Abstract
Finding out about night-time symptoms from Parkinson’s disease (PD) patients can be a challenge as many patients and their carers cannot recall many symptoms that occur during the night, resulting in an under-recognition or a large variability of responses from clinical interviews and scales. Moreover, technology-based assessments for most night-time symptoms are still not universally available for use in a patient’s home environment. Therefore, most physicians rely on their clinical acumen to capture these night-time symptoms based on pieces of patients’ history, bedpartner’s reports, clinical features, associated symptoms or conditions. To capture more night-time symptoms, the authors identified common nocturnal symptoms based on how they manifest from dusk to dawn with selected features relevant to PD. While some symptoms occur in healthy individuals, in PD patients, they may impact differently. The authors intend this narrative review to provide a practical guide on how these common night-time symptoms manifest and highlight pertinent issues by focusing on prevalence, clinical symptomatology, and specific relationships to PD. It is also important to recognise that PD-specific sleep disturbances increase with advancing disease with additional contributions from ageing, comorbidities, and medication side effects. However, the relative contribution of each factor to individual symptom may be different in individual patient, necessitating clinical expertise for individual interpretation. While there are debatable issues in certain areas, they underlie the complexity of night-time symptoms. Understanding night-time symptoms in PD is like re-arranging jigsaw pieces of clinical information to create, but never complete, a picture for physicians to instigate appropriate management.
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References
Allen RP, Picchietti DL, Garcia-Borreguero D, Ondo WG, Walters AS, Winkelman JW, Zucconi M, Ferri R, Trenkwalder C, Lee HB, International Restless Legs Syndrome Study G (2014) Restless legs syndrome/Willis-Ekbom disease diagnostic criteria: updated International Restless Legs Syndrome Study Group (IRLSSG) consensus criteria—history, rationale, description, and significance. Sleep Med 15(8):860–873. https://doi.org/10.1016/j.sleep.2014.03.025
Alonso-Navarro H, Garcia-Martin E, Agundez JAG, Jimenez-Jimenez FJ (2019) Association between restless legs syndrome and other movement disorders. Neurology 92(20):948–964. https://doi.org/10.1212/WNL.0000000000007500
American Academy of Sleep Medicine (2014) International classification of sleep disorders. 3rd edn. American Academy of Sleep Medicine, Darien, IL
Apetauerova D, Ryan RK, Ro SI, Arle J, Shils J, Papavassiliou E, Tarsy D (2006) End of day dyskinesia in advanced Parkinson's disease can be eliminated by bilateral subthalamic nucleus or globus pallidus deep brain stimulation. Mov Disord 21(8):1277–1279. https://doi.org/10.1002/mds.20896
Arnulf I, Konofal E, Merino-Andreu M, Houeto JL, Mesnage V, Welter ML, Lacomblez L, Golmard JL, Derenne JP, Agid Y (2002) Parkinson's disease and sleepiness: an integral part of PD. Neurology 58(7):1019–1024
Arnulf I, Neutel D, Herlin B, Golmard JL, Leu-Semenescu S, de Cock VC, Vidailhet M (2015) Sleepiness in idiopathic REM sleep behavior disorder and Parkinson disease. Sleep 38(10):1529–1535. https://doi.org/10.5665/sleep.5040
Asplund R (2006) Hip fractures, nocturia, and nocturnal polyuria in the elderly. Arch Gerontol Geriatr 43(3):319–326. https://doi.org/10.1016/j.archger.2005.12.002
Balash Y, Peretz C, Leibovich G, Herman T, Hausdorff JM, Giladi N (2005) Falls in outpatients with Parkinson's disease: frequency, impact and identifying factors. J Neurol 252(11):1310–1315. https://doi.org/10.1007/s00415-005-0855-3
Barnes J, David AS (2001) Visual hallucinations in Parkinson's disease: a review and phenomenological survey. J Neurol Neurosurg Psychiatry 70(6):727–733. https://doi.org/10.1136/jnnp.70.6.727
Barone P, Antonini A, Colosimo C, Marconi R, Morgante L, Avarello TP, Bottacchi E, Cannas A, Ceravolo G, Ceravolo R, Cicarelli G, Gaglio RM, Giglia RM, Iemolo F, Manfredi M, Meco G, Nicoletti A, Pederzoli M, Petrone A, Pisani A, Pontieri FE, Quatrale R, Ramat S, Scala R, Volpe G, Zappulla S, Bentivoglio AR, Stocchi F, Trianni G, Dotto PD (2009) The PRIAMO study: a multicenter assessment of nonmotor symptoms and their impact on quality of life in Parkinson's disease. Mov Disord 24(11):1641–1649. https://doi.org/10.1002/mds.22643
