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Published in: Neurological Sciences 4/2015

01-04-2015 | Original Article

The heterogeneity of non-motor symptoms of Parkinson’s disease

Authors: Ning Zhang, Weiguo Liu, Min Ye, Alexander D. Cohen, Yingdong Zhang

Published in: Neurological Sciences | Issue 4/2015

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Abstract

In addition to motor symptoms, patients with Parkinson’s disease (PD) may experience non-motor symptoms (NMS), more often with more advanced disease stage. However, the clinical feature of the NMS and potential risk factors that affect NMS in idiopathic PD patients remain unclear. 493 PD patients diagnosed with PD via the UK. Parkinson’s Disease Society Brain Bank Clinical Diagnostic Criteria and 93 healthy control subjects (CN) were recruited in the current study. Questionnaires were used to assess the NMS, motor symptoms, cognitive function, and disease severity in both groups. Levodopa daily dose was calculated in PD patients. Multivariate linear regression analysis was used to identify the risk factors that potentially affect NMS in PD patients. The results showed that, the NMS occurrence and positive endorsement rate of PD patients were significantly higher compared to CN subjects. Multiple stepwise regression analysis found the motor symptom was the only factor that affected NMS in PD patients within five years of the disease course, whereas motor symptoms, cognitive function, disease severity and Levodopa daily dose significantly affected NMS if the disease course was more than five years. These findings demonstrated that NMS are affected by several risk factors at different stages of PD. The distribution of difference NMS is associated with the severity of motor symptoms and the dosage of anti-PD medications in Chinese PD patients.
Literature
1.
go back to reference Raggi A, Leonardi M, Carella F, Soliveri P, Albanese A, Romito LM (2011) Impact of nonmotor symptoms on disability in patients with Parkinson’s disease. Int J Rehabil Res 34:316–320CrossRefPubMed Raggi A, Leonardi M, Carella F, Soliveri P, Albanese A, Romito LM (2011) Impact of nonmotor symptoms on disability in patients with Parkinson’s disease. Int J Rehabil Res 34:316–320CrossRefPubMed
2.
go back to reference Shearer J, Green C, Counsell CE, Zajicek JP (2012) The impact of motor and non motor symptoms on health state values in newly diagnosed idiopathic Parkinson’s disease. J Neurol 259:462–468CrossRefPubMed Shearer J, Green C, Counsell CE, Zajicek JP (2012) The impact of motor and non motor symptoms on health state values in newly diagnosed idiopathic Parkinson’s disease. J Neurol 259:462–468CrossRefPubMed
3.
go back to reference Ponsen MM, Stoffers D, Booij J, van Eck-Smit BL, Wolters E, Berendse HW (2004) Idiopathic hyposmia as a preclinical sign of Parkinson’s disease. Ann Neurol 56:173–181CrossRefPubMed Ponsen MM, Stoffers D, Booij J, van Eck-Smit BL, Wolters E, Berendse HW (2004) Idiopathic hyposmia as a preclinical sign of Parkinson’s disease. Ann Neurol 56:173–181CrossRefPubMed
4.
go back to reference Aarsland D, Pahlhagen S, Ballard CG, Ehrt U, Svenningsson P (2012) Depression in Parkinson disease–epidemiology, mechanisms and management. Nat Rev Neurol 8:35–47CrossRef Aarsland D, Pahlhagen S, Ballard CG, Ehrt U, Svenningsson P (2012) Depression in Parkinson disease–epidemiology, mechanisms and management. Nat Rev Neurol 8:35–47CrossRef
5.
go back to reference Caballol N, Marti MJ, Tolosa E (2007) Cognitive dysfunction and dementia in Parkinson disease. Mov Disord 22(Suppl 17):S358–S366CrossRefPubMed Caballol N, Marti MJ, Tolosa E (2007) Cognitive dysfunction and dementia in Parkinson disease. Mov Disord 22(Suppl 17):S358–S366CrossRefPubMed
6.
go back to reference Diederich NJ, Fenelon G, Stebbins G, Goetz CG (2009) Hallucinations in Parkinson disease. Nat Rev Neurol 5:331–342CrossRefPubMed Diederich NJ, Fenelon G, Stebbins G, Goetz CG (2009) Hallucinations in Parkinson disease. Nat Rev Neurol 5:331–342CrossRefPubMed
