Abstract
Purpose of Review
Sleep disturbances are an important nonmotor feature of Parkinson’s disease (PD) that can cause polysomnographic (PSG) alterations. These alterations are already present in early PD and may be associated with a specific disease course. This systematic review describes the role of PSG variables as predictors of sleep dysfunction, motor and cognitive dysfunction progression in PD.
Recent Findings
Nineteen longitudinal cohort studies were included. Their main findings were that (1) REM sleep behavioral events, REM sleep without atonia (RSWA), and electroencephalography (EEG) changes (mainly microsleep instability) are predictors of the development of REM sleep behavior disorder (RBD); (2) RBD, RSWA, and lower slow-wave sleep energy predict motor progression; (3) RBD, EEG slowing, and sleep spindles changes are predictors of cognitive deterioration; and (4) OSA is associated with severe motor and cognitive symptoms at baseline, with inconsistent findings on the effect of continuous positive airway pressure (CPAP) therapy for these symptoms.
Summary
The results of our systematic review support a role of the video-PSG in disease progression prediction in PD and its usefulness as a biomarker. However, future studies are needed to investigate whether treatment of these PSG abnormalities and sleep disturbances may have a neuroprotective effect on disease progression.
Similar content being viewed by others
References
Papers of particular interest, published recently, have been highlighted as: • Of importance
Feigin VL, Nichols E, Alam T, Bannick MS, Beghi E, Blake N, et al. Global, regional, and national burden of neurological disorders, 1990–2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol. 2019;18:459–80.
Chaudhuri KR, Healy DG, Schapira AH. Non-motor symptoms of Parkinson’s disease: diagnosis and management. Lancet Neurol. 2006;5:235–45.
Schenck CH, Mahowald MW. REM sleep behavior disorder: clinical, developmental, and neuroscience perspectives 16 years after its formal identification in SLEEP. Sleep. 2002;25:120–38.
Zhang Y, Ren R, Sanford LD, Yang L, Zhou J, Tan L, et al. Sleep in Parkinson’s disease: a systematic review and meta-analysis of polysomnographic findings. Sleep Med Rev. 2020;51:101281. https://doi.org/10.1016/j.smrv.2020.101281. This meta-analysis investigated and summarized all polysomnographic changes in Parkinson's disease compared to controls with a cross-sectional design.
Brunner H, Wetter TC, Hogl B, Yassouridis A, Trenkwalder C, Friess E. Microstructure of the non-rapid eye movement sleep electroencephalogram in patients with newly diagnosed Parkinson’s disease: effects of dopaminergic treatment. Mov Disord. 2002;17:928–33.
Puca FM, Bricolo A, Turella G. Effect of L-dopa or amantadine therapy on sleep spindles in Parkinsonism. Electroencephalogr Clin Neurophysiol. 1973;35:327–30.
Emser W, Brenner M, Stober T, Schimrigk K. Changes in nocturnal sleep in Huntington’s and Parkinson’s disease. J Neurol. 1988;235:177–9.
Christensen JAE, Kempfner J, Zoetmulder M, Leonthin HL, Arvastson L, Christensen SR, et al. Decreased sleep spindle density in patients with idiopathic REM sleep behavior disorder and patients with Parkinson’s disease. Clin Neurophysiol. 2014;125:512–9.
Schroeder LA, Rufra O, Sauvageot N, Fays F, Pieri V, Diederich NJ. Reduced] rapid eye movement density in Parkinson disease: a polysomnography-based case-control study. Sleep. 2016;39:2133–9.
Kallio M, Suominen K, Haapaniemi T, Sotaniemi K, Myllylä VV, Astafiev S, et al. Nocturnal cardiac autonomic regulation in Parkinson’s disease. Clin Auton Res. 2004;14:119–24.
Sauvageot N, Vaillant M, Diederich NJ. Reduced sympathetically driven heart rate variability during sleep in Parkinson’s disease: a case-control polysomnography-based study. Mov Disord. 2011;26:234–40.
