Elsevier

Sleep Medicine

Volume 79, March 2021, Pages 195-204
Sleep Medicine

Original Article
A quantitative analysis of the effect of bilateral subthalamic nucleus-deep brain stimulation on subjective and objective sleep parameters in Parkinson's disease

https://doi.org/10.1016/j.sleep.2020.10.021Get rights and content

Highlights

  • STN-DBS improved subjective sleep assessed by ESS, NMSS, PSQI and IRLS.

  • The improvement of EDS disappeared in the long-term follow-up.

  • PSG parameters remained largely unchanged except for a shortened RSL after STN-DBS.

  • Dopamine drug reduction correlated with the improvement in EDS after STN-DBS.

  • Motor improvement correlated with the improvement in subjective nocturnal sleep.

Abstract

Objective

To explore how subjective and objective sleep parameters respond to bilateral subthalamic nucleus-deep brain stimulation (STN-DBS) in patients with Parkinson's disease (PD).

Methods

Thirty DBS sleep studies were included by searching PubMed, Embase, and the Cochrane Library, and only 21 prospectively designed studies, including 541 patients, were eligible for the main analysis. We evaluated sleep disturbance using 1 objective measurement, polysomnography (PSG), and 4 subjective scales, including PD Sleep Scale (PDSS), Pittsburgh Sleep Quality Index (PSQI), Epworth Sleepiness Scale (ESS), and restless legs syndrome (RLS). We pooled data using the standard mean difference (SMD). The primary outcome was a change in sleep parameters 6 months postoperatively. Outcomes from <12 months to ≥12 months follow-up were compared in the subgroup analysis. Meta-regression was further conducted.

Results

STN-DBS significantly improved all 4 subjective sleep scales in the 6-month follow-up: ESS (SMD = 0.234), PDSS (SMD = 0.724), PSQI (SMD = 1.374) and RLS (SMD = 1.086), while most PSG parameters remained unchanged, except for shortened rapid eye movement sleep latency (RSL) (SMD = 0.520). In the over-12-month follow-up, improvement persisted in PDSS but not in ESS. Dopamine drug reduction (p = 0.009) and motor improvement (p = 0.036) were correlated with ESS improvement and PDSS improvement, respectively.

Conclusions

Bilateral STN-DBS continuously improved subjective nocturnal sleep, while its effect on ESS lasted for only 1 year. Medication reduction and motor improvement may contribute to improved daytime sleepiness and better subjective nocturnal sleep, respectively. Except for a shortened RSL, STN-DBS did not change PSG parameters, including sleep efficiency and sleep architecture.

Registration

Open Science Framework: DOI 10.17605/OSF.IO/3EGRC.

Introduction

Sleep disorders trouble 75%–98% of patients with Parkinson's disease (PD) [1,2] and greatly contribute to decreased quality of life [3]. Conventional drug therapy, such as clonazepam, eszopiclone and doxepin, has some effects on sleep symptoms but can potentially worsen daytime sleepiness and cognition [[4], [5], [6]]. As a well-established surgical treatment option, subthalamic nucleus-deep brain stimulation (STN-DBS) has been indicated by some reports to alleviate not only motor symptoms but also sleep disorders in PD patients [[7], [8], [9]]. Sleep problems in PD can be broadly categorized into daytime manifestations and nocturnal manifestations [10] and can be evaluated using subjective scales or objective instruments (e.g., polysomnography (PSG)). Despite some disputes, many subjective-rating and PSG studies have observed both improved excessive daytime sleepiness (EDS) and nocturnal sleep quality in patients who underwent bilateral STN-DBS [[11], [12], [13], [14]].

