Skip to main content
Top
Published in: Journal of Neurology 2/2014

01-02-2014 | Original Communication

Association between fatigue and other motor and non-motor symptoms in Parkinson’s disease patients

Authors: Paolo Solla, Antonino Cannas, Cesare Salvatore Mulas, Silvia Perra, Andrea Corona, Pier Paolo Bassareo, Francesco Marrosu

Published in: Journal of Neurology | Issue 2/2014

Login to get access

Abstract

Although fatigue is a common non-motor symptom in patients affected by Parkinson’s disease (PD), its association with motor and other non-motor symptoms is still largely unclear. We assessed fatigue in PD patients studying the possible association with motor and non-motor symptoms. Eighty-one PD patients were included in the study. The PD Fatigue Scale (PFS) and the Fatigue Severity Scale (FSS) scale were used to measure fatigue. Non-motor symptoms were assessed with the Non-Motor Symptoms Scale (NMSS). Motor impairment was assessed using the modified Hoehn and Yahr (HY) staging and the Unified PD Rating Scale (UPDRS) part-III and IV. Bivariate tests comparing all independent variables between patients with our without fatigue were used. Significant predictors of presence and severity of fatigue were determined with different models of logistic regression analyses. Fatigue severity was significantly higher in female patients. Bivariate test showed significant higher NMSS score in fatigued patients according to PFS (p < 0.00001) and FFS (p < 0.001), while HY was higher only in fatigued patients according to FSS (p < 0.022). Significant correlations between severity of fatigue and HY stage (p < 0.002) and UPDRS-III score (p < 0.001) were found, while, among specific non-motor symptoms, anhedonia presented with the most significant correlation (p < 0.003). Binary logistic regression confirmed NMSS as the main variable predicting presence of fatigue, while HY was significant as predicting variable only in the FSS model. Strongest non-motor symptoms predictors of severity were those included in Domain 3 (mood/anxiety) and Domain 2 (sleep disorders) of the NMSS. A significant increase in severity of fatigue related to the burden of non-motor symptoms (mainly affective and sleep disorders) was observed. Our findings indicate a moderate discrepancy in the ratings of the two fatigue scales, with PFS principally directed towards the burden of non-motor symptoms. Finally, the accurate individuation of the factors underlying fatigue, assessed with the systematic administration of holistic evaluation scales such as the NMSS, might improve current strategies used in the treatment of this disabling condition.
Literature
1.
go back to reference Langston JW (2006) The Parkinson’s complex: parkinsonism is just the tip of the iceberg. Ann Neurol 59(4):591–596CrossRefPubMed Langston JW (2006) The Parkinson’s complex: parkinsonism is just the tip of the iceberg. Ann Neurol 59(4):591–596CrossRefPubMed
2.
go back to reference Chaudhuri KR, Healy D, Schapira AHV (2006) The non-motor symptoms of Parkinson’s disease. Diagnosis and management. Lancet Neurol 5:235–245CrossRefPubMed Chaudhuri KR, Healy D, Schapira AHV (2006) The non-motor symptoms of Parkinson’s disease. Diagnosis and management. Lancet Neurol 5:235–245CrossRefPubMed
3.
go back to reference Beiske AG, Svensson E (2010) Fatigue in Parkinson’s disease: a short update. Acta Neurol Scand Suppl 190:78–81CrossRefPubMed Beiske AG, Svensson E (2010) Fatigue in Parkinson’s disease: a short update. Acta Neurol Scand Suppl 190:78–81CrossRefPubMed
4.
go back to reference Gelb DJ, Oliver E, Gilman S (1999) Diagnostic criteria for Parkinson disease. Arch Neurol 56(1):33–39CrossRefPubMed Gelb DJ, Oliver E, Gilman S (1999) Diagnostic criteria for Parkinson disease. Arch Neurol 56(1):33–39CrossRefPubMed