Palma J-A, Urrestarazu E, Alegre M, Pastor MA, Valencia M, Artieda J, et al. Cardiac autonomic impairment during sleep is linked with disease severity in Parkinson’s disease. Clin Neurophysiol. 2013;124:1163–8.
Sommerauer M, Werth E, Poryazova R, Gavrilov YV, Hauser S, Valko PO. Bound to supine sleep: Parkinson’s disease and the impact of nocturnal immobility. Parkinsonism Relat Disord. 2015;21:1269–72.
Cochen De Cock V, Benard-Serre N, Driss V, Granier M, Charif M, Carlander B, et al. Supine sleep and obstructive sleep apnea syndrome in Parkinson’s disease. Sleep Med. (2015)16:1497–501.
Dijkstra F, Reyn N, de Bruyn B, van den Bossche K, de Volder I, Willemen M, et al. REM sleep without atonia and nocturnal body position in prediagnostic Parkinson’s disease. Sleep Med. 2021;84:308–16.
Högl B, Stefani A, Videnovic A. Idiopathic REM sleep behaviour disorder and neurodegeneration—an update. Nat Rev Neurol. 2018;14:40–55.
Bohnen NI, Hu MTM. Sleep Disturbance as Potential Risk and Progression Factor for Parkinson’s Disease. J Parkinsons Dis. 2019;9:603–14. This review describes possible underlying mechanism in which sleep disorders can influence disease progression in PD.
Berry RB, Brooks R, Gamaldo CE, et al. for the American Academy of Sleep Medicine. The AASM Manual for the Scoring of Sleep and Associated Events: rules, terminology and technical specifications. Darien, IL: Ame Acad Sleep Med; (2017).
Lim DC, Mazzotti DR, Sutherland K, Mindel JW, Kim J, Cistulli PA, et al. Reinventing polysomnography in the age of precision medicine. Sleep Med Rev. 2020;52:101313.
Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71.
Wells G, Shea B, O’Connell D, Peterson, J, Welch V, Losos M, et al. The Newcastle–Ottawa Scale (NOS) for assessing the quality of non-randomized studies in meta-analysis. (2000). https://www.ohri.ca//programs/clinical_epidemiology/oxford.asp.
Zimansky L, Muntean M-L, Leha A, Mollenhauer B, Trenkwalder C, Sixel-Döring F. Incidence and progression of rapid eye movement behavior disorder in early Parkinson’s disease. Mov Disord Clin Pract. 2021;8:534–40.
Nomura T, Inoue Y, Kagimura T, Nakashima K. Clinical significance of REM sleep behavior disorder in Parkinson’s disease. Sleep Med. 2013;14:131–5.
Figorilli M, Marques AR, Vidal T, Delaby L, Meloni M, Pereira B, et al. Does REM sleep behavior disorder change in the progression of Parkinson’s disease? Sleep Med. 2020;68:190–8.
Bugalho P, Ladeira F, Barbosa R, Marto JP, Borbinha C, da Conceição L, et al. Polysomnographic predictors of sleep, motor and cognitive dysfunction progression in Parkinson’s disease: a longitudinal study. Sleep Med. 2021;77:205–8.
Mollenhauer B, Zimmermann J, Sixel-Döring F, Focke NK, Wicke T, Ebentheuer J, et al. Baseline predictors for progression 4 years after Parkinson’s disease diagnosis in the De Novo Parkinson Cohort (DeNoPa). Mov Disord. 2019;34:67–77.
Sommerauer M, Valko PO, Werth E, Poryazova R, Hauser S, Baumann CR. Revisiting the impact of REM sleep behavior disorder on motor progression in Parkinson’s disease. Parkinsonism Relat Disord. 2014;20:460–2.
Bugalho P, Magriço M, Alves L, Borbinha C. Objective sleep data as predictors of cognitive decline in dementia with Lewy Bodies and Parkinson’s disease. Sleep Med. 2021;80:273–8.
Anang JBM, Gagnon J-F, Bertrand J-A, Romenets SR, Latreille V, Panisset M, et al. Predictors of dementia in Parkinson disease: a prospective cohort study. Neurology. 2014;83:1253–60.