Batla A, Phe V, De Min L, Panicker JN (2016) Nocturia in Parkinson's disease: why does it occur and how to manage? Mov Disord Clin Pract 3(5):443–451. https://doi.org/10.1002/mdc3.12374
Berg D, Postuma RB, Adler CH, Bloem BR, Chan P, Dubois B, Gasser T, Goetz CG, Halliday G, Joseph L, Lang AE, Liepelt-Scarfone I, Litvan I, Marek K, Obeso J, Oertel W, Olanow CW, Poewe W, Stern M, Deuschl G (2015) MDS research criteria for prodromal Parkinson's disease. Mov Disord 30(12):1600–1611. https://doi.org/10.1002/mds.26431
Bhidayasiri R, Trenkwalder C (2018) Getting a good night sleep? The importance of recognizing and treating nocturnal hypokinesia in Parkinson's disease. Parkinsonism Relat Disord 50:10–18. https://doi.org/10.1016/j.parkreldis.2018.01.008
Bhidayasiri R, Mekawichai P, Jitkritsadakul O, Panyakaew P, Kaewwilai L, Boonrod N, Petchrutchatachart S, Jagota P, Boonpeng K, Singmaneesakulchai S, Setthawatcharawanich S (2014) Nocturnal journey of body and mind in Parkinson's disease: the manifestations, risk factors and their relationship to daytime symptoms. Evidence from the NIGHT-PD study. J Neural Transm 121(Suppl 1):59–68. https://doi.org/10.1007/s00702-014-1199-x
Bhidayasiri R, Sringean J, Thanawattano C (2016) Sensor-based evaluation and treatment of nocturnal hypokinesia in Parkinson's disease: Aan evidence-based review. Parkinsonism Relat Disord 22(Suppl 1):S127–133. https://doi.org/10.1016/j.parkreldis.2015.09.049
Bhidayasiri R, Sringean J, Rattanachaisit W, Truong DD (2017) The sleeping brain in Parkinson's disease: a focus on REM sleep behaviour disorder and related parasomnias for practicing neurologists. J Neurol Sci 374:32–37. https://doi.org/10.1016/j.jns.2017.01.018
Boeve BF, Silber MH, Ferman TJ, Lin SC, Benarroch EE, Schmeichel AM, Ahlskog JE, Caselli RJ, Jacobson S, Sabbagh M, Adler C, Woodruff B, Beach TG, Iranzo A, Gelpi E, Santamaria J, Tolosa E, Singer C, Mash DC, Luca C, Arnulf I, Duyckaerts C, Schenck CH, Mahowald MW, Dauvilliers Y, Graff-Radford NR, Wszolek ZK, Parisi JE, Dugger B, Murray ME, Dickson DW (2013) Clinicopathologic correlations in 172 cases of rapid eye movement sleep behavior disorder with or without a coexisting neurologic disorder. Sleep Med 14(8):754–762. https://doi.org/10.1016/j.sleep.2012.10.015
Bonuccelli U, Del Dotto P, Lucetti C, Petrozzi L, Bernardini S, Gambaccini G, Rossi G, Piccini P (2000) Diurnal motor variations to repeated doses of levodopa in Parkinson's disease. Clin Neuropharmacol 23(1):28–33. https://doi.org/10.1097/00002826-200001000-00006
Bruguerolle B, Simon N (2002) Biologic rhythms and Parkinson's disease: a chronopharmacologic approach to considering fluctuations in function. Clin Neuropharmacol 25(4):194–201. https://doi.org/10.1097/00002826-200207000-00002
Calzetti S, Angelini M, Negrotti A, Marchesi E, Goldoni M (2014) A long-term prospective follow-up study of incident RLS in the course of chronic DAergic therapy in newly diagnosed untreated patients with Parkinson's disease. J Neural Transm (Vienna) 121(5):499–506. https://doi.org/10.1007/s00702-013-1132-8
Chahine LM, Amara AW, Videnovic A (2017) A systematic review of the literature on disorders of sleep and wakefulness in Parkinson's disease from 2005 to 2015. Sleep Med Rev 35:33–50. https://doi.org/10.1016/j.smrv.2016.08.001
Chaudhuri KR, Prieto-Jurcynska C, Naidu Y, Mitra T, Frades-Payo B, Tluk S, Ruessmann A, Odin P, Macphee G, Stocchi F, Ondo W, Sethi K, Schapira AH, Martinez Castrillo JC, Martinez-Martin P (2010) The nondeclaration of nonmotor symptoms of Parkinson's disease to health care professionals: an international study using the nonmotor symptoms questionnaire. Mov Disord 25(6):704–709. https://doi.org/10.1002/mds.22868
Cipolli C, Franceschini C, Mattarozzi K, Mazzetti M, Plazzi G (2011) Overnight distribution and motor characteristics of REM sleep behaviour disorder episodes in patients with narcolepsy-cataplexy. Sleep Med 12(7):635–640. https://doi.org/10.1016/j.sleep.2010.12.016
De Cock VC, Abouda M, Leu S, Oudiette D, Roze E, Vidailhet M, Similowski T, Arnulf I (2010) Is obstructive sleep apnea a problem in Parkinson's disease? Sleep Med 11(3):247–252. https://doi.org/10.1016/j.sleep.2009.05.008
