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Bilateral Subthalamic Stimulation can Improve Sleep Quality in Parkinson’s Disease

Abstract

Background:

Sleep problems are among the most common non-motor symptoms of Parkinson’s disease (PD). The PD Sleep Scale 2nd version (PDSS-2) improved the original PDSS by adding more items on different aspects of sleep problems, making it a more robust tool to evaluate the severity of sleep disturbances. However, previous studies on deep brain stimulation (DBS) have not used the PDSS-2.

Objective:

To determine if the PDSS-2 could detect improvement reliably in sleep problems after bilateral subthalamic nucleus DBS for PD.

Methods:

In this prospective study, 25 consecutive patients undergoing DBS implantation were enrolled. Patients were examined twice: 1 week prior to the DBS implantation (baseline) and 12 months postoperatively. Severity of PD symptoms were assessed by the Movement Disorders Society Unified PD Rating Scale (MDS-UPDRS) and the Non-Motor Symptoms Scale (NMSS). Presence and severity of sleep disturbances were specifically measured by PDSS-2.

Results:

Total score of MDS-UPDRS improved from 81 (median, interquartile-range: 63-103) to 55 points (median, IQR: 46-75, p <  0.001). Health-related quality of life, measured by PDQ-39, also improved from 29 (IQR: 18-40) to 15 (IQR: 9-28) points (p = 0.002). Most domains of NMSS also improved. At baseline 13 patients reported sleep problems, but 1 year after DBS implantation only 3 did (p = 0.012). Although only 6 out of 15 items showed a significant decrease after DBS implantation, the total score of PDSS-2 decreased from 24 (IQR: 17-32) to 10 (IQR: 7-18) points (P <  0.001).

Conclusions:

Based on our results, PDSS-2 can detect improvements in sleep quality reliably after DBS implantation.

INTRODUCTION

Recently the non-motor symptoms (NMS) of Parkinson’s disease (PD) have been increasingly recognized as a major burden of quality of life [1, 2]. Among the NMS, sleep-related problems are the most important and troublesome. Although sleep problems can be present in up to 90% of PD patients, only a few study focused on the outcome of different therapeutic options to improve sleep quality.

Deep brain stimulation (DBS) of the subthalamic nucleus (STN) is a well-established therapy for patients with PD having advanced motor complications. Previous electrophysiological and patient-reported outcome-based studies demonstrated the beneficial effect of STN DBS on sleep quality in PD [3–6].

Because sleep-related problems are certainly multicausal, instruments capable of measuring most domains of sleep-disturbances are needed in the clinical practice. Based on the systematic review and evaluation of sleep-related rating scales by the Movement Disorders Society Task Force [7], only a few scales were found to be appropriate for the PD population. The original Parkinson’s Disease Sleep Scale (PDSS) [8] was published in 2002, and it had 15 visual analogue scale-based items. It was one of the first sleep scales designed specifically for PD. Higher values on PDSS indicate a better sleep quality. Although the application of PDSS was recommended by the MDS Task Force, they identified some weaknesses of the scale including the inability to specifically identify and measure the presence and severity of sleep apnea, rapid eye movements sleep behavioral sleep disorder (RBS) and restless legs syndrome RLS-related symptoms. To overcome these disadvantages, a new scale, the Parkinson’s Disease Sleep Scale 2nd version (PDSS-2), was developed and published in 2011 [9]. The PDSS-2 scale is composed of 15 items evaluating three domains. Each item has a 5-point Likert-type scale ranging from 0: “Never” to 4: “Very often” (except for item 1 which is reversed). Each domain consists of clusters of five questions evaluating motor symptoms at night, PD symptoms at night and disturbed sleep [9]. The sum of the 15 responses gives the total score of PDSS-2 with the maximum value of 60 points and higher scores meaning more nocturnal disturbance. The reliability, precision and test-retest validity of PDSS-2 is good [9, 10], making it suitable for measuring changes over a longer period of time. PDSS-2 is thought to have better clinimetric properties and responsiveness to changes in sleep problems than the original PDSS [11].