Anang JBM, Nomura T, Romenets SR, Nakashima K, Gagnon J-F, Postuma RB. Dementia predictors in Parkinson disease: a validation study. J Parkinsons Dis. 2017;7:159–62.
Onofrj M, Thomas A, D’Andreamatteo G, Iacono D, Luciano AL, Di Rollo A, et al. Incidence of RBD and hallucination in patients affected by Parkinson’s disease: 8-year follow-up. Neurol Sci. 2002;23:s91–4.
Marinus J, Visser M, van Hilten JJ, Lammers GJ, Stiggelbout AM. Assessment of sleep and sleepiness in Parkinson disease. Sleep. 2003;26:1049–54.
Fahn S, Marsden C, Calne D, Goldstein, M. Unified Parkinson’s disease rating scale. Recent developments in Parkinson’s disease, Macmillan, Florham Park, USA (1987) pp. 153–163.
Folstein MF, Folstein SE, McHugh PR. “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12(3):189–98.
Nasreddine ZS, Phillips NA, Bédirian V, Charbonneau S, Whitehead V, Collin I, et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc. 2005;53:695–9.
Neikrug AB, Liu L, Avanzino JA, Maglione JE, Natarajan L, Bradley L, et al. Continuous positive airway pressure improves sleep and daytime sleepiness in patients with Parkinson disease and sleep apnea. Sleep. 2014;37:177–85.
Harmell AL, Neikrug AB, Palmer BW, Avanzino JA, Liu L, Maglione JE, et al. Obstructive sleep apnea and cognition in Parkinson’s disease. Sleep Med. 2016;21:28–34.
Meng L, Benedetti A, Lafontaine A-L, Mery V, Robinson AR, Kimoff J, et al. Obstructive sleep apnea, CPAP therapy and Parkinson’s disease motor function: a longitudinal study. Parkinsonism Relat Disord. 2020;70:45–50.
Kaminska M, Mery VP, Lafontaine A-L, Robinson A, Benedetti A, Gros P, et al. Change in cognition and other non-motor symptoms with obstructive sleep apnea treatment in Parkinson disease. J Clin Sleep Med. 2018;14:819–28.
Terzaghi M, Spelta L, Minafra B, Rustioni V, Zangaglia R, Pacchetti C, et al. Treating sleep apnea in Parkinson’s disease with C-PAP: feasibility concerns and effects on cognition and alertness. Sleep Med. 2017;33:114–8.
Podsiadlo D, Richardson S. The timed “Up & Go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc. 1991;39:142–8.
Johns MW. A new method for measuring daytime sleepiness: the Epworth sleepiness scale. Sleep. 1991;14(6):540–5.
Cesari M, Christensen JAE, Muntean M-L, Mollenhauer B, Sixel-Döring F, Sorensen HBD, et al. A data-driven system to identify REM sleep behavior disorder and to predict its progression from the prodromal stage in Parkinson’s disease. Sleep Med. 2021;77:238–48.
Schreiner SJ, Imbach LL, Werth E, Poryazova R, Baumann-Vogel H, Valko PO, et al. Slow-wave sleep and motor progression in Parkinson disease. Ann Neurol. 2019;85:765–70.
Latreille V, Carrier J, Gaudet-Fex B, Rodrigues-Brazète J, Panisset M, Chouinard S, et al. Electroencephalographic prodromal markers of dementia across conscious states in Parkinson’s disease. Brain. 2016;139:1189–99.
Latreille V, Carrier J, Lafortune M, Postuma RB, Bertrand J-A, Panisset M, et al. Sleep spindles in Parkinson’s disease may predict the development of dementia. Neurobiol Aging. 2015;36:1083–90.
Zhang X, Sun X, Wang J, Tang L, Xie A. Prevalence of rapid eye movement sleep behavior disorder (RBD) in Parkinson’s disease: a meta and meta-regression analysis. Neurol Sci. 2017;38:163–70.
