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Non-motor symptoms are associated with REM sleep behavior disorder in Parkinson’s disease: a systematic review and meta-analysis

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Abstract

Objective

Parkinson’s disease (PD) is usually accompanied by rapid eye movement sleep behavior disorder (RBD). A systematic review has concluded that motor manifestations are associated with RBD in PD patients, but whether the same is true of non-motor symptoms is unclear.

Methods

A systematic review and meta-analysis was conducted by searching studies related to PD and RBD in PubMed, Web of Science, Embase, and Cochrane databases. Data were pooled where appropriate and used to calculate odds ratios (ORs), mean differences (MDs), or standardized mean differences (SMDs) with 95% confidence intervals (CI). Heterogeneity was assessed using the I2 statistic.

Results

PD patients with RBD were more likely to be male (OR 1.26, 95% CI 1.14–1.40) and older (MD 1.70 years, 95% CI 1.24–2.16) than those of patients without RBD. Patients with RBD were at a higher risk of non-motor symptoms such as constipation (OR 1.94, 95% CI 1.57–2.38), hallucination (OR 2.62, 95% CI 2.01–3.41), depression (SMD 0.39, 95% CI 0.25–0.53), and cognitive impairment (SMD − 0.29, 95% CI − 0.42 to − 0.17) based on standardized questionnaire scores. Similarly, PD patients with RBD suffered more severe motor symptoms and required higher doses of levodopa therapy.

Conclusions

The available evidence suggests that PD patients with RBD suffer severer non-motor and motor symptoms than those without RBD. A potential explanation is that PD patients with RBD present more diffuse neurodegeneration.

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References

  1. Boeve BF (2013) Idiopathic REM sleep behaviour disorder in the development of Parkinson’s disease. Lancet Neurol 12:469–482. https://doi.org/10.1016/S1474-4422(13)70054-1

    Article  PubMed  PubMed Central  Google Scholar 

  2. Morley JF, Hurtig HI (2010) Current understanding and management of Parkinson disease. Neurology 75:S9–S15. https://doi.org/10.1212/WNL.0b013e3181fb3628

    Article  PubMed  Google Scholar 

  3. Kalia LV, Lang AE (2015) Parkinson’s disease. Lancet 386:896–912. https://doi.org/10.1016/S0140-6736(14)61393-3

    Article  CAS  PubMed  Google Scholar 

  4. Berg D, Postuma RB, Adler CH, Bloem BR (2015) MDS research criteria for prodromal Parkinson’s disease key definition features of prodromal PD. Mov Disord 301:600–1609. https://doi.org/10.1002/mds.26431

    Article  Google Scholar 

  5. Schenck CH, Mahowald MW (2002) REM sleep behavior disorder: clinical, developmental, and neuroscience perspectives 16 years after its formal identification in sleep. Sleep 25:120–138. https://doi.org/10.1093/sleep/25.2.120

    Article  PubMed  Google Scholar 

  6. Schenck CH, Boeve BF, Mahowald MW (2013) 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 14:744–748. https://doi.org/10.1016/j.sleep.2012.10.009

    Article  PubMed  Google Scholar 

  7. Braak H, Tredici KD, Rüb D, De Vos RAI, Jansen ENH, Braak E (2003) Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol. Aging 24:197–211. https://doi.org/10.1016/S0197-4580(02)00065-9

    Article  PubMed  Google Scholar 

  8. Salsone M, Cerasa A, Arabia G et al (2014) Reduced thalamic volume in Parkinson disease with REM sleep behavior disorder: volumetric study. Parkinsonism Relat Disord 20:1004–1008

    Article  CAS  Google Scholar 

  9. Comella CL, Nardine TM, Diederich NJ, Stebbins GT (1998) Sleep-related violence, injury, and REM sleep behavior disorder in Parkinson’s disease. Neurology 51:526–529. https://doi.org/10.1212/WNL.51.2.526

    Article  CAS  PubMed  Google Scholar 

  10. Arnaldi D, Morbelli S, Brugnolo A, Girtler N, Picco A, Ferrara M, Accardo J, Buschiazzo A, de Carli F, Pagani M, Nobili F (2016) Functional neuroimaging and clinical features of drug naive patients with de novo Parkinson’s disease and probable RBD. Park Relat Disord 29:47–53. https://doi.org/10.1016/j.parkreldis.2016.05.031

