Abstract
Introduction
Nonmotor symptoms (NMSs) severely affect the daily quality of life of patients with Parkinson’s disease (PD). Although many studies have documented the clinical characteristics of NMSs in PD patients, some issues remain unaddressed. The severity and gender distribution of NMSs in Asian and the Western patients differ. The correlations between clinical characteristics and NMS manifestations remain unclear. We studied these relationships in a large cohort of Taiwanese PD patients.
Methods
Patients with PD were recruited from the outpatient clinic of a tertiary medical center and evaluated with standardized assessment protocols, including the NonMotor Symptoms Scale (NMSS), Unified Parkinson’s Disease Rating Scale (UPDRS), Hoehn and Yahr (H&Y) scale, Mini-Mental Status Examination, and Montreal Cognitive Assessment.
Results
Among 820 patients enrolled, 41.8% were female. The prevalence of the NMSs was 96.5%, with attention/memory (79.51%) being the most frequently involved domain. The mean severity score on the NMSS was 36.48 ± 34.30. Male patients reported higher NMS prevalence and severity than female patients, mostly in the gastrointestinal tract and urinary domains. We found that the severity of NMSs was correlated with disease duration, UPDRS Part III score, and H&Y stage.
Conclusion
Although they exhibited similar NMS prevalence, Taiwanese PD patients reported less intense NMSs compared with those reported by Western patients. Furthermore, the NMS items our patients emphasized and gender discrepancies were distinct from those in Western studies.
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References
Chaudhuri KR, Martinez-Martin P (2008) Quantitation of non-motor symptoms in Parkinson's disease. Eur J Neurol 15(Suppl 2):2–7. https://doi.org/10.1111/j.1468-1331.2008.02212.x
Martinez-Martin P, Rodriguez-Blazquez C, Abe K, Bhattacharyya KB, Bloem BR, Carod-Artal FJ, Prakash R, Esselink RA, Falup-Pecurariu C, Gallardo M, Mir P, Naidu Y, Nicoletti A, Sethi K, Tsuboi Y, van Hilten JJ, Visser M, Zappia M, Chaudhuri KR (2009) International study on the psychometric attributes of the non-motor symptoms scale in Parkinson disease. Neurology 73(19):1584–1591. https://doi.org/10.1212/WNL.0b013e3181c0d416
Solla P, Cannas A, Ibba FC, Loi F, Corona M, Orofino G, Marrosu MG, Marrosu F (2012) Gender differences in motor and non-motor symptoms among Sardinian patients with Parkinson's disease. J Neurol Sci 323(1–2):33–39. https://doi.org/10.1016/j.jns.2012.07.026
Kim SR, So HY, Choi E, Kang JH, Kim HY, Chung SJ (2014) Influencing effect of non-motor symptom clusters on quality of life in Parkinson's disease. J Neurol Sci 347(1–2):310–315. https://doi.org/10.1016/j.jns.2014.10.032
Krishnan S, Sarma G, Sarma S, Kishore A (2011) Do nonmotor symptoms in Parkinson's disease differ from normal aging? Mov Disord 26(11):2110–2113. https://doi.org/10.1002/mds.23826
Salari M, Chitsaz A, Etemadifar M, Najafi MR, Mirmosayyeb O, Bemanalizadeh M, Panahi F, Mirzajani H (2017) Evaluation of non-motor symptoms and their impact on quality of life in patients with Parkinson's disease, Isfahan Iran. Iran J Neurol 16(3):118–124
Zis P, Rizos A, Martinez-Martin P, Pal S, Silverdale M, Sharma JC, Sauerbier A, Chaudhuri KR (2014) Non-motor symptoms profile and burden in drug naive versus long-term Parkinson's disease patients. J Parkinsons Dis 4(3):541–547. https://doi.org/10.3233/JPD-140372
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
Yong MH, Allen JC Jr, Prakash KM, Tan EK (2013) Differentiating non-motor symptoms in Parkinson's disease from controls and hemifacial spasm. PLoS ONE 8(2):e49596. https://doi.org/10.1371/journal.pone.0049596
Picillo M, Palladino R, Moccia M, Erro R, Amboni M, Vitale C, Barone P, Pellecchia MT (2016) Gender and non motor fluctuations in Parkinson's disease: a prospective study. Parkinsonism Relat Disord 27:89–92. https://doi.org/10.1016/j.parkreldis.2016.04.001