De Cock VC, Bayard S, Yu H, Grini M, Carlander B, Postuma R, Charif M, Dauvilliers Y (2012) Suggested immobilization test for diagnosis of restless legs syndrome in Parkinson's disease. Mov Disord 27(6):743–749. https://doi.org/10.1002/mds.24969
De Cock VC, Bayard S, Jaussent I, Charif M, Grini M, Langenier MC, Yu H, Lopez R, Geny C, Carlander B, Dauvilliers Y (2014) Daytime sleepiness in Parkinson's disease: a reappraisal. PLoS ONE 9(9):e107278. https://doi.org/10.1371/journal.pone.0107278
De Cock VC, Benard-Serre N, Driss V, Granier M, Charif M, Carlander B, Desplan M, Croisier Langenier M, Cugy D, Bayard S (2015) Supine sleep and obstructive sleep apnea syndrome in Parkinson's disease. Sleep Med 16(12):1497–1501. https://doi.org/10.1016/j.sleep.2014.09.014
Coleman RM, Pollak CP, Weitzman ED (1980) Periodic movements in sleep (nocturnal myoclonus): relation to sleep disorders. Ann Neurol 8(4):416–421. https://doi.org/10.1002/ana.410080413
Covassin N, Neikrug AB, Liu L, Corey-Bloom J, Loredo JS, Palmer BW, Maglione J, Ancoli-Israel S (2012) Clinical correlates of periodic limb movements in sleep in Parkinson's disease. J Neurol Sci 316(1–2):131–136. https://doi.org/10.1016/j.jns.2012.01.004
Cubo E, Gracies JM, Benabou R, Olanow CW, Raman R, Leurgans S, Goetz CG (2001) Early morning off-medication dyskinesias, dystonia, and choreic subtypes. Arch Neurol 58(9):1379–1382
Currie LJ, Bennett JP Jr, Harrison MB, Trugman JM, Wooten GF (1997) Clinical correlates of sleep benefit in Parkinson's disease. Neurology 48(4):1115–1117. https://doi.org/10.1212/wnl.48.4.1115
Duarte Folle A, Paul KC, Bronstein JM, Keener AM, Ritz B (2019) Clinical progression in Parkinson's disease with features of REM sleep behavior disorder: a population-based longitudinal study. Parkinsonism Relat Disord 62:105–111. https://doi.org/10.1016/j.parkreldis.2019.01.018
Factor SA, Weiner WJ (1998) 'Sleep benefit’ in Parkinson's disease. Neurology 50(5):1514–1515. https://doi.org/10.1212/wnl.50.5.1514-b
Fenelon G, Mahieux F, Huon R, Ziegler M (2000) Hallucinations in Parkinson's disease: prevalence, phenomenology and risk factors. Brain 123(Pt 4):733–745
Fereshtehnejad SM, Zeighami Y, Dagher A, Postuma RB (2017) Clinical criteria for subtyping Parkinson's disease: biomarkers and longitudinal progression. Brain 140(7):1959–1976. https://doi.org/10.1093/brain/awx118
Ferreira JJ, Desboeuf K, Galitzky M, Thalamas C, Brefel-Courbon C, Fabre N, Senard JM, Montastruc JL, Sampaio C, Rascol O (2006) Sleep disruption, daytime somnolence and 'sleep attacks' in Parkinson's disease: a clinical survey in PD patients and age-matched healthy volunteers. Eur J Neurol 13(3):209–214. https://doi.org/10.1111/j.1468-1331.2006.01262.x
Frankel JP, Pirtosek Z, Kempster PA, Bovingdon M, Webster R, Lees AJ, Stern GM (1990) Diurnal differences in response to oral levodopa. J Neurol Neurosurg Psychiatry 53(11):948–950. https://doi.org/10.1136/jnnp.53.11.948
Frauscher B, Iranzo A, Gaig C, Gschliesser V, Guaita M, Raffelseder V, Ehrmann L, Sola N, Salamero M, Tolosa E, Poewe W, Santamaria J, Hogl B, Group S (2012) Normative EMG values during REM sleep for the diagnosis of REM sleep behavior disorder. Sleep 35(6):835–847. https://doi.org/10.5665/sleep.1886
Frucht S, Rogers JD, Greene PE, Gordon MF, Fahn S (1999) Falling asleep at the wheel: motor vehicle mishaps in persons taking pramipexole and ropinirole. Neurology 52(9):1908–1910
Gancher ST, Nutt JG (1987) Diurnal responsiveness to apomorphine. Neurology 37(7):1250–1253. https://doi.org/10.1212/wnl.37.7.1250
Gjerstad MD, Alves G, Wentzel-Larsen T, Aarsland D, Larsen JP (2006) Excessive daytime sleepiness in Parkinson disease: is it the drugs or the disease? Neurology 67(5):853–858. https://doi.org/10.1212/01.wnl.0000233980.25978.9d
Gjerstad MD, Wentzel-Larsen T, Aarsland D, Larsen JP (2007) Insomnia in Parkinson's disease: frequency and progression over time. J Neurol Neurosurg Psychiatry 78(5):476–479. https://doi.org/10.1136/jnnp.2006.100370
Gjerstad MD, Boeve B, Wentzel-Larsen T, 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(4):387–391. https://doi.org/10.1136/jnnp.2007.116830
Gjerstad MD, Tysnes OB, Larsen JP (2011) Increased risk of leg motor restlessness but not RLS in early Parkinson disease. Neurology 77(22):1941–1946. https://doi.org/10.1212/WNL.0b013e31823a0cc8
Goetz CG, Fan W, Leurgans S, Bernard B, Stebbins GT (2006) The malignant course of “benign hallucinations” in Parkinson disease. Arch Neurol 63(5):713–716. https://doi.org/10.1001/archneur.63.5.713