    Article  Google Scholar 

  11. Haba-rubio J, Frauscher B, Marques-vidal P, Toriel J, Tobback N, Andries D, Preisig M, Vollenweider P, Postuma R, Heinzer R (2018) Prevalence and determinants of rapid eye movement sleep behavior disorder in the general population. Sleep 41:1–8. https://doi.org/10.1093/sleep/zsx197

    Article  Google Scholar 

  12. Zhu RL, Xie CJ, Hu PP, Wang K (2017) Clinical variations in Parkinson’s disease patients with or without REM sleep behaviour disorder: a meta-analysis. Sci Rep 7:1–8. https://doi.org/10.1038/srep40779

    Article  CAS  Google Scholar 

  13. Gelb DJ, Oliver E, Gilman S (1999) Diagnostic criteria for Parkinson disease. Arch Neurol 56(1):33–39

    Article  CAS  Google Scholar 

  14. Larsen JP, Dupont E, Tandberg E (1994) Clinical diagnosis of Parkinson’s disease. Proposal of diagnostic subgroups classified at different levels of confidence. Acra Neurol Scond 89:242–251

    Article  CAS  Google Scholar 

  15. Rostom A, Dube C, Cranney A. et al. (2004) Celiac disease. Rockville (MD): Agency for Healthcare Research and Quality (US); (Evidence Reports/Technology Assessments, No. 104.) Appendix D. Quality Assessment Forms.http://www.ncbi.nlm.nih.gov/books/NBK35156

  16. Wells GA, Shea B, O’Connell D, Peterson J, Welch V, Losos M, Tugwell P (2012) NewCastle-Ottawa Quality Assessment Scale [EB/OL]. http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp

  17. Postuma RB, Gagnon JF, Vendette M, Charland K, Montplaisir J (2008) Manifestations of Parkinson disease differ in association with REM sleep behavior disorder. Mov Disord 23:1665–1672. https://doi.org/10.1002/mds.22099

    Article  PubMed  Google Scholar 

  18. Postuma RB, Gagnon JF, Vendette M, Charland K, Montplaisir J (2008) REM sleep behaviour disorder in Parkinson’s disease is associated with specific motor features. J Neurol Neurosurg Psychiatry 79:1117–1121. https://doi.org/10.1136/jnnp.2008.149195

    Article  CAS  PubMed  Google Scholar 

  19. Fantini ML, Macedo L, Zibetti M, Sarchioto M, Vidal T, Pereira B, Marques A, Debilly B, Derost P, Ulla M, Vitello N, Cicolin A, Lopiano L, Durif F (2015) Increased risk of impulse control symptoms in Parkinson’s disease with rem sleep behaviour disorder. J Neurol Neurosurg Psychiatry 86:174–179. https://doi.org/10.1136/jnnp-2014-307904

    Article  CAS  PubMed  Google Scholar 

  20. Ferri R, Fulda S, Cosentino FII, Pizza F, Plazzi G (2012) A preliminary quantitative analysis of REM sleep chin EMG in Parkinson’s disease with or without REM sleep behavior disorder. Sleep Med 13:707–713. https://doi.org/10.1016/j.sleep.2012.01.003

    Article  PubMed  Google Scholar 

  21. Ford AH, Duncan GW, Firbank MJ, Yarnall AJ, Khoo TK, Burn DJ, O’Brien JT (2013) Rapid eye movement sleep behavior disorder in Parkinson’s disease: magnetic resonance imaging study. Mov Disord 28:832–836. https://doi.org/10.1002/mds.25367

    Article  PubMed  Google Scholar 

  22. Gomutbutra P, Kanjanaratanakorn K, Tiyapun N (2018) Prevalence and clinical characteristics of probable REM behavior disorder in Thai Parkinson’s disease patients. Parkinson’s Disease 2018:1–6. https://doi.org/10.1155/2018/7657191

    Article  Google Scholar 

  23. Janković M, Svetel M, Kostić V (2015) Frequency of REM sleep behavior disorders in patients with Parkinson’s disease. Vojnosanit Pregl 72:442–446. https://doi.org/10.2298/VSP130501006J

