Skip to main content

Advertisement

SpringerLink
Log in

Gender-related differences in the burden of non-motor symptoms in Parkinson’s disease

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

Abstract

Differences in the expression of non-motor symptoms (NMS) by Parkinson’s disease (PD) patients may have important implications for their management and prognosis. Gender is a basic epidemiological variable that could influence such expression. The present study evaluated the prevalence and severity of NMS by gender in an international sample of 951 PD patients, 62.63% males, using the non-motor symptoms scale (NMSS). Assessments for motor impairment and complications, global severity, and health state were also applied. All disease stages were included. No significant gender differences were found for demographic and clinical characteristics. For the entire sample, the most prevalent symptoms were Nocturia (64.88%) and Fatigue (62.78%) and the most prevalent affected domains were Sleep/Fatigue (84.02%) and Miscellaneous (82.44%). Fatigue, feelings of nervousness, feelings of sadness, constipation, restless legs, and pain were more common and severe in women. On the contrary, daytime sleepiness, dribbling saliva, interest in sex, and problems having sex were more prevalent and severe in men. Regarding the NMSS domains, Mood/Apathy and Miscellaneous problems (pain, loss of taste or smell, weight change, and excessive sweating) were predominantly affected in women and Sexual dysfunction in men. No other significant differences by gender were observed. To conclude, in this study significant differences between men and women in prevalence and severity of fatigue, mood, sexual and digestive problems, pain, restless legs, and daytime sleepiness were found. Gender-related patterns of NMS involvement may be relevant for clinical trials in PD.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Chaudhuri KR, Yates L, Martinez-Martin P (2005) The non-motor symptom complex of Parkinson’s disease: time for a comprehensive assessment. Curr Neurol Neurosci Rep 5:275–283

    Article  PubMed  Google Scholar 

  2. Hely MA, Morris JGL, Reid WGJ, Trafficante R (2005) Sydney multicenter study of Parkinson’s disease: non-l-dopa-responsive problems dominate at 15 years. Mov Disord 20:190–199

    Article  PubMed  Google Scholar 

  3. Chaudhuri KR, Healy D, Schapira AHV (2006) The non-motor symptoms of Parkinson’s disease. Diagnosis and management. Lancet Neurol 5:235–245

    Article  PubMed  Google Scholar 

  4. Martinez-Martin P, Schapira AH, Stocchi F, Sethi K, Odin P, Macphee G et al (2007) Prevalence of nonmotor symptoms in Parkinson’s disease in an international setting: Study using nonmotor symptoms questionnaire in 545 patients. Mov Disord 22:1623–1629

    Article  PubMed  Google Scholar 

  5. Shulman LM, Taback RL, Rabinstein AA, Weiner WJ (2002) Non-recognition of depression and other non-motor symptoms in Parkinson’s disease. Parkinsonism Relat Disord 8:193–197

    Article  PubMed  CAS  Google Scholar 

  6. Chaudhuri KR, Prieto-Jurcynska C, Naidu Y, Mitra T, Frades-Payo B, Tluk S et al (2010) The non declaration of non motor symptoms of Parkinson’s disease to health care professionals: an international study using the non motor symptoms questionnaire. Mov Disord 25:704–709

    Article  PubMed  Google Scholar 

  7. Martinez-Martin P, Marinus J, van Hilten B (2009) Assessment tools for non-motor symptoms of Parkinson’s disease. In: Chaudhuri KR, Tolosa E, Schapira A, Poewe W (eds) Non-motor symptoms of Parkinson’s disease. Oxford University Press, Oxford, pp 47–58

    Google Scholar 

  8. Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P et al (2008) Movement disorder society-sponsored revision of the unified Parkinson’s disease rating scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord 23:2129–2170

    Article  PubMed  Google Scholar 

  9. Martinez-Martin P, Rodriguez-Blazquez C, Abe K, Bhattacharyya KB, Bloem BR, Carod-Artal FJ et al (2009) International study on the psychometric attributes of the non-motor symptoms scale in Parkinson disease. Neurology 73:1584–1591

    Article  PubMed  CAS  Google Scholar 

  10. Chaudhuri KR, Martinez-Martin P, Brown RG, Sethi K, Stocchi F, Odin P et al (2007) The metric properties of a novel non-motor symptoms scale for Parkinson’s disease: results from an international pilot study. Mov Disord 22:1901–1911

