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Autonomic symptoms in idiopathic REM behavior disorder: a multicentre case–control study

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An Erratum to this article was published on 14 December 2014

Abstract

Patients with idiopathic REM sleep behavior disorder (iRBD) are at very high risk of developing neurodegenerative synucleinopathies, which are disorders with prominent autonomic dysfunction. Several studies have documented autonomic dysfunction in iRBD, but large-scale assessment of autonomic symptoms has never been systematically performed. Patients with polysomnography-confirmed iRBD (318 cases) and controls (137 healthy volunteers and 181 sleep center controls with sleep diagnoses other than RBD) were recruited from 13 neurological centers in 10 countries from 2008 to 2011. A validated scale to study the disorders of the autonomic nervous system in Parkinson's disease (PD) patients, the SCOPA-AUT, was administered to all the patients and controls. The SCOPA-AUT consists of 25 items assessing the following domains: gastrointestinal, urinary, cardiovascular, thermoregulatory, pupillomotor, and sexual dysfunction. Our results show that compared to control subjects with a similar overall age and sex distribution, patients with iRBD experience significantly more problems with gastrointestinal, urinary, and cardiovascular functioning. The most prominent differences in severity of autonomic symptoms between our iRBD patients and controls emerged in the gastrointestinal domain. Interestingly, it has been reported that an altered gastrointestinal motility can predate the motor phase of PD. The cardiovascular domain SCOPA-AUT score in our study in iRBD patients was intermediate with respect to the scores reported in PD patients by other authors. Our findings underline the importance of collecting data on autonomic symptoms in iRBD. These data may be used in prospective studies for evaluating the risk of developing neurodegenerative disorders.

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References

  1. Schenck CH, Bundlie SR, Ettinger MG, Mahowald MW (1986) Chronic behavioral disorders of human REM sleep: a new category of parasomnia. Sleep 9:293–308

    CAS  PubMed  Google Scholar 

  2. Iranzo A, Molinuevo JL, Santamaria J, Serradell M, Martí MJ, Valldeoriola F, Tolosa E (2006) Rapid-eye-movement sleep behaviour disorder as an early marker for a neurodegenerative disorder: a descriptive study. Lancet Neurol 5:572–577

    Article  PubMed  Google Scholar 

  3. Postuma RB, Gagnon JF, Vendette M, Fantini ML, Massicotte-Marquez J, Montplaisir J (2009) Quantifying the risk of neurodegenerative disease in idiopathic REM sleep behavior disorder. Neurology 72:1296–1300

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  4. Iranzo A, Tolosa E, Gelpi E, Molinuevo JL, Valldeoriola F, Serradell M, Sanchez-Valle R, Vilaseca I, Lomeña F, Vilas D, Lladó A, Gaig C, Santamaria J (2013) Neurodegenerative disease status and post-mortem pathology in idiopathic rapid-eye-movement sleep behaviour disorder: an observational cohort study. Lancet Neurol 12:443–453

    Article  PubMed  Google Scholar 

  5. Valappil RA, Black JE, Broderick MJ, Carrillo O, Frenette E, Sullivan SS, Goldman SM, Tanner CM, Langston JW (2010) Exploring the electrocardiogram as a potential tool to screen for premotor Parkinson’s disease. Mov Disord 25:2296–2303

    Article  PubMed  Google Scholar 

  6. Postuma RB, Lanfranchi PA, Blais H, Gagnon JF, Montplaisir JY (2010) Cardiac autonomic dysfunction in idiopathic REM sleep behavior disorder. Mov Disord 25:2304–2310

    Article  PubMed  Google Scholar 

  7. Sorensen GL, Kempfner J, Zoetmulder M, Sorensen HB, Jennum P (2012) Attenuated heart rate response in REM sleep behavior disorder and Parkinson’s disease. Mov Disord 27:888–894

    Article  PubMed  Google Scholar 

  8. Miyamoto T, Miyamoto M, Suzuki K, Nishibayashi M, Iwanami M, Hirata K (2008) 123I-MIBG cardiac scintigraphy provides clues to the underlying neurodegenerative disorder in idiopathic REM sleep behavior disorder. Sleep 31:717–723

    PubMed Central  PubMed  Google Scholar 

  9. Postuma RB, Gagnon JF, Vendette M, Montplaisir JY (2009) Markers of neurodegeneration in idiopathic REM sleep behavior disorder and Parkinson's disease. Brain 132:2298–2307

    Article  Google Scholar 

  10. Postuma RB, Lang AE, Massicotte-Marquez J, Montplaisir J (2006) Potential early markers of Parkinson's disease in idiopathic REM sleep behavior disorder. Neurology 66:845–851

