REM and NREM sleep enactment behaviors in Parkinson’s disease, Parkinson’s disease dementia, and dementia with Lewy bodies

doi:10.1016/j.sleep.2012.04.015

Sleep Medicine

Volume 13, Issue 7, August 2012, Pages 926-932

https://doi.org/10.1016/j.sleep.2012.04.015 Get rights and content

Abstract

Background/objective

Nocturnal sleep enactment behaviors (SEBs) are common in patients affected by Parkinson’s disease (PD), dementia associated with Parkinson’s disease (PDD), and dementia with Lewy bodies (DLB). We investigated the occurrence and neurobiological significance of abnormal SEBs in the context of PD without cognitive decline compared to PDD/DLB patients.

Methods

We evaluated a sample of 139 patients with PD, PDD, or DLB in a cross-sectional survey. One hundred and seventeen patients showing either no cognitive impairment (PD group) or meeting the diagnostic requirements for dementia (PDD/DLB group) underwent video-polysomnography. Seventy subjects (42 males) in whom a clear-cut diagnosis of abnormal sleep-related motor-behavioral episodes was possible were included in the final analysis.

Results

SEBs consisting of RBD or occurring on arousal from NREM or REM sleep were globally more frequent in the dementia group (PDD/DLB) than in the PD group (p = 0.001), the difference being statistically significant for arousal-related episodes (p = 0.002), while a trend emerged for RBD (p = 0.07). Male sex, daytime sleepiness, higher motor impairment, and lower mini-mental score were significantly more frequent with the occurrence of abnormal sleep-related motor-behavioral episodes.

Conclusion

SEBs in PD, PDD, and DLB may consist of RBD episodes or of arousal-related NREM and REM episodes. These latter are more frequent in patients with PDD/DLB and seem to be mainly related to more advanced stages of disease with a higher degree of cognitive decline.

Introduction

Nocturnal sleep enactment behaviors (SEBs) are frequently reported by bed partners of patients affected by diseases in the clinical spectrum [1] of Parkinson’s disease (PD), dementia associated with PD (PDD), and dementia with Lewy bodies (DLB) [2], [3].

We refer to “SEBs” as an anamnestic category of motor or behavioral sleep-related phenomena which proved to be quite heterogeneous events at video-PSG monitoring. They do not merely consist of REM sleep behavior disorder (RBD), but also of arousal-related episodes arising from NREM or REM sleep or coexistence of NREM and REM-related phenomena (overlap syndrome).

RBD is by far the best-characterized parasomnia in patients with synucleinopathies [4]. It features dream-enacting movements and behaviors occurring against the background of a loss of normal skeletal muscle atonia during REM sleep. It is reported, on average, in around 30% [5] and up to 46% [6] of PD patients, 80–95% of patients with multiple system atrophy [7], and 50–80% of those with DLB [8]. Literature data indicate that RBD is associated with, or predicts, the development of cognitive impairment in PD patients [9], [10], [11].

Little is known about the occurrence and biological significance of Arousal-related Motor-Behavioral Episodes (AMBEs), which have so far been reported only in PD patients [12], [13].

The aim of this study is to investigate patterns of occurrence and the neurobiological significance of the various kinds of SEBs in the context of PD without cognitive decline compared to PDD/DLB patients.

Section snippets

Setting and patient recruitment

The study was approved by the scientific board of the “Casimiro Mondino National Institute of Neurology” Foundation, Pavia, Italy. Patients were recruited among consecutive referrals to the outpatient clinic at the Parkinson’s Disease and Movement Disorders Unit from December 2005 to July 2010.

Patients affected by idiopathic PD diagnosed according to the United Kingdom Parkinson’s Disease Society Brain Bank (UKPDSBB) criteria [14], or fulfilling either the DLB Consortium criteria for probable

Sleep patterns

Patients with PDD/DLB showed patterns of RSWA more frequently than PD patients (75.9% vs. 65.9%), although the difference was not statistically significant.

Patterns of obstructive sleep apnea were found in six patients with PD (14.6%) and in two patients with PDD/DLB (6.8%) (p = ns). No significant difference between the two groups was detected in the AHI or in the oxygen desaturation index (ODI).

There emerged a slightly higher prevalence of PLMs and ALMA in patients with PDD/DLB (41.4%) as

Discussion

Our study shows that SEBs occurred more frequently in patients with PDD/DLB than in those with PD, with 68.4% consisting of isolated RBD and 31.6% encompassing SEBs consisting of arousal-related episodes from NREM and REM sleep, i.e., “Arousal-related Motor Behavioral Episodes” (AMBEs).

Both RBD and AMBEs were more frequent in the PDD/DLB than in the PD group (p = 0.001), with the difference being statistically significant for AMBES (p = 0.002), while a trend emerged for RBD (p = 0.07).

The higher

Conflict of interest

The ICMJE Uniform Disclosure Form for Potential Conflicts of Interest associated with this article can be viewed by clicking on the following link: doi:10.1016/j.sleep.2012.04.015.

. ICMJE Form for Disclosure of Potential Conflicts of Interest form.

Acknowledgements

We thank Dr. Piero Perucca for his invaluable advice on statistical analysis conception.

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Arousal-related disorders appear to be a marker of cognitive decline in PD. Recognizing arousal-related disorders should make clinicians aware of a possible cognitive decline in PD and eventually modify the therapeutic approach.
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Original ArticleREM and NREM sleep enactment behaviors in Parkinson’s disease, Parkinson’s disease dementia, and dementia with Lewy bodies

Abstract

Background/objective

Methods

Results

Conclusion

Introduction

Section snippets

Setting and patient recruitment

Sleep patterns

Discussion

Conflict of interest

Acknowledgements

J Neurol Sci

Sleep Med Rev

Clin Neurophysiol

Lancet Neurol

Parkinsonism Relat Disord

Lancet

Spectrum of Parkinson’s disease, Parkinson’s dementia, and Lewy body dementia

Neurol Clin

REM sleep behavior disorder and REM sleep without atonia in Parkinson’s disease

Neurology

Associated factors for REM sleep behavior disorder in Parkinson disease

Neurology

REM sleep behavior disorders in multiple system atrophy

Neurology

Pathophysiology of REM sleep behaviour disorder and relevance to neurodegenerative disease

Brain

Sleepwalking in patients with Parkinson disease

Arch Neurol

Complex paroxysmal nocturnal behaviors in Parkinson’s disease

Mov Disord

Sleepwalking in Parkinson’s disease: a questionnaire-based survey

J Neurol

REM sleep behavior disorder predicts cognitive impairment in Parkinson disease without dementia

Neurology

REM behavior disorder, hallucinations and cognitive impairment in Parkinson’s disease: a two-year follow up

Mov Disord

The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson’s disease

J Neurol Neurosurg Psychiatry

Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium

Neurology

Clinical diagnostic criteria for dementia associated with Parkinson’s disease

Mov Disord

Original Article
REM and NREM sleep enactment behaviors in Parkinson’s disease, Parkinson’s disease dementia, and dementia with Lewy bodies