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Electromyography Biomarkers for Quantifying the Intraoperative Efficacy of Deep Brain Stimulation in Parkinson's Patients With Resting Tremor

Introduction: Deep brain stimulation (DBS) is an effective therapy for resting tremor in Parkinson's disease (PD). However, quick and objective biomarkers for quantifying the efficacy of DBS intraoperatively are lacking. Therefore, we aimed to study how DBS modulates the intraoperative neuromus...

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Autores principales: Wang, Kai-Liang, Burns, Mathew, Xu, Dan, Hu, Wei, Fan, Shi-Ying, Han, Chun-Lei, Wang, Qiao, Michitomo, Shimabukuro, Xia, Xiao-Tong, Zhang, Jian-Guo, Wang, Feng, Meng, Fan-Gang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7054231/
https://www.ncbi.nlm.nih.gov/pubmed/32161571
http://dx.doi.org/10.3389/fneur.2020.00142
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author Wang, Kai-Liang
Burns, Mathew
Xu, Dan
Hu, Wei
Fan, Shi-Ying
Han, Chun-Lei
Wang, Qiao
Michitomo, Shimabukuro
Xia, Xiao-Tong
Zhang, Jian-Guo
Wang, Feng
Meng, Fan-Gang
author_facet Wang, Kai-Liang
Burns, Mathew
Xu, Dan
Hu, Wei
Fan, Shi-Ying
Han, Chun-Lei
Wang, Qiao
Michitomo, Shimabukuro
Xia, Xiao-Tong
Zhang, Jian-Guo
Wang, Feng
Meng, Fan-Gang
author_sort Wang, Kai-Liang
collection PubMed
description Introduction: Deep brain stimulation (DBS) is an effective therapy for resting tremor in Parkinson's disease (PD). However, quick and objective biomarkers for quantifying the efficacy of DBS intraoperatively are lacking. Therefore, we aimed to study how DBS modulates the intraoperative neuromuscular pattern of resting tremor in PD patients and to find predictive surface electromyography (sEMG) biomarkers for quantifying the intraoperative efficacy of DBS. Methods: Intraoperative sEMG of 39 PD patients with resting tremor was measured with the DBS on and off, respectively, during the intraoperative DBS testing stage. Twelve signal features (time and frequency domains) were extracted from the intraoperative sEMG data. These sEMG features were associated with the clinical outcome to evaluate the efficacy of intraoperative DBS. Also, an sEMG-based prediction model was established to predict the clinical improvement rate (IR) of resting tremor with DBS therapy. Results: A typical resting tremor with a peak frequency of 4.93 ± 0.98 Hz (mean ± SD) was measured. Compared to the baseline, DBS modulated significant neuromuscular pattern changes in most features except for the peak frequency, by decreasing the motor unit firing rate, amplitude, or power and by changing the regularity pattern. Three sEMG features were detected with significant associations with the clinical improvement rate (IR) of the tremor scale: peak frequency power (R = 0.37, p = 0.03), weighted root mean square (R = 0.42, p = 0.01), and modified mean amplitude power (R = 0.48, p = 0.003). These were adopted to train a Gaussian process regression model with a leave-one-out cross-validation procedure. The prediction values from the trained sEMG prediction model (1,000 permutations, p = 0.003) showed a good correlation (r = 0.47, p = 0.0043) with the true IR of the tremor scale. Conclusion: DBS acutely modulated the intraoperative resting tremor, mainly by suppressing the amplitude and motor unit firing rate and by changing the regularity pattern, but not by modifying the frequency pattern. Three features showed strong robustness and could be used as quick intraoperative biomarkers to quantify and predict the efficacy of DBS in PD patients with resting tremor.