5.
6.
go back to reference Fahn S, Elton R (1987) Members of the UPDRS Development Committee. The Unified Parkinson’s Disease Rating Scale. In: Fahn S, Marsden CD, Calne DB, Goldstein M (eds) Recent developments in Parkinson’s disease, vol 2. Macmillan Health Care Information, Florham Park, pp. 153–163, 293–304 Fahn S, Elton R (1987) Members of the UPDRS Development Committee. The Unified Parkinson’s Disease Rating Scale. In: Fahn S, Marsden CD, Calne DB, Goldstein M (eds) Recent developments in Parkinson’s disease, vol 2. Macmillan Health Care Information, Florham Park, pp. 153–163, 293–304
7.
go back to reference Brown RG, Dittner A, Findley L, Wessely SC (2005) The Parkinson fatigue scale. Parkinsonism Relat Disord 11:49–55CrossRefPubMed Brown RG, Dittner A, Findley L, Wessely SC (2005) The Parkinson fatigue scale. Parkinsonism Relat Disord 11:49–55CrossRefPubMed
8.
go back to reference Krupp LB, LaRocca NG, Muir-Nash J, Steinberg AD (1989) The fatigue severity scale. Application to patients with multiple sclerosis and systemic lupus erythematosus. Arch Neurol 46:1121–1123CrossRefPubMed Krupp LB, LaRocca NG, Muir-Nash J, Steinberg AD (1989) The fatigue severity scale. Application to patients with multiple sclerosis and systemic lupus erythematosus. Arch Neurol 46:1121–1123CrossRefPubMed
9.
go back to reference Chaudhuri KR, Martinez-Martin P, Brown RG, Sethi K, Stocchi F, Odin P, Ondo W, Abe K, Macphee G, Macmahon D, Barone P, Rabey M, Forbes A, Breen K, Tluk S, Naidu Y, Olanow W, Williams AJ, Thomas S, Rye D, Tsuboi Y, Hand A, Schapira AH (2007) The metric properties of a novel non-motor symptoms scale for Parkinson’s disease: results from an international pilot study. Mov Disord 22(13):1901–1911CrossRefPubMed Chaudhuri KR, Martinez-Martin P, Brown RG, Sethi K, Stocchi F, Odin P, Ondo W, Abe K, Macphee G, Macmahon D, Barone P, Rabey M, Forbes A, Breen K, Tluk S, Naidu Y, Olanow W, Williams AJ, Thomas S, Rye D, Tsuboi Y, Hand A, Schapira AH (2007) The metric properties of a novel non-motor symptoms scale for Parkinson’s disease: results from an international pilot study. Mov Disord 22(13):1901–1911CrossRefPubMed
10.
go back to reference Beck AT, Steer RA, Ball R, Ranieri W (1996) Comparison of beck depression inventories-IA and -II in psychiatric outpatients. J Pers Assess 67(3):588–597CrossRefPubMed Beck AT, Steer RA, Ball R, Ranieri W (1996) Comparison of beck depression inventories-IA and -II in psychiatric outpatients. J Pers Assess 67(3):588–597CrossRefPubMed
11.
go back to reference 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 12:805–814CrossRef 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 12:805–814CrossRef
12.
go back to reference Tomlinson CL, Stowe R, Patel S, Rick C, Gray R, Clarke CE (2010) Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord 25(15):2649–2653CrossRefPubMed Tomlinson CL, Stowe R, Patel S, Rick C, Gray R, Clarke CE (2010) Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord 25(15):2649–2653CrossRefPubMed
13.
go back to reference Metta V, Logishetty K, Martinez-Martin P, Gage HM, Schartau PE, Kaluarachchi TK, Martin A, Odin P, Barone P, Stocchi F, Antonini A, Chaudhuri KR (2011) The possible clinical predictors of fatigue in Parkinson’s disease: a study of 135 patients as part of international nonmotor scale validation project. Parkinsons Dis 2011:125271PubMedCentralPubMed Metta V, Logishetty K, Martinez-Martin P, Gage HM, Schartau PE, Kaluarachchi TK, Martin A, Odin P, Barone P, Stocchi F, Antonini A, Chaudhuri KR (2011) The possible clinical predictors of fatigue in Parkinson’s disease: a study of 135 patients as part of international nonmotor scale validation project. Parkinsons Dis 2011:125271PubMedCentralPubMed
