Interaction of systemic oxidative stress and mesial temporal network degeneration in Parkinson’s disease with and without cognitive impairment

Abstract Background To identify the vulnerable areas associated with systemic oxidative stress and further disruption of these vulnerable areas by measuring the associated morphology and functional network alterations in Parkinson’s disease (PD) patients with and without cognitive impairment. Method...

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Main Authors: Pi-Ling Chiang, Hsiu-Ling Chen, Cheng-Hsien Lu, Yueh-Sheng Chen, Kun-Hsien Chou, Tun-Wei Hsu, Meng-Hsiang Chen, Nai-Wen Tsai, Shau-Hsuan Li, Wei-Che Lin
Format: Article
Language:English
Published: BMC 2018-09-01
Series:Journal of Neuroinflammation
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12974-018-1317-z
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spelling doaj-92f99e81733d40439637e1ab1ffff37a2020-11-24T21:45:55ZengBMCJournal of Neuroinflammation1742-20942018-09-0115111110.1186/s12974-018-1317-zInteraction of systemic oxidative stress and mesial temporal network degeneration in Parkinson’s disease with and without cognitive impairmentPi-Ling Chiang0Hsiu-Ling Chen1Cheng-Hsien Lu2Yueh-Sheng Chen3Kun-Hsien Chou4Tun-Wei Hsu5Meng-Hsiang Chen6Nai-Wen Tsai7Shau-Hsuan Li8Wei-Che Lin9Department of Diagnostic Radiology, Kaohsiung Chang Gung Memorial Hospital, Chang Gung University College of MedicineDepartment of Diagnostic Radiology, Kaohsiung Chang Gung Memorial Hospital, Chang Gung University College of MedicineDepartment of Neurology, Kaohsiung Chang Gung Memorial Hospital, Chang Gung University College of MedicineDepartment of Diagnostic Radiology, Kaohsiung Chang Gung Memorial Hospital, Chang Gung University College of MedicineBrain Research Center, National Yang-Ming UniversityDepartment of Radiology, Taipei Veterans General HospitalDepartment of Diagnostic Radiology, Kaohsiung Chang Gung Memorial Hospital, Chang Gung University College of MedicineDepartment of Neurology, Kaohsiung Chang Gung Memorial Hospital, Chang Gung University College of MedicineDepartment of Hematology and Oncology, Kaohsiung Chang Gung Memorial Hospital, Chang Gung University College of MedicineDepartment of Diagnostic Radiology, Kaohsiung Chang Gung Memorial Hospital, Chang Gung University College of MedicineAbstract Background To identify the vulnerable areas associated with systemic oxidative stress and further disruption of these vulnerable areas by measuring the associated morphology and functional network alterations in Parkinson’s disease (PD) patients with and without cognitive impairment. Methods This prospective study was approved by the institutional review board of KCGMH, and written informed consent was obtained. Between December 2010 and May 2015, 41 PD patients with different levels of cognitive functions and 29 healthy volunteers underwent peripheral blood sampling to quantify systemic oxidative stress, as well as T1W volumetric and resting state functional MRI (rs-fMRI) scans. Rs-fMRI was used to derive the healthy intrinsic connectivity patterns seeded by the vulnerable areas associated with any of the significant oxidative stress markers. The two groups were compared in terms of the functional connectivity correlation coefficient (fc-CC) and gray matter volume (GMV) of the network seeded by the vulnerable areas. Results The levels of oxidative stress markers, including leukocyte apoptosis and adhesion molecules, were significantly higher in the PD group. Using whole-brain VBM-based correlation analysis, the bilateral mesial temporal lobes (MTLs) were identified as the most vulnerable areas associated with lymphocyte apoptosis (P < 0.005). We found that the MTL network of healthy subjects resembled the PD-associated atrophy pattern. Furthermore, reduced fc-CC and GMV were further associated with the aggravated cognitive impairment. Conclusion The MTLs are the vulnerable areas associated with peripheral lymphocyte infiltration, and disruptions of the MTL functional network in both architecture and functional connectivity might result in cognitive impairments in Parkinson’s disease.http://link.springer.com/article/10.1186/s12974-018-1317-zParkinson’s diseaseSystemic oxidative stressLymphocyte apoptosisMesial temporal networkGray matter volumeFunctional connectivity