    Article  CAS  PubMed  Google Scholar 

  11. Postuma RB, Gagnon JF, Pelletier A, Montplaisir J (2013) Prodromal autonomic symptoms and signs in Parkinson’s disease and dementia with Lewy bodies. Mov Disord 28:597–604

    Article  PubMed  Google Scholar 

  12. Visser M, Marinus J, Stiggelbout AM, Van Hilten JJ (2004) Assessment of autonomic dysfunction in Parkinson’s disease: the SCOPA-AUT. Mov Disord 19:1306–1312

    Article  PubMed  Google Scholar 

  13. American Academy of Sleep Disorders (2005) International Classification of Sleep Disorders–2. American Academy of Sleep Disorders, Westchester

    Google Scholar 

  14. Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198

    Article  CAS  PubMed  Google Scholar 

  15. Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55:181–184

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  16. Boeve BF (2010) REM sleep behavior disorder: updated review of the core features, the REM sleep behavior disorder-neurodegenerative disease association, evolving concepts, controversies, and future directions. Ann N Y Acad Sci 1184:15–54

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Claassen DO, Josephs KA, Ahlskog JE, Silber MH, Tippmann-Peikert M, Boeve BF (2010) REM sleep behavior disorder preceding other aspects of synucleinopathies by up to half a century. Neurology 75:494–499

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  18. Jain S (2011) Multi-organ autonomic dysfunction in Parkinson's disease. Parkinsonism Relat Disord 17:77–83

    Article  PubMed Central  PubMed  Google Scholar 

  19. Idiaquez J, Roman GC (2011) Autonomic dysfunction in neurodegenerative dementias. J Neurol Sci 305:22–27

    Article  PubMed  Google Scholar 

  20. Wenning GK, Stefanova N (2009) Recent developments in multiple system atrophy. J Neurol 256:1791–1808

    Article  PubMed  Google Scholar 

  21. Ferini-Strambi L, Oldani A, Zucconi M, Smirne S (1996) Cardiac autonomic activity during wakefulness and sleep in REM sleep behavior disorder. Sleep 19:367–369

    CAS  PubMed  Google Scholar 

  22. Fantini ML, Michaud M, Gosselin N, Lavigne G, Montplaisir J (2002) Periodic leg movements in REM sleep behavior disorder and related autonomic and EEG activation. Neurology 59:1889–1894

    Article  CAS  PubMed  Google Scholar 

  23. Postuma RB, Gagnon JF, Vendette M, Montplaisir JY (2009) Markers of neurodegeneration in idiopathic rapid eye movement sleep behaviour disorder and Parkinson’s disease. Brain 132:3298–3307

    Article  CAS  PubMed  Google Scholar 

  24. Jennum P, Mayer G, Ju YE, Postuma R (2013) Morbidities in rapid eye movement sleep behavior disorders. Sleep Med 14:782–787

    Article  PubMed Central  PubMed  Google Scholar 

  25. Labate A, Salsone M, Novellino F, Morelli M, Sturniolo M, Gambardella A, Quattrone A (2011) Combined use of cardiac m-i123-iodobenzylguanidine scintigraphy and (1)(2)(3)I-fp-cit single photon emission computed tomography in older adults with rapid eye movement sleep behavior disorder. J Am Geriatr Soc 59:928–929

    Article  PubMed  Google Scholar 

  26. Miyamoto T, Miyamoto M, Inoue Y, Usui Y, Suzuki K, Hirata K (2006) Reduced cardiac 123I-MIBG scintigraphy in idiopathic REM sleep behavior disorder. Neurology 67:2236–2238

    Article  CAS  PubMed  Google Scholar 

  27. Frauscher B, Nomura T, Duerr S, Ehrmann L, Gschliesser V, Wenning GK, Wolf E, Inoue Y, Högl B, Poewe W (2012) Investigation of autonomic function in idiopathic REM sleep behavior disorder. J Neurol 259:1056–1061

    Article  PubMed  Google Scholar 

  28. Kashihara K, Imamura T, Shinya T (2010) Cardiac 123I-MIBG uptake is reduced more markedly in patients with REM sleep behavior disorder than in those with early stage Parkinson’s disease. Parkinsonism Relat Disord 16:252–255

    Article  PubMed  Google Scholar 

  29. Nomura T, Inoue Y, Kagimura T, Nakashima K (2013) Clinical significance of REM sleep behavior disorder in Parkinson’s disease. Sleep Med 14:131–135

    Article  PubMed  Google Scholar 

  30. Romenets SR, Gagnon JF, Latreille V, Panniset M, Chouinard S, Montplaisir J, Postuma RB (2012) Rapid eye movement sleep behavior disorder and subtypes of Parkinson’s disease. Mov Disord 27:996–1003