14.
go back to reference Friedman JH, Alves G, Hagell P, Marinus J, Marsh L, Martinez-Martin P, Goetz G, Poewe W, Rascol O, Sampaio C, Stebbins G, Schrag A (2010) Fatigue rating scales critique and recommendations by the Movement Disorders Society task force on rating scales for Parkinson’s disease. Mov Disord 25(7):805–822CrossRefPubMed Friedman JH, Alves G, Hagell P, Marinus J, Marsh L, Martinez-Martin P, Goetz G, Poewe W, Rascol O, Sampaio C, Stebbins G, Schrag A (2010) Fatigue rating scales critique and recommendations by the Movement Disorders Society task force on rating scales for Parkinson’s disease. Mov Disord 25(7):805–822CrossRefPubMed
15.
16.
go back to reference Herlofson K, Larsen JP (2003) The influence of fatigue on health-related quality of life in patients with Parkinson’s disease. Acta Neurol Scand 107:1–6CrossRefPubMed Herlofson K, Larsen JP (2003) The influence of fatigue on health-related quality of life in patients with Parkinson’s disease. Acta Neurol Scand 107:1–6CrossRefPubMed
17.
go back to reference Shulman LM, Taback RL, Bean J et al (2001) Comorbidity of the nonmotor symptoms of Parkinson’s disease. Mov Disord 16:507–510CrossRefPubMed Shulman LM, Taback RL, Bean J et al (2001) Comorbidity of the nonmotor symptoms of Parkinson’s disease. Mov Disord 16:507–510CrossRefPubMed
18.
go back to reference Alves G, Wentzel-Larsen T, Larsen JP (2004) Is fatigue an independent and persistent symptom in patients with Parkinson disease? Neurology 63:1908–1911CrossRefPubMed Alves G, Wentzel-Larsen T, Larsen JP (2004) Is fatigue an independent and persistent symptom in patients with Parkinson disease? Neurology 63:1908–1911CrossRefPubMed
19.
go back to reference Schifitto G, Friedman JH, Oakes D, Shulman L, Comella CL, Marek K, Parkinson Study Group ELLDOP A Investigator et al (2008) Fatigue in levodopa-naive subjects with Parkinson disease. Neurology 71:481–485PubMedCentralCrossRefPubMed Schifitto G, Friedman JH, Oakes D, Shulman L, Comella CL, Marek K, Parkinson Study Group ELLDOP A Investigator et al (2008) Fatigue in levodopa-naive subjects with Parkinson disease. Neurology 71:481–485PubMedCentralCrossRefPubMed
20.
go back to reference Lou JS, Kearns G, Oken B, Sexton G, Nutt J (2001) Exacerbated physical fatigue and mental fatigue in Parkinson’s disease. Mov Disord 16:190–196CrossRefPubMed Lou JS, Kearns G, Oken B, Sexton G, Nutt J (2001) Exacerbated physical fatigue and mental fatigue in Parkinson’s disease. Mov Disord 16:190–196CrossRefPubMed
21.
go back to reference Friedman JH, Brown RG, Comella C, Garber CE, Krupp LB, Lou JS et al (2007) Working Group on Fatigue in Parkinson’s Disease. Fatigue in Parkinson’s disease: a review. Mov Disord 22:297–308CrossRefPubMed Friedman JH, Brown RG, Comella C, Garber CE, Krupp LB, Lou JS et al (2007) Working Group on Fatigue in Parkinson’s Disease. Fatigue in Parkinson’s disease: a review. Mov Disord 22:297–308CrossRefPubMed
22.
go back to reference Freal JE, Draft GH, Coryell JK (1984) Symptomatic fatigue in multiple sclerosis. Arch Phys Med Rehabil 65:135–138PubMed Freal JE, Draft GH, Coryell JK (1984) Symptomatic fatigue in multiple sclerosis. Arch Phys Med Rehabil 65:135–138PubMed
24.
go back to reference Krupp LB, LaRocca NG, Muir J, Steinberg AD (1990) A study of fatigue in systemic lupus erythematosus. J Rheumatol 17(11):1450–1452PubMed Krupp LB, LaRocca NG, Muir J, Steinberg AD (1990) A study of fatigue in systemic lupus erythematosus. J Rheumatol 17(11):1450–1452PubMed
25.