collection DOAJ
language English
format Article
sources DOAJ
author Pi-Ling Chiang
Hsiu-Ling Chen
Cheng-Hsien Lu
Yueh-Sheng Chen
Kun-Hsien Chou
Tun-Wei Hsu
Meng-Hsiang Chen
Nai-Wen Tsai
Shau-Hsuan Li
Wei-Che Lin
spellingShingle Pi-Ling Chiang
Hsiu-Ling Chen
Cheng-Hsien Lu
Yueh-Sheng Chen
Kun-Hsien Chou
Tun-Wei Hsu
Meng-Hsiang Chen
Nai-Wen Tsai
Shau-Hsuan Li
Wei-Che Lin
Interaction of systemic oxidative stress and mesial temporal network degeneration in Parkinson’s disease with and without cognitive impairment
Journal of Neuroinflammation
Parkinson’s disease
Systemic oxidative stress
Lymphocyte apoptosis
Mesial temporal network
Gray matter volume
Functional connectivity
author_facet Pi-Ling Chiang
Hsiu-Ling Chen
Cheng-Hsien Lu
Yueh-Sheng Chen
Kun-Hsien Chou
Tun-Wei Hsu
Meng-Hsiang Chen
Nai-Wen Tsai
Shau-Hsuan Li
Wei-Che Lin
author_sort Pi-Ling Chiang
title Interaction of systemic oxidative stress and mesial temporal network degeneration in Parkinson’s disease with and without cognitive impairment
title_short Interaction of systemic oxidative stress and mesial temporal network degeneration in Parkinson’s disease with and without cognitive impairment
title_full Interaction of systemic oxidative stress and mesial temporal network degeneration in Parkinson’s disease with and without cognitive impairment
title_fullStr Interaction of systemic oxidative stress and mesial temporal network degeneration in Parkinson’s disease with and without cognitive impairment
title_full_unstemmed Interaction of systemic oxidative stress and mesial temporal network degeneration in Parkinson’s disease with and without cognitive impairment
title_sort interaction of systemic oxidative stress and mesial temporal network degeneration in parkinson’s disease with and without cognitive impairment
publisher BMC
series Journal of Neuroinflammation
issn 1742-2094
publishDate 2018-09-01
description Abstract Background To identify the vulnerable areas associated with systemic oxidative stress and further disruption of these vulnerable areas by measuring the associated morphology and functional network alterations in Parkinson’s disease (PD) patients with and without cognitive impairment. Methods This prospective study was approved by the institutional review board of KCGMH, and written informed consent was obtained. Between December 2010 and May 2015, 41 PD patients with different levels of cognitive functions and 29 healthy volunteers underwent peripheral blood sampling to quantify systemic oxidative stress, as well as T1W volumetric and resting state functional MRI (rs-fMRI) scans. Rs-fMRI was used to derive the healthy intrinsic connectivity patterns seeded by the vulnerable areas associated with any of the significant oxidative stress markers. The two groups were compared in terms of the functional connectivity correlation coefficient (fc-CC) and gray matter volume (GMV) of the network seeded by the vulnerable areas. Results The levels of oxidative stress markers, including leukocyte apoptosis and adhesion molecules, were significantly higher in the PD group. Using whole-brain VBM-based correlation analysis, the bilateral mesial temporal lobes (MTLs) were identified as the most vulnerable areas associated with lymphocyte apoptosis (P < 0.005). We found that the MTL network of healthy subjects resembled the PD-associated atrophy pattern. Furthermore, reduced fc-CC and GMV were further associated with the aggravated cognitive impairment. Conclusion The MTLs are the vulnerable areas associated with peripheral lymphocyte infiltration, and disruptions of the MTL functional network in both architecture and functional connectivity might result in cognitive impairments in Parkinson’s disease.
topic Parkinson’s disease
Systemic oxidative stress
Lymphocyte apoptosis
Mesial temporal network
Gray matter volume
Functional connectivity
url http://link.springer.com/article/10.1186/s12974-018-1317-z
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