Martinez-Martin P, Falup Pecurariu C, Odin P, van Hilten JJ, Antonini A, Rojo-Abuin JM, Borges V, Trenkwalder C, Aarsland D, Brooks DJ, Ray Chaudhuri K (2012) Gender-related differences in the burden of non-motor symptoms in Parkinson's disease. J Neurol 259(8):1639–1647. https://doi.org/10.1007/s00415-011-6392-3
Song Y, Gu Z, An J, Chan P, Chinese Parkinson Study G (2014) Gender differences on motor and non-motor symptoms of de novo patients with early Parkinson's disease. Neurol Sci 35(12):1991–1996. https://doi.org/10.1007/s10072-014-1879-1
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
Song W, Guo X, Chen K, Chen X, Cao B, Wei Q, Huang R, Zhao B, Wu Y, Shang HF (2014) The impact of non-motor symptoms on the health-related quality of life of Parkinson's disease patients from Southwest China. Parkinsonism Relat Disord 20(2):149–152. https://doi.org/10.1016/j.parkreldis.2013.10.005
Zis P, Martinez-Martin P, Sauerbier A, Rizos A, Sharma JC, Worth PF, Sophia R, Silverdale M, Chaudhuri KR (2015) Non-motor symptoms burden in treated and untreated early Parkinson's disease patients: argument for non-motor subtypes. Eur J Neurol 22(8):1145–1150. https://doi.org/10.1111/ene.12733
Erro R, Picillo M, Vitale C, Amboni M, Moccia M, Santangelo G, Pellecchia MT, Barone P (2016) The non-motor side of the honeymoon period of Parkinson's disease and its relationship with quality of life: a 4-year longitudinal study. Eur J Neurol 23(11):1673–1679. https://doi.org/10.1111/ene.13106
Lachman HM, Papolos DF, Saito T, Yu YM, Szumlanski CL, Weinshilboum RM (1996) Human catechol-O-methyltransferase pharmacogenetics: description of a functional polymorphism and its potential application to neuropsychiatric disorders. Pharmacogenetics 6(3):243–250
Li W, Chen Y, Yin B, Zhang L (2014) Pain in Parkinson's disease associated with COMT gene polymorphisms. Behav Neurol 2014:304203. https://doi.org/10.1155/2014/304203
Lin CH, Chaudhuri KR, Fan JY, Ko CI, Rizos A, Chang CW, Lin HI, Wu YR (2017) Depression and Catechol-O-methyltransferase (COMT) genetic variants are associated with pain in Parkinson's disease. Sci Rep 7(1):6306. https://doi.org/10.1038/s41598-017-06782-z
Lin CH, Fan JY, Lin HI, Chang CW, Wu YR (2018) Catechol-O-methyltransferase (COMT) genetic variants are associated with cognitive decline in patients with Parkinson's disease. Parkinsonism Relat Disord 50:48–53. https://doi.org/10.1016/j.parkreldis.2018.02.015
Ziegler DA, Ashourian P, Wonderlick JS, Sarokhan AK, Prelec D, Scherzer CR, Corkin S (2014) Motor impulsivity in Parkinson disease: associations with COMT and DRD2 polymorphisms. Scand J Psychol 55(3):278–286. https://doi.org/10.1111/sjop.12113
Lin YY, Chen RS, Lu CS, Huang YZ, Weng YH, Yeh TH, Lin WY, Hung J (2017) Sleep disturbances in Taiwanese patients with Parkinson's disease. Brain Behav 7(10):e00806. https://doi.org/10.1002/brb3.806
Sauerbier A, Jitkritsadakul O, Titova N, Klingelhoefer L, Tsuboi Y, Carr H, Kumar H, Banerjee R, Erro R, Bhidayasiri R, Schrag A, Zis P, Lim SY, Al-Hashel JY, Kamel WA, Martinez-Martin P, Ray Chaudhuri K (2017) Non-motor symptoms assessed by non-motor symptoms questionnaire and non-motor symptoms scale in Parkinson's disease in selected Asian populations. Neuroepidemiology 49(1–2):1–17. https://doi.org/10.1159/000478702
Paul KC, Chuang YH, Shih IF, Keener A, Bordelon Y, Bronstein JM, Ritz B (2019) The association between lifestyle factors and Parkinson's disease progression and mortality. Mov Disord 34(1):58–66. https://doi.org/10.1002/mds.27577
Nicoletti A, Vasta R, Mostile G, Nicoletti G, Arabia G, Iliceto G, Lamberti P, Marconi R, Morgante L, Barone P, Quattrone A, Zappia M (2017) Gender effect on non-motor symptoms in Parkinson's disease: are men more at risk? Parkinsonism Relat Disord 35:69–74. https://doi.org/10.1016/j.parkreldis.2016.12.008