go back to reference Irvine DM, Vincent L, Bubela N, Thompson L, Graydon J (1991) A critical appraisal of the research literature investigating fatigue in the individual with cancer. Cancer Nurs 14(4):188–199CrossRefPubMed Irvine DM, Vincent L, Bubela N, Thompson L, Graydon J (1991) A critical appraisal of the research literature investigating fatigue in the individual with cancer. Cancer Nurs 14(4):188–199CrossRefPubMed
26.
go back to reference Irvine D, Vincent L, Graydon JE, Bubela N, Thompson L (1994) The prevalence and correlates of fatigue in patients receiving treatment with chemotherapy and radiotherapy. A comparison with the fatigue experienced by healthy individuals. Cancer Nurs 17:367–378CrossRefPubMed Irvine D, Vincent L, Graydon JE, Bubela N, Thompson L (1994) The prevalence and correlates of fatigue in patients receiving treatment with chemotherapy and radiotherapy. A comparison with the fatigue experienced by healthy individuals. Cancer Nurs 17:367–378CrossRefPubMed
27.
go back to reference Hagell P, Brundin L (2009) Towards an understanding of fatigue in Parkinson disease. J Neurol Neurosurg Psychiatry 80(5):489–492CrossRefPubMed Hagell P, Brundin L (2009) Towards an understanding of fatigue in Parkinson disease. J Neurol Neurosurg Psychiatry 80(5):489–492CrossRefPubMed
28.
go back to reference 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):33–39CrossRefPubMed 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):33–39CrossRefPubMed
29.
go back to reference Martinez-Martin P, Falup PC, Odin P, van Hilten JJ, Antonini A, Rojo-Abuin JM, Borges V, Trenkwalder C, Aarsland D, Brooks DJ, Ray CK (2012) Gender-related differences in the burden of non-motor symptoms in Parkinson’s disease. J Neurol 259(8):1639–1647CrossRefPubMed Martinez-Martin P, Falup PC, Odin P, van Hilten JJ, Antonini A, Rojo-Abuin JM, Borges V, Trenkwalder C, Aarsland D, Brooks DJ, Ray CK (2012) Gender-related differences in the burden of non-motor symptoms in Parkinson’s disease. J Neurol 259(8):1639–1647CrossRefPubMed
30.
go back to reference van Hilten JJ, Hoogland G, van der Velde EA, Middelkoop HA, Kerkhof GA, Roos RA (1993) Diurnal effects of motor activity and fatigue in Parkinson’s disease. J Neurol Neurosurg 56(8):874–877CrossRef van Hilten JJ, Hoogland G, van der Velde EA, Middelkoop HA, Kerkhof GA, Roos RA (1993) Diurnal effects of motor activity and fatigue in Parkinson’s disease. J Neurol Neurosurg 56(8):874–877CrossRef
31.
go back to reference Chou KL, Persad CC, Patil PG (2012) Change in fatigue after bilateral subthalamic nucleus deep brain stimulation for Parkinson’s disease. Parkinsonism Relat Disord 18(5):510–513CrossRefPubMed Chou KL, Persad CC, Patil PG (2012) Change in fatigue after bilateral subthalamic nucleus deep brain stimulation for Parkinson’s disease. Parkinsonism Relat Disord 18(5):510–513CrossRefPubMed
32.
go back to reference Karlsen K, Larsen JP, Tandberg E, Jørgensen K (1999) Fatigue in patients with Parkinson’s disease. Mov Disord 14:237–241CrossRefPubMed Karlsen K, Larsen JP, Tandberg E, Jørgensen K (1999) Fatigue in patients with Parkinson’s disease. Mov Disord 14:237–241CrossRefPubMed
33.
go back to reference Fabbrini G, Latorre A, Suppa A, Bloise M, Frontoni M, Berardelli A (2013) Fatigue in Parkinson’s disease: motor or non-motor symptom? Parkinsonism Relat Disord 19(2):148–152CrossRefPubMed Fabbrini G, Latorre A, Suppa A, Bloise M, Frontoni M, Berardelli A (2013) Fatigue in Parkinson’s disease: motor or non-motor symptom? Parkinsonism Relat Disord 19(2):148–152CrossRefPubMed
34.
