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Neuroscience Bulletin

, Volume 33, Issue 5, pp 576–584 | Cite as

Clinical Significance of REM Sleep Behavior Disorders and Other Non-motor Symptoms of Parkinsonism

  • Hong Jin
  • Jin-Ru Zhang
  • Yun Shen
  • Chun-Feng LiuEmail author
Review

Abstract

Rapid eye movement sleep behavior disorder (RBD) is one of the most common non-motor symptoms of parkinsonism, and it may serve as a prodromal marker of neurodegenerative disease. The mechanism underlying RBD is unclear. Several prospective studies have reported that specific non-motor symptoms predict a conversion risk of developing a neurodegenerative disease, including olfactory dysfunction, abnormal color vision, autonomic dysfunction, excessive daytime sleepiness, depression, and cognitive impairment. Parkinson’s disease (PD) with RBD exhibits clinical heterogeneity with respect to motor and non-motor symptoms compared with PD without RBD. In this review, we describe the main clinical and pathogenic features of RBD, focusing on its association with other non-motor symptoms of parkinsonism.

Keywords

Parkinson’s disease Rapid eye movement sleep behavior disorder Risk factors Parkinsonism 

Notes

Acknowledgements

This review was supported by the National Natural Science Foundation of China (91649114), the Jiangsu Provincial Special Program of Medical Science, China (BL2014042), a Jiangsu Provincial Medical Key Discipline Project, the Suzhou Clinical Research Center of Neurological Disease (Szzx201503), Jiangsu Province Ordinary University Professional Degree Graduate Practice Innovation, China (SJZZ16-0242), and the Priority Academic Program Development of Jiangsu Higher Education Institutions, China.