Gomez-Esteban JC, Zarranz JJ, Lezcano E, Velasco F, Ciordia R, Rouco I, Losada J, Bilbao I (2006) Sleep complaints and their relation with drug treatment in patients suffering from Parkinson's disease. Mov Disord 21(7):983–988. https://doi.org/10.1002/mds.20874
Happe S, Berger K, Investigators FS (2002) The association between caregiver burden and sleep disturbances in partners of patients with Parkinson's disease. Age Ageing 31(5):349–354
Hatano T, Kubo SI, Shimo Y, Nishioka K, Hattori N (2009) Unmet needs of patients with Parkinson's disease: interview survey of patients and caregivers. J Int Med Res 37(3):717–726. https://doi.org/10.1177/147323000903700315
Hely MA, Morris JG, Reid WG, Trafficante R (2005) Sydney multicenter study of Parkinson's disease: non-l-dopa-responsive problems dominate at 15 years. Mov Disord 20(2):190–199. https://doi.org/10.1002/mds.20324
Hermann W, Flemming T, Brandt MD, Langner S, Reichmann H, Storch A (2019) Asymmetry of periodic leg movements in sleep (PLMS) in Parkinson's disease. J Parkinsons Dis. https://doi.org/10.3233/JPD-191667
Hermanowicz N, Jones SA, Hauser RA (2019) Impact of non-motor symptoms in Parkinson's disease: a PMDAlliance survey. Neuropsychiatr Dis Treat 15:2205–2212. https://doi.org/10.2147/NDT.S213917
Hogl B (2010) Sleep apnea in Parkinson's disease: when is it significant? Sleep Med 11(3):233–235. https://doi.org/10.1016/j.sleep.2009.11.008
Hogl B, Stefani A (2017) Restless legs syndrome and periodic leg movements in patients with movement disorders: specific considerations. Mov Disord 32(5):669–681. https://doi.org/10.1002/mds.26929
Hoglund A, Broman JE, Palhagen S, Fredrikson S, Hagell P (2015) Is excessive daytime sleepiness a separate manifestation in Parkinson's disease? Acta Neurol Scand. https://doi.org/10.1111/ane.12378
Hoque R, Chesson AL Jr (2010) Pharmacologically induced/exacerbated restless legs syndrome, periodic limb movements of sleep, and REM behavior disorder/REM sleep without atonia: literature review, qualitative scoring, and comparative analysis. J Clin Sleep Med 6(1):79–83
Horvath J, Landis T, Burkhard PR (2008) Restless arms. Lancet 371(9611):530. https://doi.org/10.1016/S0140-6736(08)60240-8
Iranzo A, Valldeoriola F, Lomena F, Molinuevo JL, Serradell M, Salamero M, Cot A, Ros D, Pavia J, Santamaria J, Tolosa E (2011) Serial dopamine transporter imaging of nigrostriatal function in patients with idiopathic rapid-eye-movement sleep behaviour disorder: a prospective study. Lancet Neurol 10(9):797–805. https://doi.org/10.1016/S1474-4422(11)70152-1
Iwaki H, Hughes KC, Gao X, Schwarzschild MA, Ascherio A (2018) The association between restless legs syndrome and premotor symptoms of Parkinson's disease. J Neurol Sci 394:41–44. https://doi.org/10.1016/j.jns.2018.08.028
Karlsen K, Larsen JP, Tandberg E, Jorgensen K (1999) Fatigue in patients with Parkinson's disease. Mov Disord 14(2):237–241. https://doi.org/10.1002/1531-8257(199903)14:2%3c237:aid-mds1006%3e3.0.co;2-x
Van Kerrebroeck P, Abrams P, Chaikin D, Donovan J, Fonda D, Jackson S, Jennum P, Johnson T, Lose GR, Mattiasson A, Robertson GL, Weiss J, International Continence S (2002) The standardization of terminology in nocturia: report from the standardization subcommittee of the International Continence Society. BJU Int 90(Suppl 3):11–15. https://doi.org/10.1046/j.1464-410x.90.s3.3.x
Kuhlman GD, Flanigan JL, Sperling SA, Barrett MJ (2019) Predictors of health-related quality of life in Parkinson's disease. Parkinsonism Relat Disord 65:86–90. https://doi.org/10.1016/j.parkreldis.2019.05.009
Lavault S, Bloch F, Houeto JL, Konofal E, Welter ML, Agid Y, Arnulf I (2009) Periodic leg movements and REM sleep without atonia in Parkinson's disease with camptocormia. Mov Disord 24(16):2419–2423. https://doi.org/10.1002/mds.22854
Lee W, Evans A, Williams DR (2017) Subjective perception of sleep benefit in Parkinson's disease: valid or irrelevant? Parkinsonism Relat Disord 42:90–94. https://doi.org/10.1016/j.parkreldis.2017.06.026
Lenka A, Pagonabarraga J, Pal PK, Bejr-Kasem H, Kulisvesky J (2019) Minor hallucinations in Parkinson disease: a subtle symptom with major clinical implications. Neurology 93(6):259–266. https://doi.org/10.1212/WNL.0000000000007913
Lim SY, Lang AE (2010) The nonmotor symptoms of Parkinson's disease—an overview. Mov Disord 25(Suppl 1):S123–130. https://doi.org/10.1002/mds.22786