7.
go back to reference Jost WH (2003) Autonomic dysfunctions in idiopathic Parkinson’s disease. J Neurol 250(Suppl 1):I28–I30CrossRefPubMed Jost WH (2003) Autonomic dysfunctions in idiopathic Parkinson’s disease. J Neurol 250(Suppl 1):I28–I30CrossRefPubMed
8.
go back to reference Suzuki K, Miyamoto M, Miyamoto T, Iwanami M, Hirata K (2011) Sleep disturbances associated with Parkinson’s disease. Parkinsons Dis 2011:219056PubMedCentralPubMed Suzuki K, Miyamoto M, Miyamoto T, Iwanami M, Hirata K (2011) Sleep disturbances associated with Parkinson’s disease. Parkinsons Dis 2011:219056PubMedCentralPubMed
9.
go back to reference Fowler CJ (2001) Urinary disorders in Parkinson’s disease and multiple system atrophy. Funct Neurol 16:277–282PubMed Fowler CJ (2001) Urinary disorders in Parkinson’s disease and multiple system atrophy. Funct Neurol 16:277–282PubMed
10.
go back to reference Schestatsky P, Valls-Sole J, Ehlers JA, Rieder CR, Gomes I (2006) Hyperhidrosis in Parkinson’s disease. Mov Disord 21:1744–1748CrossRefPubMed Schestatsky P, Valls-Sole J, Ehlers JA, Rieder CR, Gomes I (2006) Hyperhidrosis in Parkinson’s disease. Mov Disord 21:1744–1748CrossRefPubMed
11.
go back to reference Chaudhuri KR, Schapira AH (2009) Non-motor symptoms of Parkinson’s disease: dopaminergic pathophysiology and treatment. Lancet Neurol 8:464–474CrossRefPubMed Chaudhuri KR, Schapira AH (2009) Non-motor symptoms of Parkinson’s disease: dopaminergic pathophysiology and treatment. Lancet Neurol 8:464–474CrossRefPubMed
12.
go back to reference Chaudhuri KR, Yates L, Martinez-Martin P (2005) The non-motor symptom complex of Parkinson’s disease: a comprehensive assessment is essential. Curr Neurol Neurosci Rep 5:275–283CrossRefPubMed Chaudhuri KR, Yates L, Martinez-Martin P (2005) The non-motor symptom complex of Parkinson’s disease: a comprehensive assessment is essential. Curr Neurol Neurosci Rep 5:275–283CrossRefPubMed
13.
go back to reference Chaudhuri KR, Healy DG, Schapira AH (2006) Non-motor symptoms of Parkinson’s disease: diagnosis and management. Lancet Neurol 5:235–245CrossRefPubMed Chaudhuri KR, Healy DG, Schapira AH (2006) Non-motor symptoms of Parkinson’s disease: diagnosis and management. Lancet Neurol 5:235–245CrossRefPubMed
14.
go back to reference Chaudhuri KR, Odin P, Antonini A, Martinez-Martin P (2011) Parkinson’s disease: the non-motor issues. Parkinsonism Relat Disord 17:717–723CrossRefPubMed Chaudhuri KR, Odin P, Antonini A, Martinez-Martin P (2011) Parkinson’s disease: the non-motor issues. Parkinsonism Relat Disord 17:717–723CrossRefPubMed
15.
go back to reference Salawu FK, Danburam A, Olokoba AB (2010) Non-motor symptoms of Parkinson’s disease: diagnosis and management. Niger J Med 19:126–131CrossRefPubMed Salawu FK, Danburam A, Olokoba AB (2010) Non-motor symptoms of Parkinson’s disease: diagnosis and management. Niger J Med 19:126–131CrossRefPubMed
16.
go back to reference Pellicano C, Benincasa D, Pisani V, Buttarelli FR, Giovannelli M, Pontieri FE (2007) Prodromal non-motor symptoms of Parkinson’s disease. Neuropsychiatr Dis Treat 3:145–152PubMedCentralCrossRefPubMed Pellicano C, Benincasa D, Pisani V, Buttarelli FR, Giovannelli M, Pontieri FE (2007) Prodromal non-motor symptoms of Parkinson’s disease. Neuropsychiatr Dis Treat 3:145–152PubMedCentralCrossRefPubMed
17.
go back to reference Schwarz J, Odin P, Buhmann C, Csoti I, Jost W, Wullner U, Storch A (2011) Depression in Parkinson’s disease. J Neurol 258:S336–S338CrossRefPubMed Schwarz J, Odin P, Buhmann C, Csoti I, Jost W, Wullner U, Storch A (2011) Depression in Parkinson’s disease. J Neurol 258:S336–S338CrossRefPubMed
18.
go back to reference Reijnders JS, Ehrt U, Weber WE, Aarsland D, Leentjens AF (2008) A systematic review of prevalence studies of depression in Parkinson’s disease. Mov Disord 23(183–189):313 Reijnders JS, Ehrt U, Weber WE, Aarsland D, Leentjens AF (2008) A systematic review of prevalence studies of depression in Parkinson’s disease. Mov Disord 23(183–189):313