    Article  PubMed  Google Scholar 

  11. Kasten M, Chade A, Tanner CM (2007) Epidemiology of Parkinson’s disease. In: Koller WC, Melamed E (eds) Parkinson’s Disease and Related Disorders. Part I. Handbook of Clinical Neurology vol. 83, 3rd edn. Elsevier BV, Amsterdam, pp 129–151

    Chapter  Google Scholar 

  12. Lyons K, Hubble J, Tröster A, Pahwa R, Koller WC (1998) Gender differences in Parkinson’s disease. Clin Neuropharmacol 21:118–121

    PubMed  CAS  Google Scholar 

  13. Scott B, Borgman A, Engler H, Johnels B, Aquilonius SM (2000) Gender differences in Parkinson’s disease symptom profile. Acta Neurol Scand 102:37–43

    Article  PubMed  CAS  Google Scholar 

  14. Van Den Eeden SK, Tanner CM, Bernstein AL, Fross RD, Leimpeter A, Bloch DA et al (2003) Incidence of Parkinson’s disease: variation by age, gender, and race/ethnicity. Am J Epidemiol 157:1015–1022

    Article  Google Scholar 

  15. Baba Y, Putzke JD, Whaley NR, Wszolek ZK, Uitti RJ (2005) Gender and the Parkinson’s disease phenotype. J Neurol 252:1201–1205

    Article  PubMed  Google Scholar 

  16. Haaxma CA, Bloem BR, Borm GF, Oyen WJ, Leenders KL, Eshuis S et al (2007) Gender differences in Parkinson’s disease. J Neurol Neurosurg Psychiatry 78:819–824

    Article  PubMed  Google Scholar 

  17. Ehrt U, Brønnick K, De Deyn PP, Emre M, Tekin S, Lane R et al (2007) Subthreshold depression in patients with Parkinson’s disease and dementia–clinical and demographic correlates. Int J Geriatr Psychiatry 22:980–985

    Article  PubMed  Google Scholar 

  18. Celikel E, Ozel-Kizil ET, Akbostanci MC, Cevik A (2008) Assessment of sexual dysfunction in patients with Parkinson’s disease: a case–control study. Eur J Neurol 15:1168–1172

    Article  PubMed  CAS  Google Scholar 

  19. Solimeo S (2008) Sex and gender in older adults’ experience of Parkinson’s disease. J Gerontol Soc Sci 63B:S42–S48

    Article  Google Scholar 

  20. Miller IN, Cronin-Golomb A (2010) Gender differences in Parkinson’s disease: clinical characteristics and cognition. Mov Disord 25:2695–2703

    Article  PubMed  Google Scholar 

  21. Krishnan S, Sarma G, Sarma S, Kishore A (2011) Do Nonmotor Symptoms in Parkinson’s disease differ from normal aging? Mov Disord. doi:10.1002/mds.23826

  22. Lees AJ, Hardy J, Revesz T (2009) Parkinson’s disease. Lancet 373:2055–2066

    Article  PubMed  CAS  Google Scholar 

  23. Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression, and mortality. Neurology 17:427–442

    Article  PubMed  CAS  Google Scholar 

  24. Marinus J, Visser M, Stiggelbout AM, Martin Rabey J, Martinez-Martin P, Bonuccelli U et al (2004) A short scale for the assessment of motor impairments and disabilities in Parkinson’s disease: the SPES/SCOPA. J Neurol Neurosurg Psychiatry 75:388–395

    Article  PubMed  CAS  Google Scholar 

  25. Martinez-Martin P, Benito-Leon J, Burguera JA, Castro A, Linazasoro G, Martinez-Castrillo JC et al (2005) The SCOPA-Motor Scale for assessment of Parkinson’s disease is a consistent and valid measure. J Clin Epidemiol 58:674–679

    Article  PubMed  Google Scholar 

  26. Martinez-Martin P, Forjaz MJ, Cubo E, Frades B, de Pedro Cuesta J, Project Members ELEP (2006) Global versus factor-related impression of severity in Parkinson’s disease: A new clinimetric index (CISI-PD). Mov Disord 21:208–214

    Article  PubMed  Google Scholar 

  27. Martinez-Martin P, Rodriguez-Blazquez C, Forjaz MJ, de Pedro J, n Longitudinal PD, Group Patient Study (2009) The clinical impression of severity index for Parkinson’s disease: international validation study. Mov Disord 24:211–217

    Article  PubMed  Google Scholar 

  28. Group EuroQol (1990) EuroQol- a new facility for the measurement of health related quality of life. Health Policy 16:199–208

