Isolated REM Sleep without Atonia Is Not Equivalent to REM Sleep Behavior Disorder in Early-Stage Parkinson's Disease.

Item request has been placed! ×
Item request cannot be made. ×
loading   Processing Request
  • Additional Information
    • Source:
      Publisher: Wiley-Liss Country of Publication: United States NLM ID: 8610688 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1531-8257 (Electronic) Linking ISSN: 08853185 NLM ISO Abbreviation: Mov Disord Subsets: MEDLINE
    • Publication Information:
      Publication: <2001->: New York, NY : Wiley-Liss
      Original Publication: [New York, N.Y.] : Raven Press, [c1986-
    • Subject Terms:
    • Abstract:
      Background: In early-stage Parkinson's disease (PD), rapid eye movement (REM) sleep behavior disorder (RBD) predicts poor cognitive and motor outcome. However, the baseline significance and disease evolution associated with isolated REM sleep without atonia (iRWA, ie, enhanced muscle tone during 8.7% of REM sleep, but no violent behavior) are not well understood.
      Objectives: The objective is to determine whether iRWA was a mild form of RBD and progressed similarly over time.
      Methods: Participants with early PD (<4 years from medical diagnosis) were included from 2014 to 2021 in a longitudinal study. They underwent interviews and examinations in the motor, cognitive, autonomous, psychiatric, sensory, and sleep domains every year for 4 years along with a video polysomnography and magnetic resonance imaging examination of the locus coeruleus/subcoeruleus complex (LC/LsC) at baseline. The clinical characteristics were compared between groups with normal REM sleep, with iRWA and with RBD, at baseline and for 4 years.
      Results: Among 159 PD participants, 25% had RBD, 25% had iRWA, and 50% had normal REM sleep. At baseline, the non-motor symptoms were less prevalent and the LC/LsC signal intensity was more intense in participants with iRWA than with RBD. Over 4 years, participants with normal REM sleep and with iRWA had a similar cognitive and motor trajectory, whereas participants with RBD had greater cognitive and motor decline.
      Conclusions: We demonstrated that iRWA is frequent in early PD, but is not a milder form of RBD. Both groups have distinct baseline characteristics and clinical trajectories. They should be distinguished in clinical routine and research protocols. © 2024 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.
      (© 2024 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.)
    • References:
      Baker KG, Törk I, Hornung JP, Halasz P. The human locus coeruleus complex: an immunohistochemical and three dimensional reconstruction study. Exp Brain Res 1989;77(2):257–270. https://doi.org/10.1007/bf00274983.
      García‐Lorenzo D, Longo‐dos Santos C, Ewenczyk C, et al. The coeruleus/subcoeruleus complex in rapid eye movement sleep behaviour disorders in Parkinson's disease. Brain 2013;136(7):2120–2129. https://doi.org/10.1093/brain/awt152.
      Postuma RB, Iranzo A, Hu M, et al. Risk and predictors of dementia and parkinsonism in idiopathic REM sleep behaviour disorder: a multicentre study. Brain 2019;142(3):744–759. https://doi.org/10.1093/brain/awz030.
      Anang JB, Gagnon JF, Bertrand JA, et al. Predictors of dementia in Parkinson disease: a prospective cohort study. Neurology 2014;83(14):1253–1260. https://doi.org/10.1212/wnl.0000000000000842.
      Liu Y, Lawton MA, Lo C, 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(12):2821–2832. https://doi.org/10.1002/mds.28763.
      Pagano G, De Micco R, Yousaf T, Wilson H, Chandra A, Politis M. REM behavior disorder predicts motor progression and cognitive decline in Parkinson disease. Neurology 2018;91(10):e894–e905. https://doi.org/10.1212/wnl.0000000000006134.
      Postuma RB, Bertrand JA, Montplaisir J, et al. Rapid eye movement sleep behavior disorder and risk of dementia in Parkinson's disease: a prospective study. Mov Disord 2012;27(6):720–726. https://doi.org/10.1002/mds.24939.
      Fereshtehnejad SM, Romenets SR, Anang JB, Latreille V, Gagnon JF, Postuma RB. New clinical subtypes of Parkinson disease and their longitudinal progression: a prospective cohort comparison with other phenotypes. JAMA Neurol 2015;72(8):863–873. https://doi.org/10.1001/jamaneurol.2015.0703.
      Otaiku DAI. Distressing dreams and risk of Parkinson's disease: a population‐based cohort study. EClinicalMedicine 2022;48:101474. https://doi.org/10.1016/j.eclinm.2022.101474.
      Ylikoski A, Martikainen K, Partinen M. Parasomnias and isolated sleep symptoms in Parkinson's disease: a questionnaire study on 661 patients. J Neurol Sci 2014;346(1–2):204–208. https://doi.org/10.1016/j.jns.2014.08.025.
      Gagnon JF, Bédard MA, Fantini ML, et al. REM sleep behavior disorder and REM sleep without atonia in Parkinson's disease. Neurology 2002;59(4):585–589. https://doi.org/10.1212/wnl.59.4.585.