Lin YQ, Chen SD (2018) RBD: a red flag for cognitive impairment in Parkinson's disease? Sleep Med 44:38–44. https://doi.org/10.1016/j.sleep.2018.01.006
Louter M, Munneke M, Bloem BR, Overeem S (2012) Nocturnal hypokinesia and sleep quality in Parkinson's disease. J Am Geriatr Soc 60(6):1104–1108. https://doi.org/10.1111/j.1532-5415.2012.03966.x
Louter M, van Sloun RJ, Pevernagie DA, Arends JB, Cluitmans PJ, Bloem BR, Overeem S (2013) Subjectively impaired bed mobility in Parkinson disease affects sleep efficiency. Sleep Med 14(7):668–674. https://doi.org/10.1016/j.sleep.2013.03.010
Manni R, Terzaghi M, Repetto A, Zangaglia R, Pacchetti C (2010) Complex paroxysmal nocturnal behaviors in Parkinson's disease. Mov Disord 25(8):985–990. https://doi.org/10.1002/mds.22990
Marchesi E, Negrotti A, Angelini M, Goldoni M, Abrignani G, Calzetti S (2016) A prospective study of the cumulative incidence and course of restless legs syndrome in de novo patients with Parkinson's disease during chronic dopaminergic therapy. J Neurol 263(3):441–447. https://doi.org/10.1007/s00415-015-7937-7
Marsden CD, Parkes JD, Quinn N (1981) Fluctuations of disability in Parkinson's disease-clinical aspects. In: Marsden CD, Fahn S (eds) Movement disorders, neurolosgy, 2nd edn. Butterworth-Heinemann, London, pp 96–122
Martinez-Martin P, Schapira AH, Stocchi F, Sethi K, Odin P, MacPhee G, Brown RG, Naidu Y, Clayton L, Abe K, Tsuboi Y, MacMahon D, Barone P, Rabey M, Bonuccelli U, Forbes A, Breen K, Tluk S, Olanow CW, Thomas S, Rye D, Hand A, Williams AJ, Ondo W, Chaudhuri KR (2007) Prevalence of nonmotor symptoms in Parkinson's disease in an international setting; study using nonmotor symptoms questionnaire in 545 patients. Mov Disord 22(11):1623–1629. https://doi.org/10.1002/mds.21586
Martinez-Martin P, Rodriguez-Blazquez C, Kurtis MM, Chaudhuri KR, Group NV (2011) The impact of non-motor symptoms on health-related quality of life of patients with Parkinson's disease. Mov Disord 26(3):399–406. https://doi.org/10.1002/mds.23462
Matsubara T, Suzuki K, Fujita H, Watanabe Y, Sakuramoto H, Matsubara M, Hirata K (2018) Restless legs syndrome, leg motor restlessness and their variants in patients with Parkinson's disease and related disorders. J Neurol Sci 393:51–57. https://doi.org/10.1016/j.jns.2018.08.007
Merello M, Hughes A, Colosimo C, Hoffman M, Starkstein S, Leiguarda R (1997) Sleep benefit in Parkinson's disease. Mov Disord 12(4):506–508. https://doi.org/10.1002/mds.870120405
Moccia M, Erro R, Picillo M, Santangelo G, Spina E, Allocca R, Longo K, Amboni M, Palladino R, Assante R, Pappata S, Pellecchia MT, Barone P, Vitale C (2016) A four-year longitudinal study on restless legs syndrome in Parkinson disease. Sleep 39(2):405–412. https://doi.org/10.5665/sleep.5452
Mollenhauer B, Trautmann E, Sixel-Doring F, Wicke T, Ebentheuer J, Schaumburg M, Lang E, Focke NK, Kumar KR, Lohmann K, Klein C, Schlossmacher MG, Kohnen R, Friede T, Trenkwalder C, DeNoPa Study G (2013) Nonmotor and diagnostic findings in subjects with de novo Parkinson disease of the DeNoPa cohort. Neurology 81(14):1226–1234. https://doi.org/10.1212/WNL.0b013e3182a6cbd5
Moller JC, Unger M, Stiasny-Kolster K, Oertel WH (2010) Restless legs syndrome (RLS) and Parkinson's disease (PD)—related disorders or different entities? J Neurol Sci 289(1–2):135–137. https://doi.org/10.1016/j.jns.2009.08.035
Monge A, Viselli F, Stocchi F, Barbato L, Bolner A, Modugno N, Paradiso M, Ruggieri S, Nordera G (2004) Variation in the dopaminergic response during the day in Parkinson disease. Clin Neuropharmacol 27(3):116–118. https://doi.org/10.1097/00002826-200405000-00005
Monteiro L, Souza-Machado A, Valderramas S, Melo A (2012) The effect of levodopa on pulmonary function in Parkinson's disease: a systematic review and meta-analysis. Clin Ther 34(5):1049–1055. https://doi.org/10.1016/j.clinthera.2012.03.001
Morgante L, Colosimo C, Antonini A, Marconi R, Meco G, Pederzoli M, Pontieri FE, Cicarelli G, Abbruzzese G, Zappulla S, Ramat S, Manfredi M, Bottacchi E, Abrignani M, Berardelli A, Cozzolino A, Paradiso C, De Gaspari D, Morgante F, Barone P, Group PS (2012) Psychosis associated to Parkinson's disease in the early stages: relevance of cognitive decline and depression. J Neurol Neurosurg Psychiatry 83(1):76–82. https://doi.org/10.1136/jnnp-2011-300043