Maeda T, Shimo Y, Chiu SW, Yamaguchi T, Kashihara K, Tsuboi Y, Nomoto M, Hattori N, Watanabe H, Saiki H, group JF (2017) Clinical manifestations of nonmotor symptoms in 1021 Japanese Parkinson's disease patients from 35 medical centers. Parkinsonism Relat Disord 38:54–60. https://doi.org/10.1016/j.parkreldis.2017.02.024
Sauerbier A, Lenka A, Aris A, Pal PK (2017) Nonmotor symptoms in Parkinson's disease: gender and ethnic differences. Int Rev Neurobiol 133:417–446. https://doi.org/10.1016/bs.irn.2017.05.032
Miller IN, Cronin-Golomb A (2010) Gender differences in Parkinson's disease: clinical characteristics and cognition. Mov Disord 25(16):2695–2703. https://doi.org/10.1002/mds.23388
Swick TJ, Friedman JH, Chaudhuri KR, Surmann E, Boroojerdi B, Moran K, Ghys L, Trenkwalder C (2014) Associations between severity of motor function and nonmotor symptoms in Parkinson's disease: a post hoc analysis of the RECOVER Study. Eur Neurol 71(3–4):140–147. https://doi.org/10.1159/000355019
Picillo M, Palladino R, Barone P, Erro R, Colosimo C, Marconi R, Morgante L, Antonini A, Group PS (2017) The PRIAMO study: urinary dysfunction as a marker of disease progression in early Parkinson's disease. Eur J Neurol 24(6):788–795. https://doi.org/10.1111/ene.13290
Storch A, Schneider CB, Wolz M, Sturwald Y, Nebe A, Odin P, Mahler A, Fuchs G, Jost WH, Chaudhuri KR, Koch R, Reichmann H, Ebersbach G (2013) Nonmotor fluctuations in Parkinson disease: severity and correlation with motor complications. Neurology 80(9):800–809. https://doi.org/10.1212/WNL.0b013e318285c0ed
van der Velden RMJ, Broen MPG, Kuijf ML, Leentjens AFG (2018) Frequency of mood and anxiety fluctuations in Parkinson's disease patients with motor fluctuations: as systematic review. Mov Disord 33(10):1521–1527. https://doi.org/10.1002/mds.27465
Seppi K, Weintraub D, Coelho M, Perez-Lloret S, Fox SH, Katzenschlager R, Hametner EM, Poewe W, Rascol O, Goetz CG, Sampaio C (2011) The movement disorder society evidence-based medicine review update: treatments for the non-motor symptoms of Parkinson's disease. Mov Disord 26(Suppl 3):S42–80. https://doi.org/10.1002/mds.23884
Trenkwalder C, Kies B, Rudzinska M, Fine J, Nikl J, Honczarenko K, Dioszeghy P, Hill D, Anderson T, Myllyla V, Kassubek J, Steiger M, Zucconi M, Tolosa E, Poewe W, Surmann E, Whitesides J, Boroojerdi B, Chaudhuri KR, Recover Study G (2011) Rotigotine effects on early morning motor function and sleep in Parkinson's disease: a double-blind, randomized, placebo-controlled study (RECOVER). Mov Disord 26(1):90–99. https://doi.org/10.1002/mds.23441
Simuni T, Caspell-Garcia C, Coffey CS, Weintraub D, Mollenhauer B, Lasch S, Tanner CM, Jennings D, Kieburtz K, Chahine LM, Marek K (2018) Baseline prevalence and longitudinal evolution of non-motor symptoms in early Parkinson's disease: the PPMI cohort. J Neurol Neurosurg Psychiatry 89(1):78–88. https://doi.org/10.1136/jnnp-2017-316213
Erro R, Picillo M, Vitale C, Amboni M, Moccia M, Longo K, Cozzolino A, Giordano F, De Rosa A, De Michele G, Pellecchia MT, Barone P (2013) Non-motor symptoms in early Parkinson's disease: a 2-year follow-up study on previously untreated patients. J Neurol Neurosurg Psychiatry 84(1):14–17. https://doi.org/10.1136/jnnp-2012-303419
Antonini A, Calandrella D, Merello M, Koutsikos K, Pilleri M (2013) Effects of rotigotine on Parkinson's disease-related sleep disturbances. Expert Opin Pharmacother 14(18):2571–2580. https://doi.org/10.1517/14656566.2013.849692
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This is a retrospective study and therefore we do not have informed consent directly from each patients. The Institutional Review Board of Chang Gung Memorial Hospital apporved and endorsed this study (IRB number: 201900366B0).
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Chen, YC., Huang, YZ., Weng, YH. et al. Nonmotor symptoms of 820 Taiwanese patients with Parkinson’s disease: an exploratory-comparative study. J Neurol 267, 1499–1507 (2020). https://doi.org/10.1007/s00415-020-09708-4
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DOI: https://doi.org/10.1007/s00415-020-09708-4