Despite its advantages over PDSS, the assessment of sleep quality before and after bilateral STN DBS with the PDSS-2 has not been reported in the literature; thus, the responsiveness of the PDSS-2 to DBS treatment is unknown. The objective of the present study was to analyze how bilateral subthalamic deep brain stimulation therapy can change sleep disturbances as assessed by the newly developed PDSS-2 and the non-motor section of the Movement Disorders Society-sponsored Unified Parkinson’s Disease Rating Scale (MDS-UPDRS).

MATERIALS AND METHODS

Patients

In this prospective study, 25 consecutive patients undergoing bilateral subthalamic deep brain stimulation at the University of Pécs were enrolled. All patients fulfilled the UK Brain Bank criteria for PD [12]. Each subject gave written informed consent in accordance with the ethical approval of the Regional Ethical Board (3617.316-24983/KK41/2009). Each patient was examined by a neurologist specialized in movement disorders.

Because the presence of minor or major neurocognitive disorder was a contraindication for DBS surgery, such patients were not included in this study [13]. Presence of dementia was defined as either achieving ≤125 points on the Hungarian validated version of the Mattis Dementia Rating Scale [14] and/or ≤22 points on the Montreal Cognitive Assessment [15] and/or fulfilling the criteria of dementia according to the DSM-IV-TR.

Patients were evaluated in ON state while receiving their usual antiparkinsonian and other medications. Subsequently, levodopa equivalent dosage calculations were performed [16].

Rating scales utilized in the study

Patients were examined twice: 1 week prior to the DBS implantation (baseline) and 12 months postoperatively. Severity of PD symptoms was globally assessed by the Hungarian validated version of the MDS-UPDRS [17]. The recently published MDS-UPDRS is a validated scale to assess non-motor aspects (Part 1) and motor aspects (Part 2) of experiences of daily living, motor examination (Part 3) and motor complications (Part 4) [18]. Included in the non-motor part, MDS-UPDRS has two items evaluating the presence and severity of nighttime sleep problems (item 1.17) and daytime sleepiness (item 1.18). These two items serve as a screening tool for sleep disturbances and daytime sleepiness [19]. As a part of the MDS-UPDRS, the Hoehn-Yahr Scale was also taken to detect the overall severity of PD. Besides, we also applied the Clinical Global Impression – Severity scale (CGI-S) to evaluate the overall illness severity on a 7-item Likert-type scale: 1: normal, not at all ill; 2: borderline ill; 3: mildly ill; 4: moderately ill; 5: markedly ill; 6: severely ill; or 7: extremely ill.

To assess non-motor symptoms globally, the Non-Motor Symptoms Scale (NMSS) was also included. This scale is obtained by trained professionals and capable of simultaneously capturing the severity and frequency of nine non-motor domains typical for PD. Besides sleep, NMSS also evaluates cardiovascular, cognitive, mood, hallucinatory, gastrointestinal, urinary and sexual symptoms.

Presence and severity of sleep disturbances were specifically measured by PDSS-2. The threshold indicating sleep problems is 11 points for the Hungarian version of PDSS-2 [20]. Meantime, daytime sleepiness was assessed by the Epworth Sleepiness Scale [21] with the cutoff value of 8 points [20, 22].

As part of the neuropsychological domain, depression (Beck and Montgomery Depression Scales) and cognitive performance (Montreal Cognitive Assessment [15], Mattis Dementia Rating Scale [14] and Addenbrook Cognitive Examination [14]) were also examined. Health-related quality of life was measured by the Hungarian validated version of PDQ-39 [23].

Statistical analysis

All statistical analyses were carried out using the IBM SPSS software package (version 22.0.1, IBM Inc, Armonk, NY, USA). Because data from these scales were ordinal, non-parametric tests were applied. For description of the data, medians with interquartile range (IQR: 25th-75th percentile) were calculated. Wilcoxon signed rank test was applied for the comparison of baseline and follow-up values. To detect which item of PDSS-2 has changed significantly, we also used Bonferroni correction. For dichotomous variables (e.g., presence or absence of sleep-problems, usage of levodopa, etc.) McNemar test, and for categorical variables Chi-square tests were used. Statistical significance level was set at 5% .