References

  1. 1.
    Postuma RB, Gagnon JF, Vendette M, Fantini ML, Massicotte-Marquez J, Montplaisir J. Quantifying the risk of neurodegenerative disease in idiopathic REM sleep behavior disorder. Neurology 2009, 72: 1296–1300.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Mahlknecht P, Seppi K, Frauscher B, Kiechl S, Willeit J, Stockner H, et al. Probable RBD and association with neurodegenerative disease markers: A population-based study. Mov Disord 2015, 30: 1417–1421.CrossRefPubMedGoogle Scholar
  3. 3.
    Kang SH, Yoon IY, Lee SD, Han JW, Kim TH, Kim KW. REM sleep behavior disorder in the Korean elderly population: prevalence and clinical characteristics. Sleep 2013, 36: 1147–1152.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Iranzo A, Fernández-Arcos A, Tolosa E, Serradell M, Molinuevo JL, Valldeoriola F, et al. Neurodegenerative disorder risk in idiopathic REM sleep behavior disorder: study in 174 patients. PLoS One 2014, 9: e89741.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Berg D, Postuma RB, Adler CH, Bloem BR, Chan P, Dubois B, et al. MDS research criteria for prodromal Parkinson’s disease. Mov Disord 2015, 30: 1600–1611.CrossRefPubMedGoogle Scholar
  6. 6.
    Gagnon JF, Bédard MA, Fantini ML, Petit D, Panisset M, Rompré S, et al. REM sleep behavior disorder and REM sleep without atonia in Parkinson’s disease. Neurology 2002, 59: 585–589.CrossRefPubMedGoogle Scholar
  7. 7.
    Sixel-Döring F, Trautmann E, Mollenhauer B, Trenkwalder C. Associated factors for REM sleep behavior disorder in Parkinson disease. Neurology 2011, 77: 1048–1054.CrossRefPubMedGoogle Scholar
  8. 8.
    Ferman TJ, Boeve BF, Smith GE, Lin SC, Silber MH, Pedraza O, et al. Inclusion of RBD improves the diagnostic classification of dementia with Lewy bodies. Neurology 2011, 77: 875–882.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Vetrugno R, Provini F, Cortelli P, Plazzi G, Lotti EM, Pierangeli G, et al. Sleep disorders in multiple system atrophy: a correlative video-polysomnographic study. Sleep Med 2004, 5: 21–30.CrossRefPubMedGoogle Scholar
  10. 10.
    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: 1117–1121.CrossRefPubMedGoogle Scholar
  11. 11.
    Nomura T, Inoue Y, Kagimura T, Nakashima K. Clinical significance of REM sleep behavior disorder in Parkinson’s disease. Sleep Med 2013, 14: 131–135.CrossRefPubMedGoogle Scholar
  12. 12.
    Gong Y, Xiong KP, Mao CJ, Shen Y, Hu WD, Huang JY, et al. Clinical manifestations of Parkinson disease and the onset of rapid eye movement sleep behavior disorder. Sleep Med 2014, 15: 647–653.CrossRefPubMedGoogle Scholar
  13. 13.
    Ito E, Inoue Y. The International Classification of Sleep Disorders, third edition. American Academy of Sleep Medicine. Includes bibliographies and index. Nihon Rinsho 2015, 73: 916–923. [Article in Japanese]PubMedGoogle Scholar
  14. 14.
    Figorilli M, Ferri R, Zibetti M, Beudin P, Puligheddu M, Lopiano L, et al. Comparison between automatic and visual scorings of REM Sleep without atonia for the diagnosis of REM sleep behavior disorder in Parkinson disease. Sleep 2017, 4. doi:  10.1093/sleep/zsw060.
  15. 15.
    Shen Y, Xiong KP, Li J, Mao CJ, Chen J, He PC, et al. Clinical correlates of rapid eye movement sleep without atonia in Parkinson’s disease. Clin Neurophysiol 2015, 126: 1198–1203.CrossRefPubMedGoogle Scholar
  16. 16.
    Stiasny-Kolster K, Sixel-Döring F, Trenkwalder C, Heinzel-Gutenbrunner M, Seppi K, Poewe W, et al. Diagnostic value of the REM sleep behavior disorder screening questionnaire in Parkinson’s disease. Sleep Med 2015, 16: 186–189.CrossRefPubMedGoogle Scholar
  17. 17.
    Li SX, Wing YK, Lam SP, Zhang J, Yu MW, Ho CK, et al. Validation of a new REM sleep behavior disorder questionnaire (RBDQ-HK). Sleep Med 2010, 11: 43–48.CrossRefPubMedGoogle Scholar
  18. 18.