      Stefani A, Gabelia D, Högl B, et al. Long‐term follow‐up investigation of isolated rapid eye movement sleep without Atonia without rapid eye movement sleep behavior disorder: a pilot study. J Clin Sleep Med 2015;11(11):1273–1279. https://doi.org/10.5664/jcsm.5184.
      Liu Y, Zhang J, Chau SWH, et al. Evolution of prodromal REM sleep behavior disorder to neurodegeneration: a retrospective longitudinal case‐control study. Neurology 2022;99(6):e627–e637. https://doi.org/10.1212/wnl.0000000000200707.
      Sasai‐Sakuma T, Frauscher B, Mitterling T, et al. Quantitative assessment of isolated rapid eye movement (REM) sleep without atonia without clinical REM sleep behavior disorder: clinical and research implications. Sleep Med 2014;15(9):1009–1015. https://doi.org/10.1016/j.sleep.2014.02.010.
      Pauline Dodet MH, Leu‐Semenescu S, Corvol J‐C, Lehéricy S, Mangone G, Vidailhet M, Roze E. Isabelle Arnulf sleep disorders in Parkinson's disease, an early and multiple problem. NPJ Parkinsons Dis 2024;10:46.
      Goetz CG, Tilley BC, Shaftman SR, et al. Movement Disorder Society‐sponsored revision of the unified Parkinson's disease rating scale (MDS‐UPDRS): scale presentation and clinimetric testing results. Mov Disord 2008;23(15):2129–2170. https://doi.org/10.1002/mds.22340.
      Mattis SBL, Karasu TB. Mental status examination for organic mental syndrome in the elderly patient. In: Bellak L, Karasu TB, eds. Geriatric Psychiatry a Handbook for Psychiatrists and Primary Care Physicians Grune & Stratton. Vol. 77–121. Grune and Stratton: New York; 1976.
      Dubois B, Slachevsky A, Litvan I, Pillon B. The FAB: a frontal assessment battery at bedside. Neurology 2000;55(11):1621–1626. https://doi.org/10.1212/wnl.55.11.1621.
      Nasreddine ZS, Phillips NA, Bédirian V, et al. The Montreal cognitive assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 2005;53(4):695–699. https://doi.org/10.1111/j.1532-5415.2005.53221.x.
      Funkiewiez A, Bertoux M, de Souza LC, Lévy R, Dubois B. The SEA (social cognition and emotional assessment): a clinical neuropsychological tool for early diagnosis of frontal variant of frontotemporal lobar degeneration. Neuropsychology 2012;26(1):81–90. https://doi.org/10.1037/a0025318.
      Rodriguez‐Blazquez C, Forjaz MJ, Frades‐Payo B, de Pedro‐Cuesta J, Martinez‐Martin P. Independent validation of the scales for outcomes in Parkinson's disease‐autonomic (SCOPA‐AUT). Eur J Neurol 2010;17(2):194–201. https://doi.org/10.1111/j.1468-1331.2009.02788.x.
      Chaudhuri KR, Sauerbier A, Rojo JM, et al. The burden of non‐motor symptoms in Parkinson's disease using a self‐completed non‐motor questionnaire: a simple grading system. Parkinsonism Relat Disord 2015;21(3):287–291. https://doi.org/10.1016/j.parkreldis.2014.12.031.
      Lawton M, Hu MT, Baig F, et al. Equating scores of the University of Pennsylvania Smell Identification Test and Sniffin' sticks test in patients with Parkinson's disease. Parkinsonism Relat Disord 2016;33:96–101. https://doi.org/10.1016/j.parkreldis.2016.09.023.
      Doty RL, Shaman P, Dann M. Development of the University of Pennsylvania Smell Identification Test: a standardized microencapsulated test of olfactory function. Physiol Behav 1984;32(3):489–502. https://doi.org/10.1016/0031-9384(84)90269-5.
      Iber CA‐IS, Chesson A, Quan S. The AASM Manual for the Scoring of Sleep and Associated Events: Rules, Terminology and Technical Specifications. 1rst ed. Westchester, IL: American Academy of Sleep Medicine; 2007 Revision 2.5 (2018).
      Frauscher B, Iranzo A, Gaig C, et al. Normative EMG values during REM sleep for the diagnosis of REM sleep behavior disorder. Sleep 2012;35(6):835–847. https://doi.org/10.5665/sleep.1886.
      Medicine AAoS. American Academy of sleep medicine. The International Classification of Sleep Disorders. 3rd ed. Darien, IL: American Academy of Sleep Medicine; 2014.
      Nobileau A, Gaurav R, Chougar L, et al. Neuromelanin‐sensitive magnetic resonance imaging changes in the locus coeruleus/subcoeruleus complex in patients with typical and atypical parkinsonism. Mov Disord 2023;38(3):479–484. https://doi.org/10.1002/mds.29309.