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spelling pubmed-70542312020-03-11 Electromyography Biomarkers for Quantifying the Intraoperative Efficacy of Deep Brain Stimulation in Parkinson's Patients With Resting Tremor Wang, Kai-Liang Burns, Mathew Xu, Dan Hu, Wei Fan, Shi-Ying Han, Chun-Lei Wang, Qiao Michitomo, Shimabukuro Xia, Xiao-Tong Zhang, Jian-Guo Wang, Feng Meng, Fan-Gang Front Neurol Neurology Introduction: Deep brain stimulation (DBS) is an effective therapy for resting tremor in Parkinson's disease (PD). However, quick and objective biomarkers for quantifying the efficacy of DBS intraoperatively are lacking. Therefore, we aimed to study how DBS modulates the intraoperative neuromuscular pattern of resting tremor in PD patients and to find predictive surface electromyography (sEMG) biomarkers for quantifying the intraoperative efficacy of DBS. Methods: Intraoperative sEMG of 39 PD patients with resting tremor was measured with the DBS on and off, respectively, during the intraoperative DBS testing stage. Twelve signal features (time and frequency domains) were extracted from the intraoperative sEMG data. These sEMG features were associated with the clinical outcome to evaluate the efficacy of intraoperative DBS. Also, an sEMG-based prediction model was established to predict the clinical improvement rate (IR) of resting tremor with DBS therapy. Results: A typical resting tremor with a peak frequency of 4.93 ± 0.98 Hz (mean ± SD) was measured. Compared to the baseline, DBS modulated significant neuromuscular pattern changes in most features except for the peak frequency, by decreasing the motor unit firing rate, amplitude, or power and by changing the regularity pattern. Three sEMG features were detected with significant associations with the clinical improvement rate (IR) of the tremor scale: peak frequency power (R = 0.37, p = 0.03), weighted root mean square (R = 0.42, p = 0.01), and modified mean amplitude power (R = 0.48, p = 0.003). These were adopted to train a Gaussian process regression model with a leave-one-out cross-validation procedure. The prediction values from the trained sEMG prediction model (1,000 permutations, p = 0.003) showed a good correlation (r = 0.47, p = 0.0043) with the true IR of the tremor scale. Conclusion: DBS acutely modulated the intraoperative resting tremor, mainly by suppressing the amplitude and motor unit firing rate and by changing the regularity pattern, but not by modifying the frequency pattern. Three features showed strong robustness and could be used as quick intraoperative biomarkers to quantify and predict the efficacy of DBS in PD patients with resting tremor. Frontiers Media S.A. 2020-02-26 /pmc/articles/PMC7054231/ /pubmed/32161571 http://dx.doi.org/10.3389/fneur.2020.00142 Text en Copyright © 2020 Wang, Burns, Xu, Hu, Fan, Han, Wang, Michitomo, Xia, Zhang, Wang and Meng. 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 Neurology
Wang, Kai-Liang
Burns, Mathew
Xu, Dan
Hu, Wei
Fan, Shi-Ying
Han, Chun-Lei
Wang, Qiao
Michitomo, Shimabukuro
Xia, Xiao-Tong
Zhang, Jian-Guo
Wang, Feng
Meng, Fan-Gang
Electromyography Biomarkers for Quantifying the Intraoperative Efficacy of Deep Brain Stimulation in Parkinson's Patients With Resting Tremor
title Electromyography Biomarkers for Quantifying the Intraoperative Efficacy of Deep Brain Stimulation in Parkinson's Patients With Resting Tremor
title_full Electromyography Biomarkers for Quantifying the Intraoperative Efficacy of Deep Brain Stimulation in Parkinson's Patients With Resting Tremor
title_fullStr Electromyography Biomarkers for Quantifying the Intraoperative Efficacy of Deep Brain Stimulation in Parkinson's Patients With Resting Tremor
title_full_unstemmed Electromyography Biomarkers for Quantifying the Intraoperative Efficacy of Deep Brain Stimulation in Parkinson's Patients With Resting Tremor
title_short Electromyography Biomarkers for Quantifying the Intraoperative Efficacy of Deep Brain Stimulation in Parkinson's Patients With Resting Tremor
title_sort electromyography biomarkers for quantifying the intraoperative efficacy of deep brain stimulation in parkinson's patients with resting tremor
topic Neurology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7054231/
https://www.ncbi.nlm.nih.gov/pubmed/32161571
http://dx.doi.org/10.3389/fneur.2020.00142
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