    Shen SS, Shen Y, Xiong KP, Chen J, Mao CJ, Huang JY, et al. Validation study of REM sleep behavior disorder questionnaire-Hong Kong (RBDQ-HK) in east China. Sleep Med 2014, 15: 952–958.CrossRefPubMedGoogle Scholar
  19. 19.
    Postuma RB, Arnulf I, Hogl B, Iranzo A, Miyamoto T, Dauvilliers Y, et al. A single-question screen for rapid eye movement sleep behavior disorder: a multicenter validation study. Mov Disord 2012, 27: 913–916.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Frauscher B, Ehrmann L, Zamarian L, Auer F, Mitterling T, Gabelia D, et al. Validation of the Innsbruck REM sleep behavior disorder inventory. Mov Disord 2012, 27: 1673–1678.CrossRefPubMedGoogle Scholar
  21. 21.
    Lu J, Sherman D, Devor M, Saper CB. A putative flip-flop switch for control of REM sleep. Nature 2006, 441: 589–594.CrossRefPubMedGoogle Scholar
  22. 22.
    Boissard R, Gervasoni D, Schmidt MH, Barbagli B, Fort P, Luppi PH. The rat ponto-medullary network responsible for paradoxical sleep onset and maintenance: a combined microinjection and functional neuroanatomical study. Eur J Neurosci 2002, 16: 1959–1973.CrossRefPubMedGoogle Scholar
  23. 23.
    Vilas D, Iranzo A, Tolosa E, Aldecoa I, Berenguer J, Vilaseca I, et al. Assessment of α-synuclein in submandibular glands of patients with idiopathic rapid-eye-movement sleep behaviour disorder: a case-control study. Lancet Neurol 2016, 15: 708–718.CrossRefPubMedGoogle Scholar
  24. 24.
    Boeve BF, Silber MH, Ferman TJ, Lin SC, Benarroch EE, Schmeichel AM, et al. Clinicopathologic correlations in 172 cases of rapid eye movement sleep behavior disorder with or without a coexisting neurologic disorder. Sleep Med 2013, 14: 754–762.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Postuma RB, Adler CH, Dugger BN, Hentz JG, Shill HA, Driver-Dunckley E, et al. REM sleep behavior disorder and neuropathology in Parkinson’s disease. Mov Disord 2015, 30: 1413–1417.CrossRefPubMedGoogle Scholar
  26. 26.
    Iranzo A, Molinuevo JL, Santamaría J, Serradell M, Martí MJ, Valldeoriola F, et al. Rapid-eye-movement sleep behaviour disorder as an early marker for a neurodegenerative disorder: a descriptive study. Lancet Neurol 2006, 5: 572–577.CrossRefPubMedGoogle Scholar
  27. 27.
    Claassen DO, Josephs KA, Ahlskog JE, Silber MH, Tippmann-Peikert M, Boeve BF. REM sleep behavior disorder preceding other aspects of synucleinopathies by up to half a century. Neurology 2010, 75: 494–499.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Schenck CH, Boeve BF, Mahowald MW. Delayed emergence of a parkinsonian disorder or dementia in 81% of older men initially diagnosed with idiopathic rapid eye movement sleep behavior disorder: a 16-year update on a previously reported series. Sleep Med 2013, 14: 744–748.CrossRefPubMedGoogle Scholar
  29. 29.
    Schrag A, Horsfall L, Walters K, Noyce A, Petersen I. Prediagnostic presentations of Parkinson’s disease in primary care: a case-control study. Lancet Neurol 2015, 14: 57–64.CrossRefPubMedGoogle Scholar
  30. 30.
    Iranzo A, Santamaría J, Rye DB, Valldeoriola F, Martí MJ, Muñoz E, et al. Characteristics of idiopathic REM sleep behavior disorder and that associated with MSA and PD. Neurology 2005, 65: 247–252.CrossRefPubMedGoogle Scholar
  31. 31.
    Postuma RB, Gagnon JF, Bertrand JA, Génier MD, Montplaisir JY. Parkinson risk in idiopathic REM sleep behavior disorder: preparing for neuroprotective trials. Neurology 2015, 84: 1104–1113.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Iranzo A, Stockner H, Serradell M, Seppi K, Valldeoriola F, Frauscher B, et al. Five-year follow-up of substantia nigra echogenicity in idiopathic REM sleep behavior disorder. Mov Disord 2014, 29: 1774–1780.CrossRefPubMedGoogle Scholar
  33. 33.
    Miyamoto T, Miyamoto M, Iwanami M, Hirata K, Kobayashi M, Nakamura M, et al. Olfactory dysfunction in idiopathic REM sleep behavior disorder. Sleep Med 2010, 11: 458–461.CrossRefPubMedGoogle Scholar
  34. 34.