      Zhang J, Xu CY, Liu J. Meta‐analysis on the prevalence of REM sleep behavior disorder symptoms in Parkinson's disease. BMC Neurol 2017;17(1):23. https://doi.org/10.1186/s12883-017-0795-4.
      Dijkstra F, Reyn N, de Bruyn B, et al. REM sleep without atonia and nocturnal body position in prediagnostic Parkinson's disease. Sleep Med 2021;84:308–316. https://doi.org/10.1016/j.sleep.2021.06.011.
      Nomura T, Inoue Y, Kagimura T, Nakashima K. Clinical significance of REM sleep behavior disorder in Parkinson's disease. Sleep Med 2013;14(2):131–135. https://doi.org/10.1016/j.sleep.2012.10.011.
      Zimansky L, Muntean ML, 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(4):534–540. https://doi.org/10.1002/mdc3.13168.
      Rahayel S, Gaubert M, Postuma RB, et al. Brain atrophy in Parkinson's disease with polysomnography‐confirmed REM sleep behavior disorder. Sleep 2019;42(6):zsz062. https://doi.org/10.1093/sleep/zsz062.
      Kotagal V, Albin RL, Müller ML, Koeppe RA, Chervin RD, Frey KA, Bohnen NI. Symptoms of rapid eye movement sleep behavior disorder are associated with cholinergic denervation in Parkinson disease. Ann Neurol 2012;71(4):560–568. https://doi.org/10.1002/ana.22691.
      Arnaldi D, Morbelli S, Brugnolo A, et al. Functional neuroimaging and clinical features of drug naive patients with de novo Parkinson's disease and probable RBD. Parkinsonism Relat Disord 2016;29:47–53. https://doi.org/10.1016/j.parkreldis.2016.05.031.
      Sommerauer M, Fedorova TD, Hansen AK, et al. Evaluation of the noradrenergic system in Parkinson's disease: an 11C‐MeNER PET and neuromelanin MRI study. Brain 2018;141(2):496–504. https://doi.org/10.1093/brain/awx348.
      Boissard R, Fort P, Gervasoni D, Barbagli B, Luppi PH. Localization of the GABAergic and non‐GABAergic neurons projecting to the sublaterodorsal nucleus and potentially gating paradoxical sleep onset. Eur J Neurosci 2003;18(6):1627–1639. https://doi.org/10.1046/j.1460-9568.2003.02861.x.
      Braak E, Sandmann‐Keil D, Rüb U, et al. Alpha‐synuclein immunopositive Parkinson's disease‐related inclusion bodies in lower brain stem nuclei. Acta Neuropathol 2001;101(3):195–201. https://doi.org/10.1007/s004010000247.
      Iranzo A, Tolosa E, Gelpi E, et al. Neurodegenerative disease status and post‐mortem pathology in idiopathic rapid‐eye‐movement sleep behaviour disorder: an observational cohort study. Lancet Neurol 2013;12(5):443–453. https://doi.org/10.1016/s1474-4422(13)70056-5.
      McKenna D, Peever J. Degeneration of rapid eye movement sleep circuitry underlies rapid eye movement sleep behavior disorder. Mov Disord 2017;32(5):636–644. https://doi.org/10.1002/mds.27003.
      Mariotti P, Quaranta D, di Giacopo R, et al. Rapid eye movement sleep behavior disorder: a window on the emotional world of Parkinson disease. Sleep 2015;38(2):287–294. https://doi.org/10.5665/sleep.4416.
      Bugalho P, Paiva T. Dream features in the early stages of Parkinson's disease. J Neural Transm (Vienna) 2011;118(11):1613–1619. https://doi.org/10.1007/s00702-011-0679-5.
      Cygan F, Oudiette D, Leclair‐Visonneau L, Leu‐Semenescu S, Arnulf I. Night‐to‐night variability of muscle tone, movements, and vocalizations in patients with REM sleep behavior disorder. J Clin Sleep Med 2010;6(6):551–555.
      Puligheddu M, Figorilli M, Congiu P, et al. Quantification of REM sleep without atonia: a review of study methods and meta‐analysis of their performance for the diagnosis of RBD. Sleep Med Rev 2023;68:101745. https://doi.org/10.1016/j.smrv.2023.101745.
      Videnovic A, Marlin C, Alibiglou L, Planetta PJ, Vaillancourt DE, Mackinnon CD. Increased REM sleep without atonia in Parkinson disease with freezing of gait. Neurology 2013;81(12):1030–1035. https://doi.org/10.1212/WNL.0b013e3182a4a408.
    • Grant Information:
      Fondation EDF; Agence Nationale de la Recherche; Société Française de Médecine Esthétique and Energipole; Fondation planiol; fondation Saint Michel
    • Contributed Indexing:
      Keywords: REM behavior disorder; REM sleep without atonia; early‐stage Parkinson's disease; progression
    • Publication Date:
      Date Created: 20240426 Date Completed: 20240720 Latest Revision: 20240720
    • Publication Date:
      20240721
    • Accession Number:
      10.1002/mds.29813
    • Accession Number:
      38666582