Abstract
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.
Highlights
Deep brain stimulation (DBS) is an effective therapy for resting tremor in Parkinson’s disease (PD)
The purpose of the current study is to investigate how and to what extent the neuromuscular pattern of resting tremor in PD patients could be modulated by intraoperative DBS through measuring surface electromyography (sEMG) characteristics
The scores were significantly reduced to 31.19 ± 14.35 (UPDRS-III) and 3.71 ± 2.18 (UPDRS-t), TABLE 2 | Clinical scores and EMG features between intraoperative DBS-off and DBS-on in PD patients
Summary
Deep brain stimulation (DBS) is an effective therapy for resting tremor in Parkinson’s disease (PD). To achieve optimal stimulation efficacy, the targets for some patients would be changed one, two, or even more times with rescue or replacement operations or with repeat multiple-pass mapping through the use of microelectrode recording during the DBS testing stage [7,8,9]. The currently established evaluation methods for DBS efficacy mostly depend on the neurosurgeon’s or neurologist’s experience, intraoperative patients’ self-response, and post-operative assessment of a clinical scale (UPDRS, Unified Parkinson’s Disease Rating Scale) [10, 11]. An intraoperative and objective evaluation method is crucial for determining the efficacy of DBS in PD patients with resting tremor
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