    Stiasny-Kolster K, Doerr Y, Möller JC, Höffken H, Behr TM, Oertel WH, et al. Combination of ‘idiopathic’ REM sleep behaviour disorder and olfactory dysfunction as possible indicator for alpha-synucleinopathy demonstrated by dopamine transporter FP-CIT-SPECT. Brain 2005, 128: 126–137.CrossRefPubMedGoogle Scholar
  35. 35.
    Mahlknecht P, Iranzo A, Högl B, Frauscher B, Müller C, Santamaría J, et al. Olfactory dysfunction predicts early transition to a Lewy body disease in idiopathic RBD. Neurology 2015, 84: 654–658.CrossRefPubMedGoogle Scholar
  36. 36.
    Mazza S, Soucy JP, Gravel P, Michaud M, Postuma R, Massicotte-Marquez J, et al. Assessing whole brain perfusion changes in patients with REM sleep behavior disorder. Neurology 2006, 67: 1618–1622.CrossRefPubMedGoogle Scholar
  37. 37.
    Ross GW, Petrovitch H, Abbott RD, Tanner CM, Popper J, Masaki K, et al. Association of olfactory dysfunction with risk for future Parkinson’s disease. Ann Neurol 2008, 63: 167–173.CrossRefPubMedGoogle Scholar
  38. 38.
    Wang J, You H, Liu JF, Ni DF, Zhang ZX, Guan J. Association of olfactory bulb volume and olfactory sulcus depth with olfactory function in patients with Parkinson disease. AJNR Am J Neuroradiol 2011, 32: 677–681.CrossRefPubMedGoogle Scholar
  39. 39.
    Hoyles K, Sharma JC. Olfactory loss as a supporting feature in the diagnosis of Parkinson’s disease: a pragmatic approach. J Neurol 2013, 260: 2951–2958.CrossRefPubMedGoogle Scholar
  40. 40.
    Postuma RB, Gagnon JF, Vendette M, Desjardins C, Montplaisir JY. Olfaction and color vision identify impending neurodegeneration in rapid eye movement sleep behavior disorder. Ann Neurol 2011, 69: 811–818.CrossRefPubMedGoogle Scholar
  41. 41.
    Price MJ, Feldman RG, Adelberg D, Kayne H. Abnormalities in color vision and contrast sensitivity in Parkinson’s disease. Neurology 1992, 42: 887–890.CrossRefPubMedGoogle Scholar
  42. 42.
    Cardoso EF, Fregni F, Maia FM, Melo LM, Sato JR, Cruz AC, et al. Abnormal visual activation in Parkinson’s disease patients. Mov Disord 2010, 25: 1590–1596.CrossRefPubMedGoogle Scholar
  43. 43.
    Yang ZJ, Wei J, Mao CJ, Zhang JR, Chen J, Ji XY, et al. Retinal nerve fiber layer thinning: a window into rapid eye movement sleep behavior disorders in Parkinson’s disease. Sleep Breath 2016, 20: 1285–1292.CrossRefPubMedGoogle Scholar
  44. 44.
    Postuma RB, Gagnon JF, Vendette M, Montplaisir JY. Markers of neurodegeneration in idiopathic rapid eye movement sleep behaviour disorder and Parkinson’s disease. Brain 2009, 132: 3298–3307.CrossRefPubMedGoogle Scholar
  45. 45.
    Miyamoto T, Miyamoto M, Inoue Y, Usui Y, Suzuki K, Hirata K. Reduced cardiac 123I-MIBG scintigraphy in idiopathic REM sleep behavior disorder. Neurology 2006, 67: 2236–2238.CrossRefPubMedGoogle Scholar
  46. 46.
    Lanfranchi PA, Fradette L, Gagnon JF, Colombo R, Montplaisir J. Cardiac autonomic regulation during sleep in idiopathic REM sleep behavior disorder. Sleep 2007, 30: 1019–1025.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Valappil RA, Black JE, Broderick MJ, Carrillo O, Frenette E, Sullivan SS, et al. Exploring the electrocardiogram as a potential tool to screen for premotor Parkinson’s disease. Mov Disord 2010, 25: 2296–2303.CrossRefPubMedGoogle Scholar
  48. 48.
    Schmidt C, Herting B, Prieur S, Junghanns S, Schweitzer K, Globas C, et al. Valsalva manoeuvre in patients with different Parkinsonian disorders. J Neural Transm (Vienna) 2009, 116: 875–880.CrossRefGoogle Scholar
  49. 49.
    Friedrich C, Rüdiger H, Schmidt C, Herting B, Prieur S, Junghanns S, et al. Baroreflex sensitivity and power spectral analysis during autonomic testing in different extrapyramidal syndromes. Mov Disord 2010, 25: 315–324.CrossRefPubMedGoogle Scholar
  50. 50.
    Postuma RB, Gagnon JF, Pelletier A, Montplaisir J. Prodromal autonomic symptoms and signs in Parkinson’s disease and dementia with Lewy bodies. Mov Disord 2013, 28: 597–604.CrossRefPubMedGoogle Scholar
  51. 51.