19.
go back to reference Kleiner-Fisman G, Martine R, Lang AE, Stern MB (2011) Development of a non-motor fluctuation assessment instrument for Parkinson disease. Parkinsons Dis 2011:292719PubMedCentralPubMed Kleiner-Fisman G, Martine R, Lang AE, Stern MB (2011) Development of a non-motor fluctuation assessment instrument for Parkinson disease. Parkinsons Dis 2011:292719PubMedCentralPubMed
20.
go back to reference Romenets SR, Wolfson C, Galatas C, Pelletier A, Altman R, Wadup L, Postuma RB (2012) Validation of the non-motor symptoms questionnaire (NMS-Quest). Parkinsonism Relat Disord 18:54–58CrossRefPubMed Romenets SR, Wolfson C, Galatas C, Pelletier A, Altman R, Wadup L, Postuma RB (2012) Validation of the non-motor symptoms questionnaire (NMS-Quest). Parkinsonism Relat Disord 18:54–58CrossRefPubMed
21.
go back to reference 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, Williamsc 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 22:1623–1629CrossRefPubMed 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, Williamsc 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 22:1623–1629CrossRefPubMed
22.
go back to reference Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55:181–184PubMedCentralCrossRefPubMed Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55:181–184PubMedCentralCrossRefPubMed
23.
go back to reference Katzman R, Zhang MY, Ouang-Ya-Qu Wang ZY, Liu WT, Yu E, Wong SC, Salmon DP, Grant I (1988) A Chinese version of the Mini-Mental State Examination; impact of illiteracy in a Shanghai dementia survey. J Clin Epidemiol 41:971–978CrossRefPubMed Katzman R, Zhang MY, Ouang-Ya-Qu Wang ZY, Liu WT, Yu E, Wong SC, Salmon DP, Grant I (1988) A Chinese version of the Mini-Mental State Examination; impact of illiteracy in a Shanghai dementia survey. J Clin Epidemiol 41:971–978CrossRefPubMed
24.
go back to reference Martinez-Martin P, Gil-Nagel A, Gracia LM, Gomez JB, Martinez-Sarries J, Bermejo F (1994) Unified Parkinson’s Disease Rating Scale characteristics and structure. The Cooperative Multicentric Group. Mov Disord 9:76–83CrossRefPubMed Martinez-Martin P, Gil-Nagel A, Gracia LM, Gomez JB, Martinez-Sarries J, Bermejo F (1994) Unified Parkinson’s Disease Rating Scale characteristics and structure. The Cooperative Multicentric Group. Mov Disord 9:76–83CrossRefPubMed
25.
go back to reference Goetz CG, Poewe W, Rascol O, Sampaio C, Stebbins GT, Counsell C, Giladi N, Holloway RG, Moore CG, Wenning GK, Yahr MD, Seidl L (2004) Movement Disorder Society Task Force report on the Hoehn and Yahr staging scale: status and recommendations. Mov Disord 19:1020–1028CrossRefPubMed Goetz CG, Poewe W, Rascol O, Sampaio C, Stebbins GT, Counsell C, Giladi N, Holloway RG, Moore CG, Wenning GK, Yahr MD, Seidl L (2004) Movement Disorder Society Task Force report on the Hoehn and Yahr staging scale: status and recommendations. Mov Disord 19:1020–1028CrossRefPubMed
26.
go back to reference Wang G, Hong Z, Cheng Q, Xiao Q, Wang Y, Zhang J, Ma JF, Wang XJ, Zhou HY, Chen SD (2009) Validation of the Chinese non-motor symptoms scale for Parkinson’s disease: results from a Chinese pilot study. Clin Neurol Neurosurg 111:523–526CrossRefPubMed Wang G, Hong Z, Cheng Q, Xiao Q, Wang Y, Zhang J, Ma JF, Wang XJ, Zhou HY, Chen SD (2009) Validation of the Chinese non-motor symptoms scale for Parkinson’s disease: results from a Chinese pilot study. Clin Neurol Neurosurg 111:523–526CrossRefPubMed
27.
go back to reference Hobson DE, Lang AE, Martin WR, Razmy A, Rivest J, Fleming J (2002) Excessive daytime sleepiness and sudden-onset sleep in Parkinson disease: a survey by the Canadian Movement Disorders Group. JAMA 287:455–463CrossRefPubMed Hobson DE, Lang AE, Martin WR, Razmy A, Rivest J, Fleming J (2002) Excessive daytime sleepiness and sudden-onset sleep in Parkinson disease: a survey by the Canadian Movement Disorders Group. JAMA 287:455–463CrossRefPubMed
