Cortical thickness correlated with peripheral inflammatory cytokines in amyotrophic lateral sclerosis

IntroductionAmyotrophic lateral sclerosis (ALS) is a rare, devastating neurodegenerative disease that affects upper and lower motor neurons, resulting in muscle atrophy, spasticity, hyperreflexia, and paralysis. Inflammation plays an important role in the development of ALS, and associated with rapi...

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Main Authors: Jing Yang, Wenyi Li, Mei Tian, Lei Zhang, Fengping Du, Xin Li, Qi Liu, Rui Li, Zhenzhong Li, Hui Dong, Yaling Liu
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-01-01
Series:Frontiers in Neuroscience
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Online Access:https://www.frontiersin.org/articles/10.3389/fnins.2024.1514554/full
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author Jing Yang
Jing Yang
Jing Yang
Wenyi Li
Wenyi Li
Wenyi Li
Mei Tian
Mei Tian
Mei Tian
Lei Zhang
Fengping Du
Fengping Du
Fengping Du
Xin Li
Xin Li
Xin Li
Qi Liu
Qi Liu
Qi Liu
Rui Li
Rui Li
Rui Li
Zhenzhong Li
Zhenzhong Li
Zhenzhong Li
Hui Dong
Hui Dong
Hui Dong
Yaling Liu
Yaling Liu
Yaling Liu
author_facet Jing Yang
Jing Yang
Jing Yang
Wenyi Li
Wenyi Li
Wenyi Li
Mei Tian
Mei Tian
Mei Tian
Lei Zhang
Fengping Du
Fengping Du
Fengping Du
Xin Li
Xin Li
Xin Li
Qi Liu
Qi Liu
Qi Liu
Rui Li
Rui Li
Rui Li
Zhenzhong Li
Zhenzhong Li
Zhenzhong Li
Hui Dong
Hui Dong
Hui Dong
Yaling Liu
Yaling Liu
Yaling Liu
author_sort Jing Yang
collection DOAJ
description IntroductionAmyotrophic lateral sclerosis (ALS) is a rare, devastating neurodegenerative disease that affects upper and lower motor neurons, resulting in muscle atrophy, spasticity, hyperreflexia, and paralysis. Inflammation plays an important role in the development of ALS, and associated with rapid disease progression. Current observational studies indicate the thinning of cortical thickness in patients with ALS is associated with rapid disease progression and cognitive changes. However, the effects of inflammatory cytokines on cortical thickness in patients with ALS are unclear. Here, we investigated the relationship between inflammatory cytokines and cortical thickness in patients with ALS.MethodsWe evaluated 51 patients with ALS for inflammatory cytokines including interleukin (IL)-4, interferon (IFN)-α, IL-1β, IL-2, IL-5, IL-12, tumor necrosis factor (TNF)-α, IL-6, IL-10, IL-8, IL-17, and IFN-γ and analyzed the correlation between these indicators and the ALS functional rating scale-revised (ALSFRS-R) score or disease progression rate (ΔFS score). Twenty-six patients with ALS and 26 controls were studied using whole-cortex analysis, and post-hoc analyses were performed to examine the correlation between brain cortical thickness and ALSFRS-R or ΔFS scores.ResultsIL-4, IFN-α, IL-1β, and IL-2 levels were significantly correlated with ALSFRS-R scores, and the IL-2 level was significantly correlated with ΔFS scores. After controlling for age and sex, the ALS group had thinner cortexes in multiple clusters across the brain than the control group. Further analyses revealed that cortical thickness in the right superior temporal and lingual gyrus regions was inversely correlated with ΔFS scores. There was a significant positive correlation between the clusters in the right lingual cortex and IL-2 level.ConclusionThese results suggest cortical thickness was reduced in patients with ALS in motor and non-motor cortical areas. Inflammatory factors (especially IL-2) were correlated with cortical thickness, and both were related to the disease progression rate, suggesting IL-2 plays an important role in ALS.
