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Research ArticleNeuroimaging Physics/Functional Neuroimaging/CT and MRI Technology

Individual Structural Covariance Network Predicts Long-Term Motor Improvement in Parkinson Disease with Subthalamic Nucleus Deep Brain Stimulation

Yu Diao, Hutao Xie, Yanwen Wang, Baotian Zhao, Anchao Yang and Jianguo Zhang
American Journal of Neuroradiology August 2024, 45 (8) 1106-1115; DOI: https://doi.org/10.3174/ajnr.A8245
Yu Diao
aFrom the Department of Neurosurgery (Y.D., H.X., Y.W., B.Z., A.Y., J.Z.), Beijing Tiantan Hospital, Capital Medical University, Beijing, China
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Hutao Xie
aFrom the Department of Neurosurgery (Y.D., H.X., Y.W., B.Z., A.Y., J.Z.), Beijing Tiantan Hospital, Capital Medical University, Beijing, China
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Yanwen Wang
aFrom the Department of Neurosurgery (Y.D., H.X., Y.W., B.Z., A.Y., J.Z.), Beijing Tiantan Hospital, Capital Medical University, Beijing, China
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Baotian Zhao
aFrom the Department of Neurosurgery (Y.D., H.X., Y.W., B.Z., A.Y., J.Z.), Beijing Tiantan Hospital, Capital Medical University, Beijing, China
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Anchao Yang
aFrom the Department of Neurosurgery (Y.D., H.X., Y.W., B.Z., A.Y., J.Z.), Beijing Tiantan Hospital, Capital Medical University, Beijing, China
bBeijing Key Laboratory of Neurostimulation (A.Y., J.Z.), Beijing, China
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Jianguo Zhang
aFrom the Department of Neurosurgery (Y.D., H.X., Y.W., B.Z., A.Y., J.Z.), Beijing Tiantan Hospital, Capital Medical University, Beijing, China
bBeijing Key Laboratory of Neurostimulation (A.Y., J.Z.), Beijing, China
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Abstract

BACKGROUND AND PURPOSE: The efficacy of long-term chronic subthalamic nucleus deep brain stimulation (STN-DBS) in treating Parkinson disease (PD) exhibits substantial variability among individuals. The preoperative identification of suitable deep brain stimulation (DBS) candidates through predictive means becomes crucial. Our study aims to investigate the predictive value of characterizing individualized structural covariance networks for long-term efficacy of DBS, offering patients a precise and cost-effective preoperative screening tool.

MATERIALS AND METHODS: We included 138 patients with PD and 40 healthy controls. We developed individualized structural covariance networks from T1-weighted images utilizing network template perturbation, and computed the networks’ topological characteristics. Patients were categorized according to their long-term motor improvement following STN-DBS. Intergroup analyses were conducted on individual network edges and topological indices, alongside correlation analyses with long-term outcomes for the entire patient cohort. Finally, machine learning algorithms were employed for regression and classification to predict post-DBS motor improvement.

RESULTS: Among the patients with PD, 6 edges (left middle frontal and left caudate nucleus, right olfactory and right insula, left superior medial frontal gyrus and right insula, right middle frontal and left paracentral lobule, right middle frontal and cerebellum, left lobule VIIb of the cerebellum and the vermis of the cerebellum) exhibited significant results in intergroup comparisons and correlation analyses. Increased degree centrality and local efficiency of the cerebellum, parahippocampal gyrus, and postcentral gyrus were associated with DBS improvement. A regression model constructed from these 6 edges revealed a significant correlation between predicted and observed changes in the unified PD rating scale (R = 0.671, P < .001) and receiver operating characteristic analysis demonstrated an area under the curve of 0.802, effectively distinguishing between patients with good and moderate improvement post-DBS.

CONCLUSIONS: Our findings reveal the link between individual structural covariance network fingerprints in patients with PD and long-term motor outcome following STN-DBS. Additionally, binary and continuous cerebellum–basal ganglia–frontal structural covariance network edges have emerged as potential predictive biomarkers for DBS motor outcome.

ABBREVIATIONS:

AUC
area under the curve
Berg
Berg Balance Scale
DBS
deep brain stimulation
FDR
false discovery rate
FOG-Q
Freezing of Gait Questionnaire
GIG
good improvement group
HAMA
Hamilton Anxiety Rating Scale
HAMD
Hamilton Depression Rating Scale
HC
health control
ISCN
individualized structural covariance networks
IDSCN
individual differential structural covariance network
LCT
levodopa challenge test
MDS-UPDRS
Movement Disorder Society–sponsored Unified Parkinson’s Disease Rating Scale
Med-OFF
off-medication
Med-ON
on-medication
MIG
moderate improvement group
ML
machine learning
MoCA
Montreal Cognitive Assessment
MSE
mean squared error
NTP
network template perturbation
PCL
paracentral lobule
PD
Parkinson disease
ROC
receiver operating characteristic
STN-DBS
deep brain stimulation of the subthalmic nucleus
Stim-ON
stimulation-on
SCN
structural covariance network
TIV
total intracranial volume
  • © 2024 by American Journal of Neuroradiology
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American Journal of Neuroradiology: 45 (8)
American Journal of Neuroradiology
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Cite this article
Yu Diao, Hutao Xie, Yanwen Wang, Baotian Zhao, Anchao Yang, Jianguo Zhang
Individual Structural Covariance Network Predicts Long-Term Motor Improvement in Parkinson Disease with Subthalamic Nucleus Deep Brain Stimulation
American Journal of Neuroradiology Aug 2024, 45 (8) 1106-1115; DOI: 10.3174/ajnr.A8245

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Structural Covariance Network in Parkinson Disease
Yu Diao, Hutao Xie, Yanwen Wang, Baotian Zhao, Anchao Yang, Jianguo Zhang
American Journal of Neuroradiology Aug 2024, 45 (8) 1106-1115; DOI: 10.3174/ajnr.A8245
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