28.
go back to reference Gupta M, Singh G, Khwaja GA, Mehndiratta MM (2004) Hallucinations in Parkinson’s disease: a study of forty three patients. J Assoc Physicians India 52:703–706PubMed Gupta M, Singh G, Khwaja GA, Mehndiratta MM (2004) Hallucinations in Parkinson’s disease: a study of forty three patients. J Assoc Physicians India 52:703–706PubMed
29.
30.
31.
go back to reference Muller T (2002) Drug treatment of non-motor symptoms in Parkinson’s disease. Expert Opin Pharmacother 3:381–388CrossRefPubMed Muller T (2002) Drug treatment of non-motor symptoms in Parkinson’s disease. Expert Opin Pharmacother 3:381–388CrossRefPubMed
32.
33.
go back to reference Witjas T, Kaphan E, Azulay JP (2007) Non-motor fluctuations in Parkinson’s disease. Rev Neurol (Paris) 163:846–850CrossRef Witjas T, Kaphan E, Azulay JP (2007) Non-motor fluctuations in Parkinson’s disease. Rev Neurol (Paris) 163:846–850CrossRef
34.
go back to reference Maetzler W, Liepelt I, Berg D (2009) Progression of Parkinson’s disease in the clinical phase: potential markers. Lancet Neurol 8:1158–1171CrossRefPubMed Maetzler W, Liepelt I, Berg D (2009) Progression of Parkinson’s disease in the clinical phase: potential markers. Lancet Neurol 8:1158–1171CrossRefPubMed
35.
go back to reference O’Sullivan SS, Williams DR, Gallagher DA, Massey LA, Silveira-Moriyama L, Lees AJ (2008) Nonmotor symptoms as presenting complaints in Parkinson’s disease: a clinicopathological study. Mov Disord 23:101–106CrossRefPubMed O’Sullivan SS, Williams DR, Gallagher DA, Massey LA, Silveira-Moriyama L, Lees AJ (2008) Nonmotor symptoms as presenting complaints in Parkinson’s disease: a clinicopathological study. Mov Disord 23:101–106CrossRefPubMed
36.
go back to reference Welsh M (2004) Parkinson’s disease and quality of life: issues and challenges beyond motor symptoms. Neurol Clin 22:S141–S148CrossRefPubMed Welsh M (2004) Parkinson’s disease and quality of life: issues and challenges beyond motor symptoms. Neurol Clin 22:S141–S148CrossRefPubMed
37.
go back to reference Schrag A, Jahanshahi M, Quinn N (2000) What contributes to quality of life in patients with Parkinson’s disease? J Neurol Neurosurg Psychiatry 69:308–312PubMedCentralCrossRefPubMed Schrag A, Jahanshahi M, Quinn N (2000) What contributes to quality of life in patients with Parkinson’s disease? J Neurol Neurosurg Psychiatry 69:308–312PubMedCentralCrossRefPubMed
38.
go back to reference 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 20:190–199CrossRefPubMed 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 20:190–199CrossRefPubMed
39.
go back to reference Witjas T, Kaphan E, Azulay JP, Blin O, Ceccaldi M, Pouget J, Poncet M, Cherif AA (2002) Nonmotor fluctuations in Parkinson’s disease: frequent and disabling. Neurology 59:408–413CrossRefPubMed Witjas T, Kaphan E, Azulay JP, Blin O, Ceccaldi M, Pouget J, Poncet M, Cherif AA (2002) Nonmotor fluctuations in Parkinson’s disease: frequent and disabling. Neurology 59:408–413CrossRefPubMed
40.
go back to reference Czernecki V, Schupbach M, Yaici S, Levy R, Bardinet E, Yelnik J, Dubois B, Agid Y (2008) Apathy following subthalamic stimulation in Parkinson disease: a dopamine responsive symptom. Mov Disord 23:964–969CrossRefPubMed Czernecki V, Schupbach M, Yaici S, Levy R, Bardinet E, Yelnik J, Dubois B, Agid Y (2008) Apathy following subthalamic stimulation in Parkinson disease: a dopamine responsive symptom. Mov Disord 23:964–969CrossRefPubMed
Metadata
Title
The heterogeneity of non-motor symptoms of Parkinson’s disease
Authors
Ning Zhang
Weiguo Liu
Min Ye
Alexander D. Cohen
Yingdong Zhang
Publication date
01-04-2015
Publisher
Springer Milan
Published in
Neurological Sciences / Issue 4/2015
Print ISSN: 1590-1874
Electronic ISSN: 1590-3478
DOI
https://doi.org/10.1007/s10072-014-1993-0

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