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series Frontiers in Neuroscience
spelling doaj-art-4a890685b6a74eb993d28daad0764ac62025-01-07T06:42:46ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2025-01-011810.3389/fnins.2024.15145541514554Cortical thickness correlated with peripheral inflammatory cytokines in amyotrophic lateral sclerosisJing Yang0Jing Yang1Jing Yang2Wenyi Li3Wenyi Li4Wenyi Li5Mei Tian6Mei Tian7Mei Tian8Lei Zhang9Fengping Du10Fengping Du11Fengping Du12Xin Li13Xin Li14Xin Li15Qi Liu16Qi Liu17Qi Liu18Rui Li19Rui Li20Rui Li21Zhenzhong Li22Zhenzhong Li23Zhenzhong Li24Hui Dong25Hui Dong26Hui Dong27Yaling Liu28Yaling Liu29Yaling Liu30Department of Neurology, The Second Hospital of Hebei Medical University, Shijiazhuang, Hebei, ChinaThe Key Laboratory of Neurology (Hebei Medical University), Ministry of Education, Shijiazhuang, Hebei, ChinaNeurological Laboratory of Hebei Province, Shijiazhuang, Hebei, ChinaDepartment of Neurology, The Second Hospital of Hebei Medical University, Shijiazhuang, Hebei, ChinaThe Key Laboratory of Neurology (Hebei Medical University), Ministry of Education, Shijiazhuang, Hebei, ChinaNeurological Laboratory of Hebei Province, Shijiazhuang, Hebei, ChinaDepartment of Neurology, The Second Hospital of Hebei Medical University, Shijiazhuang, Hebei, ChinaThe Key Laboratory of Neurology (Hebei Medical University), Ministry of Education, Shijiazhuang, Hebei, ChinaNeurological Laboratory of Hebei Province, Shijiazhuang, Hebei, ChinaDepartment of Emergency, The Second Hospital of Hebei Medical University, Shijiazhuang, Hebei, ChinaDepartment of Neurology, The Second Hospital of Hebei Medical University, Shijiazhuang, Hebei, ChinaThe Key Laboratory of Neurology (Hebei Medical University), Ministry of Education, Shijiazhuang, Hebei, ChinaNeurological Laboratory of Hebei Province, Shijiazhuang, Hebei, ChinaDepartment of Neurology, The Second Hospital of Hebei Medical University, Shijiazhuang, Hebei, ChinaThe Key Laboratory of Neurology (Hebei Medical University), Ministry of Education, Shijiazhuang, Hebei, ChinaNeurological Laboratory of Hebei Province, Shijiazhuang, Hebei, ChinaDepartment of Neurology, The Second Hospital of Hebei Medical University, Shijiazhuang, Hebei, ChinaThe Key Laboratory of Neurology (Hebei Medical University), Ministry of Education, Shijiazhuang, Hebei, ChinaNeurological Laboratory of Hebei Province, Shijiazhuang, Hebei, ChinaDepartment of Neurology, The Second Hospital of Hebei Medical University, Shijiazhuang, Hebei, ChinaThe Key Laboratory of Neurology (Hebei Medical University), Ministry of Education, Shijiazhuang, Hebei, ChinaNeurological Laboratory of Hebei Province, Shijiazhuang, Hebei, ChinaDepartment of Neurology, The Second Hospital of Hebei Medical University, Shijiazhuang, Hebei, ChinaThe Key Laboratory of Neurology (Hebei Medical University), Ministry of Education, Shijiazhuang, Hebei, ChinaNeurological Laboratory of Hebei Province, Shijiazhuang, Hebei, ChinaDepartment of Neurology, The Second Hospital of Hebei Medical University, Shijiazhuang, Hebei, ChinaThe Key Laboratory of Neurology (Hebei Medical University), Ministry of Education, Shijiazhuang, Hebei, ChinaNeurological Laboratory of Hebei Province, Shijiazhuang, Hebei, ChinaDepartment of Neurology, The Second Hospital of Hebei Medical University, Shijiazhuang, Hebei, ChinaThe Key Laboratory of Neurology (Hebei Medical University), Ministry of Education, Shijiazhuang, Hebei, ChinaNeurological Laboratory of Hebei Province, Shijiazhuang, Hebei, ChinaIntroductionAmyotrophic lateral sclerosis (ALS) is a rare, devastating neurodegenerative disease