    Pont-Sunyer C, Hotter A, Gaig C, Seppi K, Compta Y, Katzenschlager R, et al. The onset of nonmotor symptoms in Parkinson’s disease (the ONSET PD study). Mov Disord 2015, 30: 229–237.CrossRefPubMedGoogle Scholar
  52. 52.
    Khoo TK, Yarnall AJ, Duncan GW, Coleman S, O’Brien JT, Brooks DJ, et al. The spectrum of nonmotor symptoms in early Parkinson disease. Neurology 2013, 80: 276–281.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Gelpi E, Navarro-Otano J, Tolosa E, Gaig C, Compta Y, Rey MJ, et al. Multiple organ involvement by alpha-synuclein pathology in Lewy body disorders. Mov Disord 2014, 29: 1010–1018.CrossRefPubMedGoogle Scholar
  54. 54.
    Iranzo A, Gelpi E, Tolosa E, Molinuevo JL, Serradell M, Gaig C, et al. Neuropathology of prodromal Lewy body disease. Mov Disord 2014, 29: 410–415.CrossRefPubMedGoogle Scholar
  55. 55.
    Eschweiler J, Stromps JP, Fischer M, Schick F, Rath B, Pallua N, et al. A biomechanical model of the wrist joint for patient-specific model guided surgical therapy: Part 2. Proc Inst Mech Eng H 2016, 230: 326–334.CrossRefPubMedGoogle Scholar
  56. 56.
    Kim JS, Park HE, Oh YS, Lee SH, Park JW, Son BC, et al. Orthostatic hypotension and cardiac sympathetic denervation in Parkinson disease patients with REM sleep behavioral disorder. J Neurol Sci 2016, 362: 59–63.CrossRefPubMedGoogle Scholar
  57. 57.
    Goldstein DS, Holmes C, Sharabi Y, Wu T. Survival in synucleinopathies: A prospective cohort study. Neurology 2015, 85: 1554–1561.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Maetzler W, Liepelt I, Berg D. Progression of Parkinson’s disease in the clinical phase: potential markers. Lancet Neurol 2009, 8: 1158–1171.CrossRefPubMedGoogle Scholar
  59. 59.
    Braak H, Del TK, Rüb U, de Vos RA, Jansen SEN, Braak E. Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24: 197–211.Google Scholar
  60. 60.
    Bonakis A, Howard RS, Ebrahim IO, Merritt S, Williams A. REM sleep behaviour disorder (RBD) and its associations in young patients. Sleep Med 2009, 10: 641–645.CrossRefPubMedGoogle Scholar
  61. 61.
    Arnulf I, Konofal E, Merino-Andreu M, Houeto JL, Mesnage V, Welter ML, et al. Parkinson’s disease and sleepiness: an integral part of PD. Neurology 2002, 58: 1019–1024.CrossRefPubMedGoogle Scholar
  62. 62.
    Abbott RD, Ross GW, White LR, Tanner CM, Masaki KH, Nelson JS, et al. Excessive daytime sleepiness and subsequent development of Parkinson disease. Neurology 2005, 65: 1442–1446.CrossRefPubMedGoogle Scholar
  63. 63.
    Arnulf I, Neutel D, Herlin B, Golmard JL, Leu-Semenescu S, de Cock V C, et al. Sleepiness in idiopathic REM sleep behavior disorder and Parkinson disease. Sleep 2015, 38: 1529–1535.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Hobson DE, Lang AE, Martin WR, Razmy A, Rivest J, Fleming J. Excessive daytime sleepiness and sudden-onset sleep in Parkinson disease: a survey by the Canadian Movement Disorders Group. JAMA 287: 455–463.Google Scholar
  65. 65.
    Moreno-López C, Santamaría J, Salamero M, Del SF, Albanese A, Pellecchia MT, et al. Excessive daytime sleepiness in multiple system atrophy (SLEEMSA study). Arch Neurol 2011, 68: 223–230.CrossRefPubMedGoogle Scholar
  66. 66.
    Rongve A, Boeve BF, Aarsland D. Frequency and correlates of caregiver-reported sleep disturbances in a sample of persons with early dementia. J Am Geriatr Soc 2010, 58: 480–486.CrossRefPubMedGoogle Scholar
  67. 67.
    Teman PT, Tippmann-Peikert M, Silber MH, Slocumb NL, Auger RR. Idiopathic rapid-eye-movement sleep disorder: associations with antidepressants, psychiatric diagnoses, and other factors, in relation to age of onset. Sleep Med 2009, 10: 60–65.CrossRefPubMedGoogle Scholar
  68. 68.
    Ju YE, Larson-Prior L, Duntley S. Changing demographics in REM sleep behavior disorder: possible effect of autoimmunity and antidepressants. Sleep Med 2011, 12: 278–283.CrossRefPubMedGoogle Scholar
  69. 69.