    Article  PubMed  Google Scholar 

  31. Abbott RD, Petrovitch H, White LR, Masaki KH, Tanner CM, Curb JD, Grandinetti A, Blanchette PL, Popper JS, Ross GW (2001) Frequency of bowel movements and the future risk of Parkinson’s disease. Neurology 57:456–462

    Article  CAS  PubMed  Google Scholar 

  32. Braak H, de Vos RA, Bohl J, Del Tredici K (2006) Gastric alpha-synuclein immunoreactive inclusions in Meissner’s and Auerbach’s plexuses in cases staged for Parkinson’s disease-related brain pathology. Neurosci Lett 396:67–72

    Article  CAS  PubMed  Google Scholar 

  33. Wakabayashi K, Takahashi H, Takeda S, Ohama E, Ikuta F (1989) Lewy bodies in the enteric nervous system in Parkinson’s disease. Arch Histol Cytol 52:191–194

    Article  PubMed  Google Scholar 

  34. Nihei K, Takahashi A, Koto B, Mihara B, Morita Y, Isozumi K, Ohta K, Muramatsu K, Gotoh J, Yamaguchi K, Tomita Y, Sato H, Seki M, Iwasawa S, Suzuki N (2012) REM sleep behavior disorder in Japanese patients with Parkinson’s disease: a multicenter study using the REM sleep behavior disorder screening questionnaire. J Neurol 259:1606–1612

    Article  PubMed  Google Scholar 

  35. Unger MM, Möller JC, Mankel K, Schmittinger K, Eggert KM, Stamelou M, Stiasny-Kolster K, Bohne K, Bodden M, Mayer G, Oertel WH, Tebbe JJ (2011) Patients with idiopathic rapid-eye-movement sleep behavior disorder show normal gastric motility assessed by the 13C-octanoate breath test. Mov Disord 26:2559–2563

    Article  PubMed  Google Scholar 

  36. Unger MM, Möller JC, Mankel K, Eggert KM, Bohne K, Bodden M, Stiasny-Kolster K, Kann PH, Mayer G, Tebbe JJ, Oertel WH (2011) Postprandial ghrelin response is reduced in patients with Parkinson’s disease and idiopathic REM sleep behaviour disorder: a peripheral biomarker for early Parkinson’s disease? J Neurol 258:982–990

    Article  CAS  PubMed  Google Scholar 

Download references

Conflicts of interest

The authors report no disclosures relevant to the manuscript. L. Ferini-Strambi has received honoraria for serving on scientific advisory boards from UCB, Mundipharma, Menarini. Full financial disclosure for the previous 12 months W. Oertel has received honoraria for consultancy and for serving on scientific advisory boards; travel support from UCB; and honoraria for consultancy and lecture fees from Teva, Novartis, GlaxoSmithKline, Boehringer Ingelheim, Orion Pharma, and Merck Serono. Y. Dauvilliers has received funds for speaking and board engagements with UCB, Cephalon, Jazz, and Bioprojet. R.B. Postuma has received research funds from the Canadian Institute of Health Research, Fonds de la Recherche en Sante Quebec, The Webster Foundation, and the Drummond Foundation, as well as funds for travel and speaker fees from Novartis Canada and Teva Neurosciences. A. Iranzo had speaking and board engagements with UCB and Sanofi-Synthelabo. I Arnulf received honoraria for a speaking engagement and board from UCB Pharma. I. Arnulf received honoraria from UCB Pharma and Jazz for a speaking engagement and consultancy. B. Hogl has received honoraria for speaking, serving on an advisory board, or consulting from UCB, Mundipharma, BI, GSK, Respironics, Sanofi, Lundbeck, and Jazz; and a grant to institution from UCB, and travel support from Habel Medizintechnik and Vivisol, Austria. K. Sonka served on a scientific advisory board for UCB Pharma, received lecture fees from Ipsen, Pfizer, UCB Pharma, and GlaxoSmithKline, and participated in clinical trials managed by UCB Pharma, Bioprojet, and Eisai; and received research support from Charles University in Prague (PRVOUK P26/LF1/4). B. Frauscher has had speaking engagements with UCB and received a competitive research grant from the Austrian Science Fund (KLI 236), grant of the Nationalbank of Austria (15127). M. Unger received grants from the Micheal J. Fox Foundation for Parkinson’s Research and from the International Parkinson Fonds Germany. K. Stiasny-Kolster has received honoraria for serving on the scientific advisory boards for Boehringer Ingelheim, and UCB, and has received honoraria for speaking engagements sponsored by UCB and Boehringer Ingelheim. J. Montplaisir received funds from Merck and GlaxoSmithKline, and has received honoraria for consultancy from Jazz, Merck, Valeant, Servier, and Impac laboratories. S. Marelli, R. Manni, T. Miyamoto, M.L. Fantini, M. Puligheddu, P. Jennum, J. Santamaria, M. Zucconi, M.V·P. Rancoita, S. Leu-Semenesceu, M. Terzaghi, M. Miyamoto, A. Desautels, C. Wolfson, and A. Pelletier have nothing to disclose.