Xu Z, Anderson KN, Saffari SE, Lawson RA, Chaudhuri KR, Brooks D, et al. Progression of sleep disturbances in Parkinson’s disease: a 5-year longitudinal study. J Neurol. 2021;268:312–20.
Boeve BF, Silber MH, Saper CB, Ferman TJ, Dickson DW, Parisi JE, et al. Pathophysiology of REM sleep behaviour disorder and relevance to neurodegenerative disease. Brain. 2007;130:2770–88.
Dijkstra F, Van den Bossche K, de Bruyn B, Reyn N, Viaene M, De Volder I, et al. REM sleep without atonia and the relation with Lewy body disease. Parkinsonism Relat Disord. 2019;67:90–8.
Sixel-Döring F, Trautmann E, Mollenhauer B, Trenkwalder C. Rapid eye movement sleep behavioral events: a new marker for neurodegeneration in early Parkinson disease? Sleep. 2014;37:431–8.
Pagano G, Micco RD, Yousaf T, Wilson H, Chandra A, Politis M. REM behavior disorder predicts motor progression and cognitive decline in Parkinson disease. Neurology. 2018;91:e894-905.
Liu Y, Lawton MA, Lo C, Bowring F, Klein JC, Querejeta-Coma A, et al. Longitudinal changes in Parkinson’s disease symptoms with and without rapid eye movement sleep behavior disorder: The Oxford Discovery Cohort Study. Mov Disord. 2021;36:2821–32.
Duarte Folle A, Paul KC, Bronstein JM, Keener AM, Ritz B. Clinical progression in Parkinson’s disease with features of REM sleep behavior disorder: a population-based longitudinal study. Parkinsonism Relat Disord. 2019;62:105–11.
Kumru H, Santamaria J, Tolosa E, Iranzo A. Relation between subtype of Parkinson’s disease and REM sleep behavior disorder. Sleep Med. 2007;8:779–83.
Postuma RB, Gagnon JF, Vendette M, Charland K, Montplaisir J. REM sleep behaviour disorder in Parkinson’s disease is associated with specific motor features. J Neurol Neurosurg Psychiatry. 2008;79:1117–21.
Elfil M, Bahbah EI, Attia MM, Eldokmak M, Koo BB. Impact of Obstructive Sleep Apnea on Cognitive and Motor Functions in Parkinson’s Disease. Mov Disord. 2021;36:570–80. This meta-analysis investigated and summarized the impact of obstructive sleep apnea on Parkinson symptoms.
Kaminska M, Lafontaine A-L, Kimoff RJ. The interaction between obstructive sleep apnea and Parkinson’s disease: possible mechanisms and implications for cognitive function. Parkinsons Dis. 2015;2015:849472.
Morawska MM, Moreira CG, Ginde VR, Valko PO, Weiss T, Büchele F, et al. Slow-wave sleep affects synucleinopathy and regulates proteostatic processes in mouse models of Parkinson’s disease. Sci Trans Med 2021;13:eabe7099. https://doi.org/10.1126/scitranslmed.abe7099.
Hablitz LM, Vinitsky HS, Sun Q, Stæger FF, Sigurdsson B, Mortensen KN, et al. Increased glymphatic influx is correlated with high EEG delta power and low heart rate in mice under anesthesia. Sci Adv. 2019;5:eaav5447. https://doi.org/10.1126/sciadv.aav5447.
Lee H-J, Lee DA, Shin KJ, Park KM. Glymphatic system dysfunction in obstructive sleep apnea evidenced by DTI-ALPS. Sleep Med. 2022;89:176–81.
Ding XB, Wang XX, Xia DH, Liu H, Tian HY, Fu Y, et al. Impaired meningeal lymphatic drainage in patients with idiopathic Parkinson’s disease. Nat Med. 2021;27(3):411–8.
Vendette M, Gagnon J-F, Décary A, Massicotte-Marquez J, Postuma RB, Doyon J, et al. REM sleep behavior disorder predicts cognitive impairment in Parkinson disease without dementia. Neurology. 2007;69:1843–9.