RESULTS

Demographic and PD-related clinical data

The subject population consisted of 25 non-demented PD patients (18 males, age: 55.9±8.7 years, disease duration: 11.0±4.8 years). Nine patients had rigid-akinetic, 6 had tremor-dominant and 10 had mixed-type of PD. Hoehn-Yahr staging, medication usage and levodopa equivalent dosages are demonstrated in Table 1.

Severity of PD

While the antiparkinsonian medication was significantly reduced from 814 mg (median, IQR: 564-914 mg) to 420 mg (IQR: 250-594 mg, p = 0.001), the total score of MDS-UPDRS improved from 81 (median, IQR: 63-103 points) to 55 points (median, IQR: 46-75 points, p <  0.001). Besides, all domains of MDS-UPDRS also improved 12 months after DBS implantation (Table 1). Although the HY staging showed improvement, it did not reach the level of statistical significance (p = 0.095). However, significantly more patients (9/25) reported either no or borderline severity of PD after treatment compared to baseline based on the CGI-S scale (3/25, p = 0.047, Chi-square test).

Health-related quality of life also improved from 29 (IQR: 18–40) to 15 (IQR: 9–28) points (p = 0.002) measured by the PDQ-39 Summary Index.

Non-motor symptoms

With the exception of hallucinatory symptoms and sexual dysfunction, all domains of NMSS improved after DBS treatment. The total score of NMSS decreased from 68 (IQR: 46–85) to 40 points (IQR: 16–52, p = 0.001), whereas the Sleep domain of NMSS improved from 19 (IQR: 14–27) to 9 points (IQR: 6–16, p = 0.002, Table 1).

At baseline, 13 patients reported sleep problems (i.e., a total score of PDSS-2 ≥11 points), but 1 year after the DBS implantation only 3 did (p = 0.012, McNemar test). Simultaneously, the total score of PDSS-2 decreased from 24 (IQR: 17–32) to 10 (IQR: 7–18) points (P <  0.001). Although all domains of the PDSS-2 improved, only 6 items showed a significant decrease after DBS implantation. “Bed sleep quality”, “Restlessness of legs and arms at night”, “Urge to move legs and arms at night”, “Uncomfortable and immobility at night”, “Muscle cramps in arms and legs” and “Tremor on waking” items had significant improvement after Bonferroni correction (Table 2). This improvement in sleep quality was also captured by the MDS-UPDRS item 1.7 (“Sleep problems”, Table 2).

Before DBS implantation, 15 patients reported daytime sleepiness (i.e., total score of ESS ≥8 points), which decreased to 9 patients 1 year after the operation (p = 0.032, McNemar test). Meanwhile, the total score of ESS improved from 9 (IQR: 6–13) to 5 (IQR: 4–11) points (P = 0.003, Table 1). However, we detected only a trend for improvement on item 1.8 (“Daytime sleepiness”) of the MDS-UPDRS.

Both depression-measuring tools (BDI and MADRS) demonstrated a significant improvement in depressive symptoms; whereas, the neurocognitive performance on neuropsychological tests (MDRS, ACE and MOCA) did not change (Table 1).

DISCUSSION

The aim of the present study was to identify the beneficiary effects of bilateral subthalamic deep brain stimulation on sleep quality by the utilization of the recently developed PDSS-2. As far as the authors are aware, this is the first prospective study utilizing the PDSS-2 and MDS-UPDRS scales to assess the longitudinal changes in sleep disturbances. Since the PDSS-2 has distinctive items on different aspects of sleep disturbances specific for PD, we were able to analyze what components of sleep responded to DBS therapy.

Fulfilling our expectations, most non-motor symptoms (including mood, gastrointestinal, urinary, cardiovascular and sleep) improved by STN DBS according to the subscales of NMSS, MDS-UPDRS, BDI and MADRS scales. Not only the number of patients reporting clinically relevant sleep problems decreased, but also the general sleep quality measured by both Sleep section of the NMSS and the total score of PDSS-2 improved.