    Article  PubMed  Google Scholar 

  24. Lavault S, Leu-Semenescu S, Tezenas Du Montcel S, Cochen De Cock V, Vidailhet M, Arnulf I (2010) Does clinical rapid eye movement behavior disorder predict worse outcomes in Parkinson’s disease? J Neurol 257:1154–1159. https://doi.org/10.1007/s00415-010-5482-y

    Article  CAS  PubMed  Google Scholar 

  25. Leclair-Visonneau L, Clairembault T, Coron E, Dily SL, Vavasseur F, Dalichampt M, Péréon Y, Neunlist M, Derkinderen P (2017) REM sleep behavior disorder is related to enteric neuropathology in Parkinson disease. Neurology 89:1612–1618

    Article  Google Scholar 

  26. Liu H, Ou R, Wei Q, Hou Y, Cao B, Zhao B, Shang H (2019) Rapid eye movement behavior disorder in drug-naïve patients with Parkinson’s disease. J Clin Neurosci 59:254–258. https://doi.org/10.1016/j.jocn.2018.07.007

    Article  PubMed  Google Scholar 

  27. Mariotti P, Quaranta D, Di Giacopo R, Bentivoglio AR, Mazza M, Martini A et al (2015) Rapid eye movement sleep behavior disorder: a window on the emotional world of Parkinson disease. Sleep 38:287–294. https://doi.org/10.5665/sleep.4416

    Article  PubMed  PubMed Central  Google Scholar 

  28. Nardone R, Bergmann J, Brigo F, Christova M, Kunz A, Seidl M, Tezzon F, Trinka E, Golaszewski S (2013) Functional evaluation of central cholinergic circuits in patients with Parkinson’s disease and REM sleep behavior disorder: a TMS study. J Neural Transm 120:413–422. https://doi.org/10.1007/s00702-012-0888-6

    Article  CAS  PubMed  Google Scholar 

  29. Nihei Y, Takahashi K, Koto A, 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. https://doi.org/10.1007/s00415-011-6386-1

    Article  PubMed  Google Scholar 

  30. 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. https://doi.org/10.1016/j.sleep.2012.10.011

    Article  PubMed  Google Scholar 

  31. Özekmekçi S, Apaydin H, Kiliç E (2005) Clinical features of 35 patients with Parkinson’s disease displaying REM behavior disorder. Clin Neurol Neurosurg 107:306–309. https://doi.org/10.1016/j.clineuro.2004.09.021

    Article  PubMed  Google Scholar 

  32. Postuma RB, Bertrand JA, Montplaisir J, Desjardins C, Vendette M, Rios Romenets S, Panisset M, Gagnon JF (2012) Rapid eye movement sleep behavior disorder and risk of dementia in Parkinson’s disease: a prospective study. Mov Disord 27:720–726. https://doi.org/10.1002/mds.24939

    Article  PubMed  Google Scholar 

  33. Rolinski M, Szewczyk-Krolikowski K, Tomlinson PR, Nithi K, Talbot K, Ben-Shlomo Y, Hu MT (2014) REM sleep behaviour disorder is associated with worse quality of life and other non-motor features in early Parkinson’s disease. J Neurol Neurosurg Psychiatry 85:560–566. https://doi.org/10.1136/jnnp-2013-306104

    Article  PubMed  Google Scholar 

  34. 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. https://doi.org/10.1002/mds.25086

    Article  PubMed  Google Scholar 

  35. Sixel-Döring F, Trautmann E, Mollenhauer B, Trenkwalder C (2011) Associated factors for REM sleep behavior disorder in Parkinson disease. Neurology 77:1048–1054. https://doi.org/10.1212/WNL.0b013e31822e560e

    Article  CAS  PubMed  Google Scholar 

  36. Vibha D, Shukla G, Goyal V, Singh S, Srivastava AK, Behari M (2011) RBD in Parkinson’s disease: a clinical case control study from North India. Clin Neurol Neurosurg 113:472–476. https://doi.org/10.1016/j.clineuro.2011.02.007

    Article  PubMed  Google Scholar 

  37. Yoritaka A, Ohizumi H, Tanaka S, Hattori N (2009) Parkinson’s disease with and without REM sleep behaviour disorder: are there any clinical differences? Eur Neurol 61:164–170. https://doi.org/10.1159/000189269

