrenia. Interleukin 10 (IL-10) has been proven to be related to schizophrenia in both...

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Autores principales: Fu, Gui, Zhang, Wenjing, Dai, Jing, Liu, Jieke, Li, Fei, Wu, Dongsheng, Xiao, Yuan, Shah, Chandan, Sweeney, John A., Wu, Min, Lui, Su
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6374337/
https://www.ncbi.nlm.nih.gov/pubmed/30792621
http://dx.doi.org/10.3389/fnins.2019.00052
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author Fu, Gui
Zhang, Wenjing
Dai, Jing
Liu, Jieke
Li, Fei
Wu, Dongsheng
Xiao, Yuan
Shah, Chandan
Sweeney, John A.
Wu, Min
Lui, Su
author_facet Fu, Gui
Zhang, Wenjing
Dai, Jing
Liu, Jieke
Li, Fei
Wu, Dongsheng
Xiao, Yuan
Shah, Chandan
Sweeney, John A.
Wu, Min
Lui, Su
author_sort Fu, Gui
collection PubMed
description Background: Schizophrenia is characterized by the disruption of microstructural white matter (WM) integrity, while the pathogenesis remains unclear. Inflammation has been associated with the WM pathology in schizophrenia. Interleukin 10 (IL-10) has been proven to be related to schizophrenia in both animal and human models. The aim of this study was to explore whether peripheral IL-10 was associated with microstructural WM integrity in schizophrenia. Methods: A total of 47 patients with schizophrenia (SZ) and 49 healthy controls (HC) underwent diffusion tensor imaging and venous blood sampling. Tract-based spatial statistics was conducted to explore the differences in fractional anisotropy (FA), radial diffusivity (RD), mean diffusivity (MD), and axial diffusivity (AD) between patients and controls. A quantitative chemiluminescence assay was performed to measure peripheral IL-10 levels. General linear regression analysis using a stepwise method was applied to examine the relationship between peripheral IL-10 and diffusion measures. Results: Compared with the HC, peripheral IL-10 levels were higher and a significant reduction of FA and AD, and increase of RD and MD were observed in SZ (corrected p < 0.05). A regression analysis revealed that peripheral IL-10 was negatively correlated with FA in the right posterior thalamic radiation and left inferior fronto-occipital fasciculus, in SZ (β = -0.51, p = 0.01; β = -0.47, p = 0.02, respectively) but not in HC (β = -0.01, p = 0.95; β = -0.003, p = 0.98, respectively), and the differences in regression curves were significant (z = 2.50, p = 0.01; z = 2.37, p = 0.02, respectively). IL-10 was negatively connected with MD in the right parietal arcuate fasciculus (β = -0.40, p = 0.048) and body of the corpus callosum (β = -0.43, p = 0.03) in SZ, while not in HC. The magnitude of correlation in the patient and control group was different (z = 2.48, p = 0.01 and z = 2.61, p < 0.01, respectively). In addition, IL-10 was positively correlated with RD in the right parietal arcuate fasciculus in patients (β = 0.45, p = 0.04) but not in HC (β = 0.26, p = 0.94), but the correlation coefficients were not significant (z = 0.98, p = 0.32). Conclusion: Our findings demonstrated that elevated peripheral IL-10 levels were associated with the disruption of microstructural WM integrity in schizophrenia, supporting the notion that inflammation plays a regulatory role in the pathology of microstructural WM and is associated with schizophrenia.
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spelling pubmed-63743372019-02-21 Increased Peripheral Interleukin 10 Relate to White Matter Integrity in Schizophrenia Fu, Gui Zhang, Wenjing Dai, Jing Liu, Jieke Li, Fei Wu, Dongsheng Xiao, Yuan Shah, Chandan Sweeney, John A. Wu, Min Lui, Su Front Neurosci Neuroscience Background: Schizophrenia is characterized by the disruption of microstructural white matter (WM) integrity, while the pathogenesis remains unclear. Inflammation has been associated with the WM pathology in schizophrenia. Interleukin 10 (IL-10) has been proven to be related to schizophrenia in both animal and human models. The aim of this study was to explore whether peripheral IL-10 was associated with microstructural WM integrity in schizophrenia. Methods: A total of 47 patients with schizophrenia (SZ) and 49 healthy controls (HC) underwent diffusion tensor imaging and venous blood sampling. Tract-based spatial statistics was conducted to explore the differences in fractional anisotropy (FA), radial diffusivity (RD), mean diffusivity (MD), and axial diffusivity (AD) between patients and controls. A quantitative chemiluminescence assay was performed to measure peripheral IL-10 levels. General linear regression analysis using a stepwise method was applied to examine the relationship between peripheral IL-10 and diffusion measures. Results: Compared with the HC, peripheral IL-10 levels were higher and a significant reduction of FA and AD, and increase of RD and MD were observed in SZ (corrected p < 0.05). A regression analysis revealed that peripheral IL-10 was negatively correlated with FA in the right posterior thalamic radiation and left inferior fronto-occipital fasciculus, in SZ (β = -0.51, p = 0.01; β = -0.47, p = 0.02, respectively) but not in HC (β = -0.01, p = 0.95; β = -0.003, p = 0.98, respectively), and the differences in regression curves were significant (z = 2.50, p = 0.01; z = 2.37, p = 0.02, respectively). IL-10 was negatively connected with MD in the right parietal arcuate fasciculus (β = -0.40, p = 0.048) and body of the corpus callosum (β = -0.43, p = 0.03) in SZ, while not in HC. The magnitude of correlation in the patient and control group was different (z = 2.48, p = 0.01 and z = 2.61, p < 0.01, respectively). In addition, IL-10 was positively correlated with RD in the right parietal arcuate fasciculus in patients (β = 0.45, p = 0.04) but not in HC (β = 0.26, p = 0.94), but the correlation coefficients were not significant (z = 0.98, p = 0.32). Conclusion: Our findings demonstrated that elevated peripheral IL-10 levels were associated with the disruption of microstructural WM integrity in schizophrenia, supporting the notion that inflammation plays a regulatory role in the pathology of microstructural WM and is associated with schizophrenia. Frontiers Media S.A. 2019-02-07 /pmc/articles/PMC6374337/ /pubmed/30792621 http://dx.doi.org/10.3389/fnins.2019.00052 Text en Copyright © 2019 Fu, Zhang, Dai, Liu, Li, Wu, Xiao, Shah, Sweeney, Wu and Lui. http://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 Neuroscience
Fu, Gui
Zhang, Wenjing
Dai, Jing
Liu, Jieke
Li, Fei
Wu, Dongsheng
Xiao, Yuan
Shah, Chandan
Sweeney, John A.
Wu, Min
Lui, Su
Increased Peripheral Interleukin 10 Relate to White Matter Integrity in Schizophrenia
title Increased Peripheral Interleukin 10 Relate to White Matter Integrity in Schizophrenia
title_full Increased Peripheral Interleukin 10 Relate to White Matter Integrity in Schizophrenia
title_fullStr Increased Peripheral Interleukin 10 Relate to White Matter Integrity in Schizophrenia
title_full_unstemmed Increased Peripheral Interleukin 10 Relate to White Matter Integrity in Schizophrenia
title_short Increased Peripheral Interleukin 10 Relate to White Matter Integrity in Schizophrenia
title_sort increased peripheral interleukin 10 relate to white matter integrity in schizophrenia
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6374337/
https://www.ncbi.nlm.nih.gov/pubmed/30792621
http://dx.doi.org/10.3389/fnins.2019.00052
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