The analysis of individual components of PDSS-2 revealed that only a few distinctive components of sleep contributed to the observed improvement in sleep quality. According to our data, RLS-related problems (items 4 and 5: “Restlessness of legs and arms at night” and “Urge to move legs and arms”), some nocturnal OFF symptoms (items 9 and 11: “Uncomfortable and immobility at night” and “Muscle cramps in arms and legs”), tremor on waking (item 13) and general sleep quality (item 1) improved significantly after STN DBS therapy.

Previously, only a few studies utilized the MDS-UPDRS to reveal the changes associated with STN DBS. We identified a single study (Pubmed search, keywords: MDS-UPDRS and DBS, assessed on January 4, 2015) to determine if the MDS-UPDRS could detect improvement in both motor and non-motor symptoms after bilateral STN DBS for PD [24]. Although the authors concluded that all sections of MDS-UPDRS improved 6 months after DBS implantation, they did not find any improvement in item 1.7, “Sleep problems”. Conversely, our study showed a significant improvement in “Sleep problems” and a trend for improvement in “Daytime Sleepiness” items of MDS-UPDRS after Bonferroni correction. These incongruent results might be due to methodological discrepancies (20 patients vs. 25 patients, 6-month vs. 12-month follow-up, parametric vs. non-parametric tests). Probably because of the longer follow-up time, we also experienced a more robust improvement in Part 1 (5 points – median vs. 3.1 points – mean) of the MDS-UPDRS.

To our knowledge, previous DBS studies have not used the MDS-UPDRS and PDSS-2 at baseline and post-DBS to track clinical symptoms. Although our sample size was small, the degree of improvement in motor symptoms, as a result of STN DBS in our study, was similar to the improvement reported in a large randomized trial of DBS that used the original UPDRS [25, 26]. Although the clinimetric properties of PDSS differ from those of PDSS-2 (15 visual analogue scales vs. 15 Likert-type scales grouping into 3 major domains, higher values on PDSS represent a better sleep quality vs. lower numbers mean a better sleep quality on PDSS-2), we can compare their responsiveness to STN DBS. Hjort et al. demonstrated a 31.9% improvement (from 79.8 to 105.3 points on PDSS) in 10 PD patients who underwent DBS implantation. Chahine et al. analyzed 17 patients (12 receiving unilateral and 5 bilateral DBS) 6 months after surgery and reported a 30.5% improvement (from 94.2 to 122.9 points on PDSS) [6]. On the contrary, one article (available only in Chinese) did not report any significant improvement on PDSS 1 year after the operation [27]. Despite the above mentioned discrepancies between the PDSS and PDSS-2, we measured a comparable improvement in sleep quality (58.3% , from 24 to 10 points, median values, p <  0.001).

CONCLUSIONS

Subthalamic deep brain stimulation not only can decrease the number of patients reporting clinically relevant sleep problems but also improve the general sleep quality. This improvement can be consistently demonstrated by the PDSS-2, NMSS and the MDS-UPDRS. Besides sleep, most domains of non-motor symptoms and the health-related quality of life can be improved by DBS therapy.

The PDSS-2 has some advantages over the original PDSS in that it more comprehensively assesses the different aspects of sleep problems specific for PD. Because our results suggest that the PDSS-2 can reliably detect the sleep-related changes after DBS, we recommend that the PDSS-2 should be utilized in future DBS studies.

AUTHOR ROLES

  • 1 Research project: A. Conception, B. Organization, C. Execution.

  • 2 Statistical Analysis: A. Design, B. Execution, C. Review and Critique.

  • 3 Manuscript: A. Writing of the first draft, B. Review and Critique.

  • GD 1, 2, 3

  • ZA 1B, 2C, 3B

  • PA 1B, 2C, 3B

  • EB. 1B, 2C, 3B

  • JJ 1A, 2C, 3B

  • BF 1C, 2C, 3B

  • AM 1C, 2C, 3B

  • MK 1C, 2C, 3B

  • SK 1B, 2C, 3B

  • IB. 1B, 2C, 3B

  • TD 1B, 2C, 3B

  • NK 1, 2, 3

8FINANCIAL DISCLOSURES

GD reported no financial disclosure.