    Vilas D, Iranzo A, Pont-Sunyer C, Serradell M, Gaig C, Santamaria J, et al. Brainstem raphe and substantia nigra echogenicity in idiopathic REM sleep behavior disorder with comorbid depression. J Neurol 2015, 262: 1665–1672.CrossRefPubMedGoogle Scholar
  70. 70.
    Alonso A, Rodríguez LA, Logroscino G, Hernán MA. Use of antidepressants and the risk of Parkinson’s disease: a prospective study. J Neurol Neurosurg Psychiatry 2009, 80: 671–674.CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Reijnders JS, Ehrt U, Weber WE, Aarsland D, Leentjens AF. A systematic review of prevalence studies of depression in Parkinson’s disease. Mov Disord 2008, 23: 183–189; quiz 313.Google Scholar
  72. 72.
    Postuma RB, Aarsland D, Barone P, Burn DJ, Hawkes CH, Oertel W, et al. Identifying prodromal Parkinson’s disease: pre-motor disorders in Parkinson’s disease. Mov Disord 2012, 27: 617–626.CrossRefPubMedGoogle Scholar
  73. 73.
    Terzaghi M, Sinforiani E, Zucchella C, Zambrelli E, Pasotti C, Rustioni V, et al. Cognitive performance in REM sleep behaviour disorder: a possible early marker of neurodegenerative disease. Sleep Med 2008, 9: 343–351.CrossRefPubMedGoogle Scholar
  74. 74.
    Ferini-Strambi L. Does idiopathic REM sleep behavior disorder (iRBD) really exist? What are the potential markers of neurodegeneration in iRBD. Sleep Med 2011, 12 Suppl 2: S43–49.CrossRefPubMedGoogle Scholar
  75. 75.
    Gagnon JF, Vendette M, Postuma RB, Desjardins C, Massicotte-Marquez J, Panisset M, et al. Mild cognitive impairment in rapid eye movement sleep behavior disorder and Parkinson’s disease. Ann Neurol 2009, 66: 39–47.CrossRefPubMedGoogle Scholar
  76. 76.
    Delazer M, Högl B, Zamarian L, Wenter J, Ehrmann L, Gschliesser V, et al. Decision making and executive functions in REM sleep behavior disorder. Sleep 2012, 35: 667–673.CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Manni R, Sinforiani E, Pacchetti C, Zucchella C, Cremascoli R, Terzaghi M. Cognitive dysfunction and REM sleep behavior disorder: key findings in the literature and preliminary longitudinal findings. Int J Psychophysiol 2013, 89: 213–217.CrossRefPubMedGoogle Scholar
  78. 78.
    Yarnall A, Rochester L, Burn DJ. The interplay of cholinergic function, attention, and falls in Parkinson’s disease. Mov Disord 2011, 26: 2496–2503.CrossRefPubMedGoogle Scholar
  79. 79.
    Poletti M, Frosini D, Pagni C, Baldacci F, Nicoletti V, Tognoni G, et al. Mild cognitive impairment and cognitive-motor relationships in newly diagnosed drug-naive patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 2012, 83: 601–606.CrossRefPubMedGoogle Scholar
  80. 80.
    Levy G, Jacobs DM, Tang MX, Côté LJ, Louis ED, Alfaro B, et al. Memory and executive function impairment predict dementia in Parkinson’s disease. Mov Disord 2002, 17: 1221–1226.CrossRefPubMedGoogle Scholar
  81. 81.
    Zhang JR, Chen J, Yang ZJ, Zhang HJ, Fu YT, Shen Y, et al. Rapid eye movement sleep behavior disorder symptoms correlate with domains of cognitive impairment in Parkinson’s disease. Chin Med J (Engl) 2016, 129: 379–385.CrossRefGoogle Scholar
  82. 82.
    Rupprecht S, Walther B, Gudziol H, Steenbeck J, Freesmeyer M, Witte OW, et al. Clinical markers of early nigrostriatal neurodegeneration in idiopathic rapid eye movement sleep behavior disorder. Sleep Med 2013, 14: 1064–1070.CrossRefPubMedGoogle Scholar
  83. 83.
    Iranzo A, Valldeoriola F, Lomeña F, Molinuevo JL, Serradell M, Salamero M, et al. Serial dopamine transporter imaging of nigrostriatal function in patients with idiopathic rapid-eye-movement sleep behaviour disorder: a prospective study. Lancet Neurol 2011, 10: 797–805.CrossRefPubMedGoogle Scholar
  84. 84.
    Scherfler C, Frauscher B, Schocke M, Iranzo A, Gschliesser V, Seppi K, et al. White and gray matter abnormalities in idiopathic rapid eye movement sleep behavior disorder: a diffusion-tensor imaging and voxel-based morphometry study. Ann Neurol 2011, 69: 400–407.CrossRefPubMedGoogle Scholar