go back to reference Lou JS, Kearns G, Benice T, Oken B, Sexton G, Nutt J (2003) Levodopa improves physical fatigue in Parkinson’s disease: a double-blind, placebo-controlled, crossover study. Mov Disord 18(10):1108–1114CrossRefPubMed Lou JS, Kearns G, Benice T, Oken B, Sexton G, Nutt J (2003) Levodopa improves physical fatigue in Parkinson’s disease: a double-blind, placebo-controlled, crossover study. Mov Disord 18(10):1108–1114CrossRefPubMed
35.
go back to reference Dooneief G, Mirabello E, Bell K, Marder K, Stern Y, Mayeux R (1992) An estimate of the incidence of depression in idiopathic Parkinson’s disease. Arch Neurol 49:305–307CrossRefPubMed Dooneief G, Mirabello E, Bell K, Marder K, Stern Y, Mayeux R (1992) An estimate of the incidence of depression in idiopathic Parkinson’s disease. Arch Neurol 49:305–307CrossRefPubMed
36.
go back to reference Marsh L, McDonald WM, Cummings J, Ravina B (2006) Provisional diagnostic criteria for depression in Parkinson’s Disease: report of an NINDS/NIMH Work Group. Mov Disord 21:148–158CrossRefPubMed Marsh L, McDonald WM, Cummings J, Ravina B (2006) Provisional diagnostic criteria for depression in Parkinson’s Disease: report of an NINDS/NIMH Work Group. Mov Disord 21:148–158CrossRefPubMed
37.
go back to reference Starkstein SE, Mayberg HS, Preziosi TJ, Andrezejewski P, Leiguarda R, Robinson RG (1992) Reliability, validity, and clinical correlates of apathy in Parkinson’s disease. J Neuropsychiatry Clin Neurosci 4(2):134–139CrossRefPubMed Starkstein SE, Mayberg HS, Preziosi TJ, Andrezejewski P, Leiguarda R, Robinson RG (1992) Reliability, validity, and clinical correlates of apathy in Parkinson’s disease. J Neuropsychiatry Clin Neurosci 4(2):134–139CrossRefPubMed
38.
go back to reference American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders, 5th edn. American Psychiatric Publishing, Arlington American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders, 5th edn. American Psychiatric Publishing, Arlington
39.
go back to reference Havlikova E, Rosenberger J, Nagyova I, Middel B, Dubayova T, Gdovinova Z et al (2008) Clinical and psychosocial factors associated with fatigue in patients with Parkinson’s disease. Parkinsonism Relat Disord 14(3):187–192CrossRefPubMed Havlikova E, Rosenberger J, Nagyova I, Middel B, Dubayova T, Gdovinova Z et al (2008) Clinical and psychosocial factors associated with fatigue in patients with Parkinson’s disease. Parkinsonism Relat Disord 14(3):187–192CrossRefPubMed
40.
go back to reference Valko PO, Waldvogel D, Weller M, Bassetti CL, Held U, Baumann CR (2010) Fatigue and excessive daytime sleepiness in idiopathic Parkinson’s disease differently correlate with motor symptoms, depression and dopaminergic treatment. Eur J Neurol 17(12):1428–1436CrossRefPubMed Valko PO, Waldvogel D, Weller M, Bassetti CL, Held U, Baumann CR (2010) Fatigue and excessive daytime sleepiness in idiopathic Parkinson’s disease differently correlate with motor symptoms, depression and dopaminergic treatment. Eur J Neurol 17(12):1428–1436CrossRefPubMed
41.
go back to reference Okuma Y, Kamei S, Morita A et al (2009) Fatigue in Japanese patients with Parkinson’s disease: a study using Parkinson fatigue scale. Mov Disord 24:1977–1983CrossRefPubMed Okuma Y, Kamei S, Morita A et al (2009) Fatigue in Japanese patients with Parkinson’s disease: a study using Parkinson fatigue scale. Mov Disord 24:1977–1983CrossRefPubMed
Metadata
Title
Association between fatigue and other motor and non-motor symptoms in Parkinson’s disease patients
Authors
Paolo Solla
Antonino Cannas
Cesare Salvatore Mulas
Silvia Perra
Andrea Corona
Pier Paolo Bassareo
Francesco Marrosu
Publication date
01-02-2014
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 2/2014
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-013-7207-5

Other articles of this Issue 2/2014

Journal of Neurology 2/2014 Go to the issue