ZA received <1000 EUR consultation fees from Hungarian subsidiaries of Novartis, GlaxoSmithKline, UCB and Teva Pharmaceutical Industries Ltd. Regarding this study the author did not receive any corporate funding.

PA reported no financial disclosure.

EB. reported no financial disclosure.

JJ received <1000 EUR consultation fees from Hungarian subsidiaries of UCB, GlaxoSmithKline, Valenat and Eisai. Regarding this pilot study the author did not receive any corporate funding..

BF reported no financial disclosure.

SK: <1000 EUR consultation fees from Hungarian subsidiaries of Biogen, TEVA, Astellas, Pfizer, Novartis. Regarding this pilot study the author did not receive any corporate funding.

IB received <1000 EUR consultation fees from Hungarian subsidiaries of Medtronic. Regarding this study the author did not receive any corporate funding.

TD reported no financial disclosure.

NK received <1000 EUR consultation fees from Hungarian subsidiaries of Medtronic. Boehringer Ingelheim. Novartis. GlaxoSmithKline. UCB, Krka and Abbvie. Regarding this study the author did not receive any corporate funding.

MK reported no financial disclosure.

AM reported no financial disclosure.

Abbreviations

ACE

Addenbrooke Cognitive Examination

BDI

Beck Depression Inventory

CGI-S

Clinical Global Impression–Severity

COMTI

Catechol-O-methyl transferase inhibitor

ESS

Epworth Sleepiness Scale

LED

levodopa-equivalent dosage

MADRS

Montgomery-Asberg Depression Rating Scale

MAOI

monoamine-oxidase inhibitor

MDS-UPDRS

The Movement Disorder Society-sponsored Unified Parkinson’s Disease Rating Scale

MOCA

Montreal Cognitive Assessment

NMS

Non-motor Symptoms

ACKNOWLEDGMENTS

Our study was supported by the Bolyai Scholarship of the Hungarian Academy of Sciences, OTKA PD103964, TáMOP 4.2.2.A-11/1/KONV-2012-0017 and the Hungarian Brain Research Program - Grant No. KTIA_13_NAP-A-II/10 government-based funds. The present scientific contribution is dedicated to the 650th anniversary of the foundation of the University of Pécs, Hungary. We also thank Dr. Csaba Juhész for his language editing work.

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Figures and Tables

Table 1

Comparison of preoperative and postoperative medication, motor and non-motor symptoms of Parkinson’s disease and the health-related quality of life