    Article  Google Scholar 

  29. Jenkinson C, Fitzpatrick R, Peto V, Greenhall R, Hyman N (1997) The PDQ-8: development and validation of a short-form Parkinson’s disease questionnaire. Psychol Health 12:805–814

    Article  Google Scholar 

  30. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc 57:289–300

    Google Scholar 

  31. Friedman JH, Friedman H (1993) Fatigue in Parkinson’s disease. Neurology 43:2016–2018

    Article  PubMed  CAS  Google Scholar 

  32. Martinez-Martin P, Catalan MJ, Benito-Leon J et al (2006) Impact of fatigue in Parkinson’s disease: the fatigue impact scale for daily use (D-FIS). Qual Life Res 15:597–606

    Article  PubMed  Google Scholar 

  33. Friedman JH, Brown RG, Comella C et al (2007) Fatigue in Parkinson’s disease: a review. Mov Disord 22:297–308

    Article  PubMed  Google Scholar 

  34. Barone P, Antonini A, Colosimo C, Marconi R, Morgante L, Avarello TP et al (2009) The PRIAMO study: a multicenter assessment of nonmotor symptoms and their impact on quality of life in Parkinson’s disease. Mov Disord 24:1641–1649

    Article  PubMed  Google Scholar 

  35. Beiske AG, Loge JH, Hjermstad MJ, Svensson E (2010) Fatigue in Parkinson’s disease: prevalence and associated factors. Mov Disord 25:2456–2460

    Article  PubMed  Google Scholar 

  36. Stein MB, Heuser IJ, Juncos JL, Uhde TW (1990) Anxiety disorders in patients with Parkinson’s disease. Am J Psychiatry 147:217–220

    PubMed  CAS  Google Scholar 

  37. Richard IH (2005) Anxiety disorders in Parkinson’s disease. Adv Neurol 96:42–55

    PubMed  Google Scholar 

  38. Weintraub D, Burn DJ (2011) Parkinson’s disease: the quintessential neuropsychiatric disorder. Mov Disord 26:1022–1031

    Article  PubMed  Google Scholar 

  39. Blonder LX, Slevin JT (2011) Emotional dysfunction in Parkinson’s disease. Behav Neurol 24:201–217

    PubMed  Google Scholar 

  40. Martinez-Martin P, Damian J (2010) Depression and anxiety in Parkinson’s disease. Nature Rev Neurol 6:243–245

    Article  Google Scholar 

  41. Leentjens AF, Dujardin K, Marsh L, Martinez-Martin P, Richard IH, Starkstein SE (2011) Symptomatology and markers of anxiety disorders in Parkinson’s disease: a cross-sectional study. Mov Disord 26:484–492

    Article  PubMed  Google Scholar 

  42. Carod-Artal FJ, Vargas AP, Martínez-Martín P (2007) Determinants of quality of life in Brazilian patients with Parkinson’s disease. Mov Disord 22:1408–1415

    Article  PubMed  Google Scholar 

  43. Kulisevsky J, Pagonabarraga J, Pascual-Sedano B, García-Sánchez C, Gironell A, Study Trapecio Group (2008) Prevalence and correlates of neuropsychiatric symptoms in Parkinson’s disease without dementia. Mov Disord 23:1889–1896

    Article  PubMed  Google Scholar 

  44. Reijnders JSAM, Ehrt U, Weber WEJ, Aarsland D, Leentjens AFG (2008) A systematic review of prevalence studies of depression in Parkinson’s disease. Mov Disord 23:183–189

    Article  PubMed  Google Scholar 

  45. Rojo A, Aguilar M, Garolera MT, Cubo E, Navas I, Quintana S (2003) Depression in Parkinson’s disease: clinical correlates and outcome. Parkinsonism Relat Disord 10:23–28

    Article  PubMed  CAS  Google Scholar 

  46. Krogh K, Ostergaard K, Sabroe S, Laurberg S (2008) Clinical aspects of bowel symptoms in Parkinson’s disease. Acta Neurol Scand 117:60–64

    PubMed  CAS  Google Scholar 

  47. Kamm MA (2003) Constipation and its management. Br Med J 327:459–460

    Article  Google Scholar 

  48. Goetz CG, Tanner CM, Levy M, Wilson RS, Garron DC (1986) Pain in Parkinson’s disease. Mov Disord 1:45–49

    Article  PubMed  CAS  Google Scholar 

  49. Defazio G, Berardelli A, Fabbrini G, Martino D, Fincati E, Fiaschi A et al (2008) Pain as a nonmotor symptom of Parkinson disease. Arch Neurol 65:1191–1194