Muntean ML, Sixel-Doring F, Trenkwalder C (2015) Serum ferritin levels in Parkinson's disease patients with and without restless legs syndrome. Mov Disord Clin Pract 2(3):249–252. https://doi.org/10.1002/mdc3.12165
Muntean ML, Benes H, Sixel-Doring F, Chaudhuri KR, Suzuki K, Hirata K, Zimmermann J, Trenkwalder C (2016) Clinically relevant cut-off values for the Parkinson's Disease Sleep Scale-2 (PDSS-2): a validation study. Sleep Med 24:87–92. https://doi.org/10.1016/j.sleep.2016.06.026
Ondo WG, Vuong KD, Jankovic J (2002) Exploring the relationship between Parkinson disease and restless legs syndrome. Arch Neurol 59(3):421–424. https://doi.org/10.1001/archneur.59.3.421
Onozawa R, Tsugawa J, Tsuboi Y, Fukae J, Mishima T, Fujioka S (2016) The impact of early morning off in Parkinson's disease on patient quality of life and caregiver burden. J Neurol Sci 364:1–5. https://doi.org/10.1016/j.jns.2016.02.066
O'Suilleabhain PE, Dewey RB Jr (2002) Contributions of dopaminergic drugs and disease severity to daytime sleepiness in Parkinson disease. Arch Neurol 59(6):986–989. https://doi.org/10.1001/archneur.59.6.986
Pappert EJ, Goetz CG, Niederman FG, Raman R, Leurgans S (1999) Hallucinations, sleep fragmentation, and altered dream phenomena in Parkinson's disease. Mov Disord 14(1):117–121
Paus S, Brecht HM, Koster J, Seeger G, Klockgether T, Wullner U (2003) Sleep attacks, daytime sleepiness, and dopamine agonists in Parkinson's disease. Mov Disord 18(6):659–667
Perez-Diaz H, Iranzo A, Rye DB, Santamaria J (2011) Restless abdomen: a phenotypic variant of restless legs syndrome. Neurology 77(13):1283–1286. https://doi.org/10.1212/WNL.0b013e318230207a
Porter B, Macfarlane R, Walker R (2008) The frequency and nature of sleep disorders in a community-based population of patients with Parkinson's disease. Eur J Neurol 15(1):50–54. https://doi.org/10.1111/j.1468-1331.2007.01998.x
Puligheddu M, Figorilli M, Arico D, Raggi A, Marrosu F, Ferri R (2014) Time structure of leg movement activity during sleep in untreated Parkinson disease and effects of dopaminergic treatment. Sleep Med 15(7):816–824. https://doi.org/10.1016/j.sleep.2014.03.011
Ravina B, Marder K, Fernandez HH, Friedman JH, McDonald W, Murphy D, Aarsland D, Babcock D, Cummings J, Endicott J, Factor S, Galpern W, Lees A, Marsh L, Stacy M, Gwinn-Hardy K, Voon V, Goetz C (2007) Diagnostic criteria for psychosis in Parkinson's disease: report of an NINDS, NIMH work group. Mov Disord 22(8):1061–1068. https://doi.org/10.1002/mds.21382
Rice JE, Antic R, Thompson PD (2002) Disordered respiration as a levodopa-induced dyskinesia in Parkinson's disease. Mov Disord 17(3):524–527. https://doi.org/10.1002/mds.10072
Rizos A, Martinez-Martin P, Odin P, Antonini A, Kessel B, Kozul TK, Todorova A, Douiri A, Martin A, Stocchi F, Dietrichs E, Chaudhuri KR, Europar, the In-MPDSG (2014) Characterizing motor and non-motor aspects of early-morning off periods in Parkinson's disease: an international multicenter study. Parkinsonism Relat Disord 20(11):1231–1235. https://doi.org/10.1016/j.parkreldis.2014.09.013
Sabate M, Gonzalez I, Ruperez F, Rodriguez M (1996) Obstructive and restrictive pulmonary dysfunctions in Parkinson's disease. J Neurol Sci 138(1–2):114–119. https://doi.org/10.1016/0022-510x(96)00003-2
Sakakibara R, Shinotoh H, Uchiyama T, Sakuma M, Kashiwado M, Yoshiyama M, Hattori T (2001) Questionnaire-based assessment of pelvic organ dysfunction in Parkinson's disease. Auton Neurosci 92(1–2):76–85
Sammour ZM, Gomes CM, Barbosa ER, Lopes RI, Sallem FS, Trigo-Rocha FE, Bruschini H, Srougi M (2009) Voiding dysfunction in patients with Parkinson's disease: impact of neurological impairment and clinical parameters. Neurourol Urodyn 28(6):510–515. https://doi.org/10.1002/nau.20681
Sateia MJ (2014) International classification of sleep disorders-third edition: highlights and modifications. Chest 146(5):1387–1394. https://doi.org/10.1378/chest.14-0970
Schenck CH, Mahowald MW (2002) REM sleep behavior disorder: clinical, developmental, and neuroscience perspectives 16 years after its formal identification in SLEEP. Sleep 25(2):120–138
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(8):744–748. https://doi.org/10.1016/j.sleep.2012.10.009
Simuni T, Caspell-Garcia C, Coffey C, Chahine LM, Lasch S, Oertel WH, Mayer G, Hogl B, Postuma R, Videnovic A, Amara AW, Marek K, Investigators PSWgobotP (2015) Correlates of excessive daytime sleepiness in de novo Parkinson's disease: a case control study. Mov Disord 30(10):1371–1381. https://doi.org/10.1002/mds.26248