    Article  PubMed  Google Scholar 

  38. Aygün D, Türkel Y, Akkurt A, Onar MK (2012) The effect of REM sleep behaviour disorder on clinical severity in Parkinson’s disease. Turkish J Med Sci 42:1033–1038. https://doi.org/10.3906/sag-1105-35

    Article  Google Scholar 

  39. Bjørnarå KA, Dietrichs E, Toft M (2014) Clinical features associated with sleep disturbances in Parkinson’s disease. Clin Neurol Neurosurg 124:37–43. https://doi.org/10.1016/j.clineuro.2014.06.027

    Article  PubMed  Google Scholar 

  40. Bugalho P, Da Silva JA, Neto B (2011) Clinical features associated with REM sleep behavior disorder symptoms in the early stages of Parkinson’s disease. J Neurol 258:50–55. https://doi.org/10.1007/s00415-010-5679-0

    Article  PubMed  Google Scholar 

  41. Chung SJ, Lee Y, Lee JJ, Lee PH, Sohn YH (2017) Rapid eye movement sleep behaviour disorder and striatal dopamine depletion in patients with Parkinson’s disease. Eur J Neurol 24:1314–1319. https://doi.org/10.1111/ene.13388

    Article  CAS  PubMed  Google Scholar 

  42. Figorilli M, Ferri R, Zibetti M, Beudin P, Puligheddu M, Lopiano L, Cicolin A, Durif F, Marques A, Fantini ML (2017) Comparison between automatic and visual scorings of REM sleep without atonia for the diagnosis of REM sleep behavior disorder in Parkinson disease. Sleep 40:13–16. https://doi.org/10.1093/sleep/zsw060

    Article  Google Scholar 

  43. Gagnon JF, Vendette M, Postuma RB, Desjardins C, Massicotte-Marquez J, Panisset M, Montplaisir J (2009) Mild cognitive impairment in rapid eye movement sleep behavior disorder and Parkinson’s disease. Ann Neurol 66:39–47. https://doi.org/10.1002/ana.21680

    Article  PubMed  Google Scholar 

  44. Gjerstad MD, Boeve B, Aarsland D, Larsen JP (2008) Occurrence and clinical correlates of REM sleep behaviour disorder in patients with Parkinson’s disease over time. J Neurol Neurosurg Psychiatry 79:387–391. https://doi.org/10.1136/jnnp.2007.116830

    Article  CAS  PubMed  Google Scholar 

  45. Gong Y, Ping XK, Jie MC, Shen Y, Dong HW, Ying HJ et al (2014) Clinical manifestations of Parkinson disease and the onset of rapid eye movement sleep behavior disorder. Sleep Med 15:647–653. https://doi.org/10.1016/j.sleep.2013.12.021

    Article  PubMed  Google Scholar 

  46. Hu Y, Yu SY, Zuo LJ, Cao CJ, Wang F, Chen ZJ, du Y, Lian TH, Wang YJ, Chan P, Chen SD, Wang XM, Zhang W (2015) Parkinson disease with REM sleep behavior disorder: features, α-synuclein, and inflammation. Neurology 84:888–894. https://doi.org/10.1212/WNL.0000000000001308

    Article  CAS  PubMed  Google Scholar 

  47. Jozwiak N, Postuma RB, Montplaisir J, Latreille V, Panisset M, Chouinard S et al (2017) Rem sleep behavior disorder and cognitive impairment in Parkinson’s disease. Sleep 40:1–10

    Article  Google Scholar 

  48. Lee JE, Kim KS, Shin HW, Sohn YH (2010) Factors related to clinically probable REM sleep behavior disorder in Parkinson disease. Park Relat Disord 16:105–108. https://doi.org/10.1016/j.parkreldis.2009.08.005

    Article  Google Scholar 

  49. Kim JS, Park HE, Oh YS, Lee SH, Park JW, Son BC, Lee KS (2016) Orthostatic hypotension and cardiac sympathetic denervation in Parkinson disease patients with REM sleep behavioral disorder. J Neurol Sci 362:59–63. https://doi.org/10.1016/j.jns.2016.01.020