Müller MLTM, Bohnen NI, Kotagal V, Scott PJH, Koeppe RA, Frey KA, et al. Clinical markers for identifying cholinergic deficits in Parkinson’s disease: clinical marers of cholinergic deficits in PD. Mov Disord. 2015;30:269–73.
Fereshtehnejad S-M, Zeighami Y, Dagher A, Postuma RB. Clinical criteria for subtyping Parkinson’s disease: biomarkers and longitudinal progression. Brain. 2017;140:1959–76.
Menšíková K, Matěj R, Colosimo C, Rosales R, Tučková L, Ehrmann J, et al. Lewy body disease or diseases with Lewy bodies? npj Parkinsons Dis. 2022;8:1–11. https://doi.org/10.1038/s41531-021-00273-9.
McKeith IG, Boeve BF, Dickson DW, Halliday G, Taylor J-P, Weintraub D, et al. Diagnosis and management of dementia with Lewy bodies: fourth consensus report of the DLB Consortium. Neurology. 2017;89:88–100.
Bubu OM, Andrade AG, Umasabor-Bubu OQ, Hogan MM, Turner AD, de Leon MJ, et al. Obstructive sleep apnea, cognition and Alzheimer’s disease: a systematic review integrating three decades of multidisciplinary research. Sleep Med Rev. 2020;50:101250.
Kozak VV, Chaturvedi M, Gschwandtner U, Hatz F, Meyer A, Roth V, et al. EEG slowing and axial motor impairment are independent predictors of cognitive worsening in a three-year cohort of patients with Parkinson’s disease. Front Aging Neurosci. 2020;12:171.
Cozac VV, Chaturvedi M, Hatz F, Meyer A, Fuhr P, Gschwandtner U. Increase of EEG spectral theta power indicates higher risk of the development of severe cognitive decline in Parkinson’s disease after 3 years. Front Aging Neurosci. 2016;8:284.
Caviness JN, Hentz JG, Belden CM, Shill HA, Driver-Dunckley ED, Sabbagh MN, et al. Longitudinal EEG changes correlate with cognitive measure deterioration in Parkinson’s disease. J Parkinsons Dis. 2015;5:117–24.
Arnaldi D, De Carli F, Famà F, Brugnolo A, Girtler N, Picco A, et al. Prediction of cognitive worsening in de novo Parkinson’s disease: clinical use of biomarkers. Mov Disord. 2017;32:1738–47.
Klassen BT, Hentz JG, Shill HA, Driver-Dunckley E, Evidente VGH, Sabbagh MN, et al. Quantitative EEG as a predictive biomarker for Parkinson disease dementia. Neurology. 2011;77:118–24.
Steriade M, Gloor P, Llinás RR, Lopes da Silva FH, Mesulam M-M. Basic mechanisms of cerebral rhythmic activities. Electroencephal Clin Neurophysiol. 1990;76:481–508.
Jellinger KA. Morphological basis of Parkinson disease-associated cognitive impairment: an update. J Neural Transm. 2022;129:977–999. https://doi.org/10.1007/s00702-022-02522-4.
Caporro M, Haneef Z, Yeh HJ, Lenartowicz A, Buttinelli C, Parvizi J, et al. Functional MRI of sleep spindles and K-complexes. Clin Neurophysiol. 2012;123:303–9.
Funding
We thank the patient support group “Move for Parkinson”, Rotary Belgium and the Koning Boudewijn Stichting/Fondsen Druwé-Eerdekens/Van Ael/Vlaamse Parkinson Liga for their participation in funding the project. Funding sources were not involved in the research or manuscript editing.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
All authors: no financial or non-financial disclosures.
Human and Animal Rights and Informed Consent
This article does not contain any studies with human or animal subjects performed by any of the authors.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
This article is part of the Topical Collection on Sleep.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Dijkstra, F., de Volder, I., Viaene, M. et al. Polysomnographic Predictors of Sleep, Motor, and Cognitive Dysfunction Progression in Parkinson’s Disease. Curr Neurol Neurosci Rep 22, 657–674 (2022). https://doi.org/10.1007/s11910-022-01226-2
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11910-022-01226-2