Sinforiani E, Pacchetti C, Zangaglia R, Pasotti C, Manni R, Nappi G (2008) REM behavior disorder, hallucinations and cognitive impairment in Parkinson's disease: a two-year follow up. Mov Disord 23(10):1441–1445. https://doi.org/10.1002/mds.22126
Sixel-Doring F, Trautmann E, Mollenhauer B, Trenkwalder C (2011) Associated factors for REM sleep behavior disorder in Parkinson disease. Neurology 77(11):1048–1054. https://doi.org/10.1212/WNL.0b013e31822e560e
Sixel-Doring F, Zimmermann J, Wegener A, Mollenhauer B, Trenkwalder C (2016) The evolution of REM sleep behavior disorder in early Parkinson disease. Sleep 39(9):1737–1742. https://doi.org/10.5665/sleep.6102
Smith M, Seth J, Batla A, Hofereiter J, Bhatia KP, Panicker JN (2016) Nocturia in patients With Parkinson's disease. Mov Disord Clin Pract 3(2):168–172. https://doi.org/10.1002/mdc3.12279
Sobreira-Neto MA, Pena-Pereira MA, Sobreira EST, Chagas MHN, de Almeida CMO, Fernandes RMF, Tumas V, Eckeli AL (2020) Chronic insomnia in patients with parkinson disease: which associated factors are relevant? J Geriatr Psychiatry Neurol 33(1):22–27. https://doi.org/10.1177/0891988719856687
Sommerauer M, Werth E, Poryazova R, Gavrilov YV, Hauser S, Valko PO (2015) Bound to supine sleep: Parkinson's disease and the impact of nocturnal immobility. Parkinsonism Relat Disord 21(10):1269–1272. https://doi.org/10.1016/j.parkreldis.2015.08.010
Sringean J, Taechalertpaisarn P, Thanawattano C, Bhidayasiri R (2016) How well do Parkinson's disease patients turn in bed? Quantitative analysis of nocturnal hypokinesia using multisite wearable inertial sensors. Parkinsonism Relat Disord 23:10–16. https://doi.org/10.1016/j.parkreldis.2015.11.003
Sringean J, Anan C, Thanawattano C, Bhidayasiri R (2017) Time for a strategy in night-time dopaminergic therapy? An objective sensor-based analysis of nocturnal hypokinesia and sleeping positions in Parkinson's disease. J Neurol Sci 373:244–248. https://doi.org/10.1016/j.jns.2016.12.045
Stack EL, Ashburn AM (2006) Impaired bed mobility and disordered sleep in Parkinson's disease. Mov Disord 21(9):1340–1342. https://doi.org/10.1002/mds.20944
Stavitsky K, Saurman JL, McNamara P, Cronin-Golomb A (2010) Sleep in Parkinson's disease: a comparison of actigraphy and subjective measures. Parkinsonism Relat Disord 16(4):280–283. https://doi.org/10.1016/j.parkreldis.2010.02.001
Stefani A, Hogl B (2020) Sleep in Parkinson's disease. Neuropsychopharmacology 45(1):121–128. https://doi.org/10.1038/s41386-019-0448-y
Stefansdottir S, Gjerstad MD, Tysnes OB, Larsen JP (2012) Subjective sleep problems in patients with early Parkinson's disease. Eur J Neurol 19(12):1575–1581. https://doi.org/10.1111/j.1468-1331.2012.03791.x
Stocchi F, Coletti C, Bonassi S, Radicati FG, Vacca L (2019) Early-morning OFF and levodopa dose failures in patients with Parkinson's disease attending a routine clinical appointment using Time-to-ON Questionnaire. Eur J Neurol 26(5):821–826. https://doi.org/10.1111/ene.13895
Suzuki K, Suzuki H, Suzuki Y, Hirata K (2017) "Restless face" as a variant of restless legs syndrome. Parkinsonism Relat Disord 41:130–131. https://doi.org/10.1016/j.parkreldis.2017.05.015
Tandberg E, Larsen JP, Karlsen K (1999) Excessive daytime sleepiness and sleep benefit in Parkinson's disease: a community-based study. Mov Disord 14(6):922–927
Tholfsen LK, Larsen JP, Schulz J, Tysnes OB, Gjerstad MD (2017) Changes in insomnia subtypes in early Parkinson disease. Neurology 88(4):352–358. https://doi.org/10.1212/WNL.0000000000003540
Tikkinen KA, Johnson TM 2nd, Tammela TL, Sintonen H, Haukka J, Huhtala H, Auvinen A (2010) Nocturia frequency, bother, and quality of life: how often is too often? A population-based study in Finland. Eur Urol 57(3):488–496. https://doi.org/10.1016/j.eururo.2009.03.080
Tinuper P, Provini F, Bisulli F, Vignatelli L, Plazzi G, Vetrugno R, Montagna P, Lugaresi E (2007) Movement disorders in sleep: guidelines for differentiating epileptic from non-epileptic motor phenomena arising from sleep. Sleep Med Rev 11(4):255–267. https://doi.org/10.1016/j.smrv.2007.01.001
Trenkwalder C, Kohnen R, Hogl B, Metta V, Sixel-Doring F, Frauscher B, Hulsmann J, Martinez-Martin P, Chaudhuri KR (2011) Parkinson's disease sleep scale—validation of the revised version PDSS-2. Mov Disord 26(4):644–652. https://doi.org/10.1002/mds.23476