    Article  PubMed  Google Scholar 

  50. Kim YE, Jeon BS, Yang HJ, Ehm G, Yun JY, Kim HJ, Kim JM (2014) REM sleep behavior disorder: association with motor complications and impulse control disorders in Parkinson’s disease. Park Relat Disord 20:1081–1084. https://doi.org/10.1016/j.parkreldis.2014.03.022

    Article  Google Scholar 

  51. Kotagal V, Albin RL, Müller MLTM, Koeppe RA, Chervin RD, Frey KA, Bohnen NI (2012) Symptoms of rapid eye movement sleep behavior disorder are associated with cholinergic denervation in Parkinson disease. Ann Neurol 71:560–568. https://doi.org/10.1002/ana.22691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Li D, Huang P, Zang Y, Lou Y, Cen Z, Gu Q, Xuan M, Xie F, Ouyang Z, Wang B, Zhang M, Luo W (2017) Abnormal baseline brain activity in Parkinson’s disease with and without REM sleep behavior disorder: a resting-state functional MRI study. J Magn Reson Imaging 46:697–703. https://doi.org/10.1002/jmri.25571

    Article  PubMed  Google Scholar 

  53. Lim JS, Shin SA, Lee JY, Nam H, Lee JY, Kim YK (2016) Neural substrates of rapid eye movement sleep behavior disorder in Parkinson’s disease. Park Relat Disord 23:31–36. https://doi.org/10.1016/j.parkreldis.2015.11.027

    Article  Google Scholar 

  54. Liu Y, Zhu XY, Zhang XJ, Kuo SH, Ondo WG, Wu YC (2017) Clinical features of Parkinson’s disease with and without rapid eye movement sleep behavior disorder. Transl Neurodegener 6:1–6. https://doi.org/10.1186/s40035-017-0105-5

    Article  Google Scholar 

  55. Neikrug AB, Avanzino JA, Liu L, Maglione JE, Natarajan L, Corey-Bloom J, Palmer BW, Loredo JS, Ancoli-Israel S (2014) Parkinson’s disease and REM sleep behavior disorder result in increased non-motor symptoms. Sleep Med 15:959–966. https://doi.org/10.1016/j.sleep.2014.04.009

    Article  PubMed  PubMed Central  Google Scholar 

  56. Nomura T, Kishi M, Nakashima K (2017) Differences in clinical characteristics when REM sleep behavior disorder precedes or comes after the onset of Parkinson’s disease. J Neurol Sci 382:58–60. https://doi.org/10.1016/j.jns.2017.08.3247

    Article  PubMed  Google Scholar 

  57. Sorensen GL, Mehlsen J, Jennum P (2013) Reduced sympathetic activity in idiopathic rapid-eye-movement sleep behavior disorder and Parkinson’s disease. Auton Neurosci Basic Clin 179:138–141. https://doi.org/10.1016/j.autneu.2013.08.067

    Article  Google Scholar 

  58. Suzuki K, Miyamoto T, Miyamoto M, Watanabe Y, Suzuki S, Tatsumoto M, Iwanami M, Sada T, Kadowaki T, Numao A, Hashimoto K, Sakuta H, Hirata K (2013) Probable rapid eye movement sleep behavior disorder, nocturnal disturbances and quality of life in patients with Parkinson’s disease: a case-controlled study using the rapid eye movement sleep behavior disorder screening questionnaire. BMC Neurol 13:1–9. https://doi.org/10.1186/1471-2377-13-18

    Article  Google Scholar 

  59. Jiao YZ, Wei J, Jie MC, Ru ZJ, Chen J, Yan JX et al (2016) Retinal nerve fiber layer thinning: a window into rapid eye movement sleep behavior disorders in Parkinson’s disease. Sleep Breath 20:1285–1292. https://doi.org/10.1007/s11325-016-1366-4

    Article  Google Scholar 

  60. Sinforiani E, Zangaglia R, Manni R, Cristina S, Marchioni E, Nappi G, Mancini F, Pacchetti C (2006) REM sleep behavior disorder, hallucinations, and cognitive impairment in Parkinson’s disease. Mov Disord 21:462–466. https://doi.org/10.1002/mds.20719