PreoperativePostoperativeSignificancetest
Mean or number

of patients
Standard

deviation
MedianPercentile

25
Percentile

75
MeanStandard

deviation
MedianPercentile

25
Percentile

75
MedicationLevodopa dosage (in LED)755.7418.97805201000282.9316.425004550.000W
Dopamine-agonist doseage (in LED)260.3196.3300150374213.4159.630003200.382W
Antiparkinson medication (in LED)848.9545.8814564914480.2245.04202505940.001W
Dopamine agonist usage19 (76%)18 (72%)1.000McN
MAOI usage2 (8%)1 (4%)0.125McN
Levodopa usage25 (100%)14 (56%)0.001McN
COMTI usage15 (60%)6 (24%)0.002McN
MDS-UPDRSHoehn-Yahr Scale
(stages 1/2/3/4/5)0/20/2/3/00/18/5/2/00.095Chi
CGI-S (1/2/3/4/5/6/7)0/3/7/5/6/2/22/7/10/3/3/0/00.001Chi
MDS-UPDRS Part115.35.315121811.17.0107120.004W
Item 1.7 “Sleep problem”2.41.33231.31.51030.003W
Item 1.8 “Daytime sleepiness”1.80.82221.21.11020.063W
MDS-UPDRS Part219.89.022122712.45.9129160.000W
MDS-UPDRS Part341.317.339295331.811.22924400.012W
MDS-UPDRS Part46.73.66593.52.93250.000W
MDS-UPDRS Total83.127.3816310358.820.25546750.000W
Non-motor symptomsNMSS (Part 1, Cardiovascular problems)4.34.14062.53.11040.049W
NMSS (Part 2, Sleep problems)19.39.419142712.210.296160.002W
NMSS (Part 3, Mood problems)12.310.0104228.913.731100.038W
NMSS (Part 4, Hallucinations)0.31.20000.41.60001.000W
NMSS (Part 5, Memory problems)6.36.36183.44.12060.004W
NMSS (Part 6, Gastrointestinal problems)5.96.74283.64.82050.041W
NMSS (Part 7, Urinary problems)9.89.663145.45.54180.042W
NMSS (Part 8, Sexual problems)4.36.20084.87.70080.937W
NMSS (Part 9, Miscellaneous problems)8.16.982124.25.52070.004W
NMSS Total score70.732.368468545.638.84016520.001W
Presence of Sleep problems12N/13Y22N/3Y0.012McN
PDSS-2 Total score24.89.924173214.211.4107180.000W
Presence of daytime sleepiness10N/15Y16N/9Y0.031McN
ESS Total score9.35.296137.15.254110.003W
PDQ-39 Summary index29.511.529184019.816.2159280.002W
NeuropsychologicalBDI Total score12.25.9117169.58.175110.039W
MADRS Total score11.85.9128159.38.465120.033W
MOCA23.13.523202625.93.02724280.220W
Mattis138.25.4140137141140.94.11421411440.407W
ACE86.47.187819186.86.58986900.423W

Presence of sleep problems was defined as having ≥11 points on PDSS-2 and presence of daytime sleepiness was defined as having ≥8 points on ESS. Abbreviations: ACE = Addenbrooke Cognitive Examination; BDI = Beck Depression Inventory; CGI-S = Clinical Global Impression-Severity; COMTI = catechol-O-methyl transferase inhibitor; ESS = Epworth Sleepiness Scale; LED = levodopa-equivalent dosage; MADRS = Montgomery-Asberg Depression Rating Scale; MAOI = monoamine-oxidase inhibitor; MDS-UPDRS = The Movement Disorder Society-sponsored Unified Parkinson’s Disease Rating Scale; MOCA = Montreal Cognitive Assessment; NMSS = Non-motor Symptoms Scale; PDSS-2 = Parkinson’s Disease Sleep Scale 2nd version. Applied statistical tests: Chi = Chi-square; McN = McNemar test; W = Wilcoxon signed rank test.

Table 1

Postoperative changes in the PDSS-2 items and domains

PreopPostopSignificance
ItemName of itemMeanStandard

deviation
MedianPercentile

25
Percentile

75
MeanStandard

deviation
MedianPercentile

25
Percentile

75
1Bed sleep quality2.21.22131.51.41020.047
2Difficulties falling asleep1.71.32131.01.30020.280
3Difficulties staying asleep2.51.33241.91.72040.445
4Restlessness of legs

   and arms at night
1.71.22030.91.10020.044
5Urge to move legs and arms1.61.42030.71.10010.043
6Distressing dreams at night0.80.91020.51.10001.000
7Distressing hallucinations

   at night
0.20.50000.10.40001.000
8Nocturia2.71.13241.81.51130.137
9Uncomfortable and

immobility at night
2.11.42130.81.10010.008
10Pain in arms and legs1.61.51030.91.10020.597
11Muscle cramps in arms and legs1.61.31120.81.20020.042
12Painful posturing in the morning1.31.41020.81.20010.183
13Tremor on waking2.11.32130.81.40010.005
14Tired and sleepy after waking

   in the morning
1.91.02131.41.11120.383
15Snoring or difficulties in breathing0.91.20020.20.70000.166
Motor symptoms at night domain7.54.175103.64.03050.001
PD symptoms at night domain6.33.66493.03.72040.002
Disturbed sleep domain11.04.5118147.65.373120.001
Total score of PDSS-224.89.924173214.211.4107180.000

Abbreviation: PDSS-2 = Parkinson’s Disease Sleep Scale 2nd version; p-values are indicated after Bonferroni correction (based on Wilcoxon signed rank test).