However, it should be noted that current DBS sleep studies have some drawbacks, including their retrospective design, limited sample size and employment of only self-rating scales. In addition, mild improvement or even worsening of sleep symptoms has occasionally been reported [[15], [16], [17]]. We currently do not have a holistic understanding of the effect of STN-DBS on sleep. There are three major questions that remain unclear and imperative to address. First, not all authors agree that STN-DBS improves sleep. Conflicting opinions have been proposed, primarily in PSG studies [15,16]. Thus, whether and to what extent STN-DBS improves sleep disorders is worth exploring. Second, most DBS sleep studies have outcomes with less than 1-year follow-up [18,19], leaving questions, such as how the benefits provided by STN-DBS last, whether the beneficial effect will persist or wane with time, and which factors are correlated with postoperative sleep improvement. Exploring these factors may greatly facilitate predicting which patients may benefit from DBS and can help enhance our understanding of how STN-DBS affects sleep.

Although previous studies have reviewed the effect of bilateral STN-DBS on sleep problems [[20], [21], [22], [23]], none of them have answered any of the above questions in a quantitative or systematic way. In 2019, Zhang et al. [20] quantitatively evaluated the effect of STN-DBS on sleep quality and restless leg symptoms in a meta-analysis. However, they included only 2 subjective sleep scales and did not discuss objective sleep change evaluated by PSG. As the gold standard of sleep measurement [24], PSG may lead to results that are very different from those of subjective scales [25]. In addition, only 7 articles were included in Zhang's study, making further subgroup analysis and meta-regression analysis impossible. Thus, in this study, we aimed to explore how both subjective and objective sleep parameters respond to STN-DBS in both short-term and longer follow-up and to identify potentially relevant factors.

Section snippets

Literature search

This study was conducted following the PRISMA guidelines. PubMed, Embase, Cochrane Central Register of Controlled Trials and Cochrane Movement Disorders Group Trials Register were searched for relevant studies. The following keywords were employed for standard searches utilizing Medical Subject Headings and Subheadings: “deep brain stimulation”, “Parkinson's disease”, “sleep disturbance”, “sleep quality”, “restless legs syndrome” and “excessive daytime sleepiness”. The detailed search algorism

Search results

A total of 30 studies, including 792 patients, were identified that met all inclusion and exclusion criteria (Fig. 1). Detailed information and specific quality assessment of all 30 studies are shown in Table 1 and Supplementary Table 1, respectively. However, it should be noted that only 21 studies that employed prospective design, including 541 patients, were eligible for the main analysis.

Quality assessment and baseline information

On average, included studies scored 4.8 in the MOOSE quality assessment tool. The most common reason for

PSG parameters

Results regarding the effect of STN-DBS on PSG parameters are controversial and include reports of improving [13,14,18,35], no change [36] and worsening [15,16]. In our study, except for reduced RSL, all parameters remained unchanged after DBS surgery, indicating only a mild effect of STN-DBS on objective sleep. However, we did observe a significantly shortened RSL, which is consistent with the observation of Torun et al. [16]. RSL is the time span between the onset of sleep and the start of

Conclusions

Bilateral STN-DBS significantly improved patient subjective sleep as assessed by PDSS/PDSS-2 in both the less-than-1-year and over-1-year follow-up, while its effect on EDS was significant only in the less-than-1-year follow-up subgroup. The reduction of LEDD was correlated with improved EDS, and the alleviation of motor symptoms was correlated with improved nocturnal sleep quality. Among all PSG parameters, only a shortened RSL was observed after STN-DBS. There was insufficient evidence to

Author contribution

Zixiao Yin: study design, data collection and analysis and manuscript draft.

Yutong Bai: study design, data collection and analysis and manuscript draft.

Boyuan Guan: manuscript revision.

Yin Jiang: manuscript draft and revision.

Zhan Wang: manuscript draft.

Fangang Meng: analyses.

Anchao Yang: manuscript review and revision.

Jianguo Zhang: manuscript review and revision.

Acknowledgements

This work was supported by National Natural Science Foundation of China (81671104, 81830033, 61761166004) and the Beijing Municipal Administration of Hospitals’ Ascent Plan (DFL20150503).

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