    Article  PubMed  Google Scholar 

  61. Remy P, Doder M, Lees A, Turjanski N, Brooks D (2005) Depression in Parkinson’s disease: loss of dopamine and noradrenaline innervation in the limbic system. Brain 128:1314–1322. https://doi.org/10.1093/brain/awh445

    Article  PubMed  Google Scholar 

  62. Vriend C, Raijmakers P, Veltman DJ, Van Dijk KD, Van Der Werf YD, Foncke EMJ et al (2014) Depressive symptoms in Parkinson’s disease are related to reduced [ 123 I ] FP-CIT binding in the caudate nucleus. J Neurol Neurosurg Psychiatry 85:159–164. https://doi.org/10.1136/jnnp-2012-304811

    Article  PubMed  Google Scholar 

  63. Kostic VS, Petrovic I, Jec M (2010) Regional patterns of brain tissue loss associated with depression in Parkinson disease. Neurology 75:857–863. https://doi.org/10.1212/WNL.0b013e3181f11c1d

    Article  CAS  PubMed  Google Scholar 

  64. Boucetta S, Salimi A, Dadar M, Jones BE, Collins DL, Dang-Vu TT (2016) Structural brain alterations associated with rapid eye movement sleep behavior disorder in Parkinson’s disease. Sci Rep 6:26782

    Article  CAS  Google Scholar 

  65. Postuma RB, Adler CH, Dugger BN, Hentz JG, Shill HA, Driver-Dunckley E, Sabbagh MN, Jacobson SA, Belden CM, Sue LI, Serrano G, Beach TG (2015) REM sleep behavior disorder and neuropathology in Parkinson’s disease. Mov Disord 30:1413–1417

    Article  CAS  Google Scholar 

  66. Nomura T, Inoue Y, Kagimura T, Uemura Y, Nakashima K (2011) Utility of the REM sleep behavior disorder screening questionnaire (RBDSQ) in Parkinson’s disease patients. Sleep Med 12:711–713. https://doi.org/10.1016/j.sleep.2011.01.015

    Article  PubMed  Google Scholar 

  67. Stiasny-kolster K, Sixel-döring F, Trenkwalder C, Heinzel-gutenbrunner M, Seppi K, Poewe W et al (2015) Diagnostic value of the REM sleep behavior disorder screening questionnaire in Parkinson’s disease. Sleep Med 16:186–189. https://doi.org/10.1016/j.sleep.2014.08.014

    Article  PubMed  Google Scholar 

  68. Stiasny-kolster K, Mayer G, Scha S, Mo JC, Heinzel-gutenbrunner M, Oertel WH (2007) The REM sleep behavior disorder screening questionnaire — a new diagnostic instrument. Mov Disord 22:2386–2393. https://doi.org/10.1002/mds.21740

    Article  PubMed  Google Scholar 

  69. Schapira AHV, Chaudhuri KR, Jenner P (2017) Non-motor features of Parkinson disease. Nat Publ Gr 18:435–450. https://doi.org/10.1038/nrn.2017.62

    Article  CAS  Google Scholar 

  70. Zhang LY, Liu WY, Kang Y, Yang Q, Wang XY, Ding JQ, Chen SD, Liu J (2016) Association of rapid eye movement sleep behavior disorder with sleep-disordered breathing in Parkinson’s disease. Sleep Med 20:110–115. https://doi.org/10.1016/j.sleep.2015.12.018

    Article  PubMed  Google Scholar 

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Funding

This work was funded by the Basic Conditions Platform Construction Project of Sichuan Science and Technology Department (2019JDPT0015) and Sichuan Province Applied Basic Research Program (17ZD011).

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DX wrote the main manuscript. YMX provided the study idea. DX and QYS conducted article literature search and data extraction. DX and JYZ contributed to analyze and interpret the data. YMX and JYZ made critical comments and revision for the manuscript. All authors reviewed and approved the final manuscript.

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Correspondence to Junying Zhou or Yanming Xu.

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Xie, D., Shen, Q., Zhou, J. et al. Non-motor symptoms are associated with REM sleep behavior disorder in Parkinson’s disease: a systematic review and meta-analysis. Neurol Sci 42, 47–60 (2021). https://doi.org/10.1007/s10072-020-04769-9

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