that affects upper and lower motor neurons, resulting in muscle atrophy, spasticity, hyperreflexia, and paralysis. Inflammation plays an important role in the development of ALS, and associated with rapid disease progression. Current observational studies indicate the thinning of cortical thickness in patients with ALS is associated with rapid disease progression and cognitive changes. However, the effects of inflammatory cytokines on cortical thickness in patients with ALS are unclear. Here, we investigated the relationship between inflammatory cytokines and cortical thickness in patients with ALS.MethodsWe evaluated 51 patients with ALS for inflammatory cytokines including interleukin (IL)-4, interferon (IFN)-α, IL-1β, IL-2, IL-5, IL-12, tumor necrosis factor (TNF)-α, IL-6, IL-10, IL-8, IL-17, and IFN-γ and analyzed the correlation between these indicators and the ALS functional rating scale-revised (ALSFRS-R) score or disease progression rate (ΔFS score). Twenty-six patients with ALS and 26 controls were studied using whole-cortex analysis, and post-hoc analyses were performed to examine the correlation between brain cortical thickness and ALSFRS-R or ΔFS scores.ResultsIL-4, IFN-α, IL-1β, and IL-2 levels were significantly correlated with ALSFRS-R scores, and the IL-2 level was significantly correlated with ΔFS scores. After controlling for age and sex, the ALS group had thinner cortexes in multiple clusters across the brain than the control group. Further analyses revealed that cortical thickness in the right superior temporal and lingual gyrus regions was inversely correlated with ΔFS scores. There was a significant positive correlation between the clusters in the right lingual cortex and IL-2 level.ConclusionThese results suggest cortical thickness was reduced in patients with ALS in motor and non-motor cortical areas. Inflammatory factors (especially IL-2) were correlated with cortical thickness, and both were related to the disease progression rate, suggesting IL-2 plays an important role in ALS.https://www.frontiersin.org/articles/10.3389/fnins.2024.1514554/fullamyotrophic lateral sclerosiscortical thicknessdisease progressioninflammatory cytokinesMRI
spellingShingle Jing Yang
Jing Yang
Jing Yang
Wenyi Li
Wenyi Li
Wenyi Li
Mei Tian
Mei Tian
Mei Tian
Lei Zhang
Fengping Du
Fengping Du
Fengping Du
Xin Li
Xin Li
Xin Li
Qi Liu
Qi Liu
Qi Liu
Rui Li
Rui Li
Rui Li
Zhenzhong Li
Zhenzhong Li
Zhenzhong Li
Hui Dong
Hui Dong
Hui Dong
Yaling Liu
Yaling Liu
Yaling Liu
Cortical thickness correlated with peripheral inflammatory cytokines in amyotrophic lateral sclerosis
Frontiers in Neuroscience
amyotrophic lateral sclerosis
cortical thickness
disease progression
inflammatory cytokines
MRI
title Cortical thickness correlated with peripheral inflammatory cytokines in amyotrophic lateral sclerosis
title_full Cortical thickness correlated with peripheral inflammatory cytokines in amyotrophic lateral sclerosis
title_fullStr Cortical thickness correlated with peripheral inflammatory cytokines in amyotrophic lateral sclerosis
title_full_unstemmed Cortical thickness correlated with peripheral inflammatory cytokines in amyotrophic lateral sclerosis
title_short Cortical thickness correlated with peripheral inflammatory cytokines in amyotrophic lateral sclerosis
title_sort cortical thickness correlated with peripheral inflammatory cytokines in amyotrophic lateral sclerosis
topic amyotrophic lateral sclerosis
cortical thickness
disease progression
inflammatory cytokines
MRI
url https://www.frontiersin.org/articles/10.3389/fnins.2024.1514554/full
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