Vaughan CP, Juncos JL, Trotti LM, Johnson TM 2nd, Bliwise DL (2013) Nocturia and overnight polysomnography in Parkinson disease. Neurourol Urodyn 32(8):1080–1085. https://doi.org/10.1002/nau.22365
Videnovic A (2018) Disturbances of sleep and alertness in Parkinson's disease. Curr Neurol Neurosci Rep 18(6):29. https://doi.org/10.1007/s11910-018-0838-2
Vincken WG, Darauay CM, Cosio MG (1989) Reversibility of upper airway obstruction after levodopa therapy in Parkinson's disease. Chest 96(1):210–212. https://doi.org/10.1378/chest.96.1.210
Viwattanakulvanid P, Kaewwilai L, Jitkritsadakul O, Brenden NR, Setthawatcharawanich S, Boonrod N, Mekawichai P, Bhidayasiri R (2014) The impact of the nocturnal disabilities of Parkinson's disease on caregivers' burden: implications for interventions. J Neural Transm 121(Suppl 1):15–24. https://doi.org/10.1007/s00702-014-1200-8
Wetter TC, Collado-Seidel V, Pollmacher T, Yassouridis A, Trenkwalder C (2000) Sleep and periodic leg movement patterns in drug-free patients with Parkinson's disease and multiple system atrophy. Sleep 23(3):361–367
Wetter TC, Brunner H, Hogl B, Yassouridis A, Trenkwalder C, Friess E (2001) Increased alpha activity in REM sleep in de novo patients with Parkinson's disease. Mov Disord 16(5):928–933. https://doi.org/10.1002/mds.1163
Winge K, Skau AM, Stimpel H, Nielsen KK, Werdelin L (2006) Prevalence of bladder dysfunction in Parkinsons disease. Neurourol Urodyn 25(2):116–122. https://doi.org/10.1002/nau.20193
Yang X, Liu B, Shen H, Li S, Zhao Q, An R, Hu F, Ren H, Xu Y, Xu Z (2018) Prevalence of restless legs syndrome in Parkinson's disease: a systematic review and meta-analysis of observational studies. Sleep Med 43:40–46. https://doi.org/10.1016/j.sleep.2017.11.1146
Ylikoski A, Martikainen K, Partinen M (2014) Parasomnias and isolated sleep symptoms in Parkinson's disease: a questionnaire study on 661 patients. J Neurol Sci 346(1–2):204–208. https://doi.org/10.1016/j.jns.2014.08.025
Zadra A, Pilon M (2011) NREM parasomnias. Handb Clin Neurol 99:851–868. https://doi.org/10.1016/B978-0-444-52007-4.00011-4
Zhang J, Xu CY, Liu J (2017) Meta-analysis on the prevalence of REM sleep behavior disorder symptoms in Parkinson's disease. BMC Neurol 17(1):23. https://doi.org/10.1186/s12883-017-0795-4
Zhu XY, Liu Y, Zhang XJ, Yang WH, Feng Y, Ondo WG, Tan EK, Wu YC (2015) Clinical characteristics of leg restlessness in Parkinson's disease compared with idiopathic restless legs syndrome. J Neurol Sci 357(1–2):109–114. https://doi.org/10.1016/j.jns.2015.07.008
Zimmerman TR Jr, Sage JI, Lang AE, Mark MH (1994) Severe evening dyskinesias in advanced Parkinson's disease: clinical description, relation to plasma levodopa, and treatment. Mov Disord 9(2):173–177. https://doi.org/10.1002/mds.870090208
Zoccolella S, Savarese M, Lamberti P, Manni R, Pacchetti C, Logroscino G (2011) Sleep disorders and the natural history of Parkinson's disease: the contribution of epidemiological studies. Sleep Med Rev 15(1):41–50. https://doi.org/10.1016/j.smrv.2010.02.004
Zucconi M, Ferri R, Allen R, Baier PC, Bruni O, Chokroverty S, Ferini-Strambi L, Fulda S, Garcia-Borreguero D, Hening WA, Hirshkowitz M, Hogl B, Hornyak M, King M, Montagna P, Parrino L, Plazzi G, Terzano MG, International Restless Legs Syndrome Study G (2006) The official World Association of Sleep Medicine (WASM) standards for recording and scoring periodic leg movements in sleep (PLMS) and wakefulness (PLMW) developed in collaboration with a task force from the International Restless Legs Syndrome Study Group (IRLSSG). Sleep Med 7(2):175–183. https://doi.org/10.1016/j.sleep.2006.01.001
Acknowledgements
Roongroj Bhidayasiri is supported by Thailand Science Research and Innovation Grant (RTA6280016), International Research Network Grant (IRN59W0005) of the Thailand Research Fund, Chulalongkorn Academic Advancement Fund into Its 2nd Century Project of Chulalongkorn University (2300042200), and Center of Excellence Grant of Chulalongkorn University (GCE 6100930004-1).
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Bhidayasiri, R., Sringean, J. & Trenkwalder, C. Mastering nocturnal jigsaws in Parkinson’s disease: a dusk-to-dawn review of night-time symptoms. J Neural Transm 127, 763–777 (2020). https://doi.org/10.1007/s00702-020-02170-6
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DOI: https://doi.org/10.1007/s00702-020-02170-6