    Article  PubMed  Google Scholar 

  50. Beiske AG, Loge JH, Rønningen A, Svensson E (2009) Pain in Parkinson’s disease: prevalence and characteristics. Pain 141:173–177

    Article  PubMed  CAS  Google Scholar 

  51. Zambito Marsala S, Tinazzi M, Vitaliani R, Recchia S, Fabris F, Marchini C et al (2011) Spontaneous pain, pain threshold, and pain tolerance in Parkinson’s disease. J Neurol 258:627–633

    Article  PubMed  Google Scholar 

  52. Hanagasi HA, Akat S, Gurvit H, Yazici J, Emre M (2011) Pain is common in Parkinson’s disease. Clin Neurol Neurosurg 113:11–13

    Article  PubMed  Google Scholar 

  53. Gomez-Esteban JC, Zarranz JJ, Tijero B, Velasco F, Barcena J, Rouco I et al (2007) Restless legs syndrome in Parkinson’s disease. Mov Disord 22:1912–1916

    Article  PubMed  Google Scholar 

  54. Peralta CM, Frauscher B, Seppi K, Wolf E, Wenning GK, Högl B et al (2009) Restless legs syndrome in Parkinson’s disease. Mov Disord 24:2076–2080

    Article  PubMed  Google Scholar 

  55. Verbaan D, van Rooden SM, van Hilten JJ, Rijsman RM (2010) Prevalence and clinical profile of restless legs syndrome in Parkinson’s disease. Mov Disord 25:2142–2147

    Article  PubMed  Google Scholar 

  56. Ondo WG, Dat Vuong K, Khan H, Atassi F, Kwak C, Jankovic J (2001) Daytime sleepiness and other sleep disorders in Parkinson’s disease. Neurology 57:1392–1396

    Article  PubMed  CAS  Google Scholar 

  57. Gjerstad MD, Alves G, Wentzel-Larsen T, Aarsland A, Larsen JP (2006) Excessive daytime sleepiness in Parkinson disease. Is it the drugs or the disease? Neurology 67:853–858

    Article  PubMed  CAS  Google Scholar 

  58. Stavitsky K, Cronin-Golomb A (2011) Sleep quality in Parkinson disease: an examination of clinical variables. Cogn Behav Neurol 24:43–49

    Article  PubMed  Google Scholar 

  59. Merello M (2008) Sialorrhoea and drooling in patients with Parkinson’s disease: epidemiology and management. Drugs Aging 25:1007–1019

    Article  PubMed  CAS  Google Scholar 

  60. Wüllner U, Schmitz-Hübsch T, Antony G, Fimmers R, Spottke A, Oertel WH et al (2007) Autonomic dysfunction in 3414 Parkinson’s disease patients enrolled in the German Network on Parkinson’s disease (KNP e.V.): the effect of ageing. Eur J Neurol 14:1405–1408

    Article  PubMed  Google Scholar 

  61. Mshana G, Dotchin CL, Walker RW (2011) We call it the shaking illness: perceptions and experiences of Parkinson’s disease in rural northern Tanzania. BMC Public Health 11:219

    Article  PubMed  Google Scholar 

  62. Chaudhuri KR, Schapira AHV (2009) Non-motor symptoms of Parkinson’s disease: dopaminergic pathophysiology and treatment. Lancet Neurol 8:464–474

    Article  PubMed  CAS  Google Scholar 

  63. Gillies GE, McArthur S (2010) Estrogen actions in the brain and the basis for differential action in men and women: a case for sex-specific medicines. Pharmacol Rev 62:155–198

    Article  PubMed  CAS  Google Scholar 

  64. Fuhrer R, Wessely S (1995) The epidemiology of fatigue and depression: a French primary-care study. Psychol Med 25:895–905

    Article  PubMed  CAS  Google Scholar 

  65. Sharpe M, Wilks D (2002) Fatigue. Br Med J 325:480–483

    Article  Google Scholar 

  66. Howell HB, Brawman-Mintzer O, Monnier J, Yonkers KA (2001) Generalized anxiety disorder in women. Psychiatr Clin North Am 24:165–178

    Article  PubMed  CAS  Google Scholar 

  67. Tyrer P, Baldwin D (2006) Generalised anxiety disorder. Lancet 368:2156–2166

    Article  PubMed  Google Scholar 

  68. Djernes JK (2006) Prevalence and predictors of depression in populations of elderly: a review. Acta Psychiatr Scand 113:372–387

