Skip to main content
Log in

Nonmotor symptoms of 820 Taiwanese patients with Parkinson’s disease: an exploratory-comparative study

  • Original Communication
  • Published:
Journal of Neurology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. 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

    Article  PubMed  Google Scholar 

  2. 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

    Article  CAS  PubMed  Google Scholar 

  3. 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

    Article  PubMed  Google Scholar 

  4. 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

    Article  PubMed  Google Scholar 

  5. 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

    Article  PubMed  Google Scholar 

  6. 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

    PubMed  PubMed Central  Google Scholar 

  7. 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

    Article  PubMed  Google Scholar 

  8. 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

    Article  PubMed  Google Scholar 

  9. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. 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

    Article  PubMed  Google Scholar 

  11. 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

    Article  PubMed  Google Scholar 

  12. 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

    Article  PubMed  Google Scholar 

  13. 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

    Article  PubMed  Google Scholar 

  14. 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

    Article  PubMed  Google Scholar 

  15. 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

    Article  CAS  PubMed  Google Scholar 

  16. 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

    Article  CAS  PubMed  Google Scholar 

  17. 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

    Article  CAS  Google Scholar 

  18. 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

    Article  PubMed  PubMed Central  Google Scholar 

  19. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. 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

    Article  PubMed  Google Scholar 

  21. 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

    Article  PubMed  PubMed Central  Google Scholar 

  22. 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

    Article  PubMed  PubMed Central  Google Scholar 

  23. 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

    Article  PubMed  Google Scholar 

  24. 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

    Article  PubMed  PubMed Central  Google Scholar 

  25. 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

    Article  CAS  PubMed  Google Scholar 

  26. 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

    Article  PubMed  Google Scholar 

  27. 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

    Article  PubMed  Google Scholar 

  28. 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

    Article  PubMed  PubMed Central  Google Scholar 

  29. 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

    Article  PubMed  Google Scholar 

  30. 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

    Article  CAS  PubMed  Google Scholar 

  31. 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

    Article  PubMed  Google Scholar 

  32. 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

    Article  PubMed  Google Scholar 

  33. 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

    Article  PubMed  PubMed Central  Google Scholar 

  34. 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

    Article  PubMed  Google Scholar 

  35. 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

    Article  PubMed  Google Scholar 

  36. 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

    Article  PubMed  Google Scholar 

  37. 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

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rou‐Shayn Chen.

Ethics declarations

Conflicts of interests

The authors declare that they have no conflict of interest.

Ethical standards

This chapter does not contain any studies with animals performed by any of the authors.

Informed consent

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).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00415-020-09708-4

Keywords

Navigation