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Authors and Affiliations

  1. Department of Clinical Neuroscience, Sleep Disorders Center, Università Vita-Salute San Raffaele, Via Stamira d’ Ancona 20, 20127, Milan, Italy

    Luigi Ferini-Strambi, Sara Marelli & Marco Zucconi

  2. Department of Neurology, Philipps-University, Marburg, Marburg, Germany

    Wolfgang Oertel & Karin Stiasny-Kolster

  3. Neurological Department, University Hospital, Montpellier, France

    Yves Dauvilliers

  4. Centre d’Études Avancées en Médecine du Sommeil, Hôpital du Sacré-Cœur de Montréal, Montreal, Canada

    Ronald B. Postuma, Alex Desautels, Amélie Pelletier & Jacques Montplaisir

  5. Neurology Service, Hospital clinic de Barcelona, Barcelona, Spain

    Alex Iranzo & Joan Santamaria

  6. Unité des pathologies du sommeil, Hôpital Pitié-Salpêtrière, APHP and Inserm U975-CRICM-Pierre and Marie Curie University, Paris Cedex 13, France

    Isabelle Arnulf & Smeranda Leu-Semenescu

  7. Department of Neurology, Innsbruck Medical University, Innsbruck, Austria

    Högl Birgit & Birgit Frauscher

  8. Sleep and Epilepsy Unit, IRCCS C. Mondino National Institute of Neurology Foundation, Pavia, Italy

    Raffaele Manni & Michele Terzaghi

  9. Department of Neurology, Dokkyo Medical University Koshigaya Hospital, Koshigaya, Saitama, Japan

    Tomoyuki Miyamoto & Masayuki Miyamoto

  10. Department of Neurosciences, Sleep Disorders Center, University of Turin, Ospedale San Giovanni Battista–Molinette, Turin, Italy

    Maria-Livia Fantini

  11. Department of Cardiovascular and Neurological Sciences, Sleep Center, University of Cagliari, Cagliari, CA, Italy

    Monica Puligheddu

  12. Danish Center for Sleep Medicine, University of Copenhagen, Copenhagen, Denmark

    Poul Jennum

  13. Department of Neurology and Center of Clinical Neuroscience, First Faculty of Medicine and General University Hospital in Prague, Charles University in Prague, Prague, Czech Republic

    Karel Sonka

  14. CUSSB (University Centre for Statistics in the Biomedical Sciences), Vita-Salute San Raffaele University, Milan, Italy

    Paola M. V. Rancoita

  15. Department of Neurology, Saarland University Homburg/Saar, Saar, Germany

    Marcus Unger

  16. Department of Epidemiology, Biostatistics and Occupational Health, McGill University, Montreal, Canada

    Christina Wolfson

Authors
  1. Luigi Ferini-Strambi
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  2. Wolfgang Oertel
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  3. Yves Dauvilliers
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  4. Ronald B. Postuma
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  5. Sara Marelli
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  6. Alex Iranzo
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  7. Isabelle Arnulf
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  8. Högl Birgit
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  9. Raffaele Manni
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  10. Tomoyuki Miyamoto
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  11. Maria-Livia Fantini
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  12. Monica Puligheddu
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  13. Poul Jennum
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  14. Karel Sonka
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  15. Joan Santamaria
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  16. Marco Zucconi
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  17. Paola M. V. Rancoita
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  18. Smeranda Leu-Semenescu
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  19. Birgit Frauscher
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  20. Michele Terzaghi
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  21. Masayuki Miyamoto
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  22. Marcus Unger
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  23. Karin Stiasny-Kolster
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  24. Alex Desautels
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  25. Christina Wolfson
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  26. Amélie Pelletier
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  27. Jacques Montplaisir
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Corresponding author

Correspondence to Luigi Ferini-Strambi.

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Ferini-Strambi, L., Oertel, W., Dauvilliers, Y. et al. Autonomic symptoms in idiopathic REM behavior disorder: a multicentre case–control study. J Neurol 261, 1112–1118 (2014). https://doi.org/10.1007/s00415-014-7317-8

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  • DOI: https://doi.org/10.1007/s00415-014-7317-8

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