  85. 85.
    Hanyu H, Inoue Y, Sakurai H, Kanetaka H, Nakamura M, Miyamoto T, et al. Voxel-based magnetic resonance imaging study of structural brain changes in patients with idiopathic REM sleep behavior disorder. Parkinsonism Relat Disord 2012, 18: 136–139.CrossRefPubMedGoogle Scholar
  86. 86.
    Rolinski M, Griffanti L, Piccini P, Roussakis AA, Szewczyk-Krolikowski K, Menke RA, et al. Basal ganglia dysfunction in idiopathic REM sleep behaviour disorder parallels that in early Parkinson’s disease. Brain 2016, 139: 2224–2234.CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Iranzo A, Lomeña F, Stockner H, Valldeoriola F, Vilaseca I, Salamero M, et al. Decreased striatal dopamine transporter uptake and substantia nigra hyperechogenicity as risk markers of synucleinopathy in patients with idiopathic rapid-eye-movement sleep behaviour disorder: a prospective study [corrected]. Lancet Neurol 2010, 9: 1070–1077.CrossRefPubMedGoogle Scholar
  88. 88.
    Gan-Or Z, Mirelman A, Postuma RB, Arnulf I, Bar-Shira A, Dauvilliers Y, et al. GBA mutations are associated with Rapid Eye Movement Sleep Behavior Disorder. Ann Clin Transl Neurol 2015, 2: 941–945.CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Beavan M, McNeill A, Proukakis C, Hughes DA, Mehta A, Schapira AH. Evolution of prodromal clinical markers of Parkinson disease in a GBA mutation-positive cohort. JAMA Neurol 2015, 72: 201–208.CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Gan-Or Z, Girard SL, Noreau A, Leblond CS, Gagnon JF, Arnulf I, et al. Parkinson’s disease genetic loci in rapid eye movement sleep behavior disorder. J Mol Neurosci 2015, 56: 617–622.CrossRefPubMedGoogle Scholar
  91. 91.
    Saunders-Pullman R, Alcalay RN, Mirelman A, Wang C, Luciano MS, Ortega RA, et al. REM sleep behavior disorder, as assessed by questionnaire, in G2019S LRRK2 mutation PD and carriers. Mov Disord 2015, 30: 1834–1839.CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Fernández-Santiago R, Iranzo A, Gaig C, Serradell M, Fernández M, Tolosa E, et al. Absence of LRRK2 mutations in a cohort of patients with idiopathic REM sleep behavior disorder. Neurology 2016, 86: 1072–1073.CrossRefPubMedGoogle Scholar
  93. 93.
    Mirelman A, Alcalay RN, Saunders-Pullman R, Yasinovsky K, Thaler A, Gurevich T, et al. Nonmotor symptoms in healthy Ashkenazi Jewish carriers of the G2019S mutation in the LRRK2 gene. Mov Disord 2015, 30: 981–986.CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Ehrminger M, Leu-Semenescu S, Cormier F, Corvol JC, Vidailhet M, Debellemaniere E, et al. Sleep aspects on video-polysomnography in LRRK2 mutation carriers. Mov Disord 2015, 30: 1839–1843.CrossRefPubMedGoogle Scholar
  95. 95.
    Bergareche A, Rodríguez-Oroz MC, Estanga A, Gorostidi A, de Munain A L, Castillo-Triviño T, et al. DAT imaging and clinical biomarkers in relatives at genetic risk for LRRK2 R1441G Parkinson’s disease. Mov Disord 2016, 31: 335–343.CrossRefPubMedGoogle Scholar
  96. 96.
    Konno T, Ross OA, Puschmann A, Dickson DW, Wszolek ZK. Autosomal dominant Parkinson’s disease caused by SNCA duplications. Parkinsonism Relat Disord 2016, 22 Suppl 1: S1–6.CrossRefPubMedGoogle Scholar
  97. 97.
    Papadimitriou D, Antonelou R, Miligkos M, Maniati M, Papagiannakis N, Bostantjopoulou S, et al. Motor and nonmotor features of carriers of the p.A53T alpha-synuclein mutation: a longitudinal study. Mov Disord 2016, 31: 1226–1230.CrossRefPubMedGoogle Scholar

Copyright information

© Shanghai Institutes for Biological Sciences, CAS and Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  • Hong Jin
    • 1
  • Jin-Ru Zhang
    • 1
  • Yun Shen
    • 1
  • Chun-Feng Liu
    • 1
    • 2
    Email author
  1. 1.Department of Neurology and Sleep CenterThe Second Affiliated Hospital of Soochow UniversitySuzhouChina
  2. 2.Institute of NeuroscienceSoochow UniversitySuzhouChina

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