    Article  PubMed  CAS  Google Scholar 

  69. Vink D, Aartsen MJ, Comijs HC, Heymans MW, Penninx BW, Stek ML et al (2009) Onset of anxiety and depression in the aging population: comparison of risk factors in a 9-year prospective study. Am J Geriatr Psychiatry 17:642–652

    Article  PubMed  Google Scholar 

  70. Mourão AF, Blyth FM, Branco JC (2010) Generalised musculoskeletal pain syndromes. Best Pract Res Clin Rheumatol 24:829–840

    Article  PubMed  Google Scholar 

  71. Leresche L (2011) Defining gender disparities in pain management. Clin Orthop Relat Res 469:1871–1877

    Article  PubMed  Google Scholar 

  72. Yeh P, Walters AS, Tsuang JW (2011) Restless legs syndrome: a comprehensive overview on its epidemiology, risk factors, and treatment. Sleep Breath. doi:10.1007/s11325-011-0606-x

  73. Krishnan V, Collop NA (2006) Gender differences in sleep disorders. Curr Opin Pulm Med 12:383–389

    Article  PubMed  Google Scholar 

  74. Honig H, Antonini A, Martinez-Martin P, Forgacs I, Faye GC, Fox T et al (2009) Intrajejunal levodopa infusion in Parkinson’s disease: a pilot multicenter study of effects on nonmotor symptoms and quality of life. Mov Disord 24:1468–1474

    Article  PubMed  Google Scholar 

  75. Reddy P, Martinez-Martin P, Antonini A, Odin P, Martin A, Calandrella D (2011) Comparison of non-motor effects of subcutaneous apomorphine infusion and intrajejunal levodopa infusion in advanced Parkinson’s disease. Eur J Neurol 18(Suppl 2):242

    Google Scholar 

Download references

Conflicts of interest

The authors have no conflicts of interest or competing financial interests with regards to this article.

Author information

Authors and Affiliations

  1. Research Unit, Alzheimer Center Reina Sofia Foundation, and CIBERNED. Carlos III Institute of Health, C/. Valderrebollo, 5, 28031, Madrid, Spain

    Pablo Martinez-Martin

  2. Department of Neurology, Emergency University Hospital, Faculty of Medicine, Transylvania University, Braşov, Romania

    Cristian Falup Pecurariu

  3. Department of Neurology, University Hospital, Lund, Sweden

    Per Odin

  4. Department of Neurology, Central Hospital, Bremerhaven, Germany

    Per Odin

  5. Department of Neurology, Leiden University Medical Center, Leiden, The Netherlands

    Jacobus J. van Hilten

  6. Department for Parkinson’s Disease, IRCCS San Camillo, Venice, Italy

    Angelo Antonini

  7. Statistical Analysis Unit, Center for Human and Social Sciences, Spanish Council for Scientific Research, Madrid, Spain

    Jose M. Rojo-Abuin

  8. Movement Disorders Section, Department of Neurology, Universidade Federal de Sao Paulo, Sao Paolo, Brazil

    Vanderci Borges

  9. Center of Parkinsonism and Movement Disorders, Paracelsus-Elena Hospital, Kassel, Germany

    Claudia Trenkwalder

  10. Alzheimer Disease Research, Karolinska Institutet, Stockholm, Sweden

    Dag Aarsland

  11. Department of Psychiatry, Stavanger University Hospital, Stavanger, Norway

    Dag Aarsland

  12. Department of Medicine, Imperial College, London, UK

    David J. Brooks

  13. National Parkinson Foundation Centre of Excellence, King’s College Hospital and University Hospital Lewisham, London, UK

    Kallol Ray Chaudhuri

Authors
  1. Pablo Martinez-Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cristian Falup Pecurariu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Per Odin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jacobus J. van Hilten
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Angelo Antonini
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jose M. Rojo-Abuin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Vanderci Borges
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Claudia Trenkwalder
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Dag Aarsland
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. David J. Brooks
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Kallol Ray Chaudhuri
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pablo Martinez-Martin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Martinez-Martin, P., Falup Pecurariu, C., Odin, P. et al. Gender-related differences in the burden of non-motor symptoms in Parkinson’s disease. J Neurol 259, 1639–1647 (2012). https://doi.org/10.1007/s00415-011-6392-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00415-011-6392-3

Keywords

Search

Navigation