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Clinical determinants of primary and secondary fatigue in patients with Parkinson’s disease

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Abstract

Clinical and psychosocial factors associated separately with primary and secondary fatigue in Parkinson’s disease (PD) patients have not been thoroughly studied before. The aim of our study was to assess factors associated with different fatigue domains in groups with primary and secondary fatigue in PD separately. We divided 165 non-demented PD patients according to the absence/presence of depression, anxiety and excessive somnolence into groups with primary fatigue (N = 63) and with secondary fatigue (N = 102). Fatigue domains examined using the multidimensional fatigue inventory were associated through multiple linear regression analyses for each group separately with sociodemographic data, disease duration, functional status as assessed by the Unified Parkinson’s Disease Rating Scale, treatment, depression, anxiety, excessive somnolence and sleep quality. Out of the assessed non-motor symptoms, fatigue was the most frequent (77.6 %). The prevalence of fatigue in the secondary fatigue group was significantly higher than in the primary fatigue group. Both fatigue groups differed significantly in factors associated with different fatigue domains. Functional status or other disease-related factors were not associated with primary fatigue. In the secondary fatigue group, we found associations between some fatigue domains and functional status, older age, male gender and higher anxiety scores. To our knowledge, this is the first study to separately describe clinical determinants and psychosocial factors associated with different fatigue domains in primary and secondary fatigue in PD, underlining the importance of distinguishing primary and secondary fatigue in future PD studies and clinical practice.

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References

  1. Friedman JH, Abrantes A, Sweet LH (2011) Fatigue in Parkinson’s disease. Expert Opin Pharmacother 13:1999–2007

    Article  Google Scholar 

  2. Barone P, Antonini A, Colosimo C et al (2009) The PRIAMO study: a multicenter assessment of non-motor symptoms and their impact on quality of life in Parkinson’s disease. Mov Disord 24:1641–1649

    Article  PubMed  Google Scholar 

  3. Havlikova E, Rosenberger J, Nagyova J, Middel B, Dubayova T, Gdovinova Z, van Dijk JP, Groothoff JW (2008) Impact of fatigue on quality of life in patients with Parkinson’s disease. Eur J Neurol 15:475–480

    Article  PubMed  CAS  Google Scholar 

  4. Gomez-Esteban JC, Tijero B, Somme J, Ciordia R, Berganzo K, Roucu I, Bustos JL, Valle MA, Lezcano E, Zarranz JJ (2011) Impact of psychiatric symptoms and sleep disorders on the quality of life of patients with Parkinson’s disease. J Neurol 258:494–499

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  6. Trail M, Peterson NJ, Nelson N, Lai EC (2012) An exploratory study of activity in veterans with Parkinson’s disease. J Neurol 259:1686–1693

    Article  PubMed  CAS  Google Scholar 

  7. Nisenzon AN, Robinson ME, Bowers D, Banou E, Malaty I, Okun MS (2011) Measurement of patient-centered outcomes in Parkinson’s disease: what do patients really want from their treatment? Parkinsonism Relat Disord 2:89–94

    Article  Google Scholar 

  8. van Hilten JJ, Weggeman M, van der Velde EA, Kerkhof GA, van Dijk JG, Roos RA (1993) Sleep, excessive daytime sleepiness and fatigue in Parkinson’s disease. J Neural Transm Park Dis Dement Sect 5:235–244

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  10. Brown RG, Dittner A, Findley L, Wessely SC (2005) The Parkinson fatigue scale. Parkinsonism Relat Disord 11:49–55

    Article  PubMed  CAS  Google Scholar 

  11. Havlikova E, Rosenberger J, Nagyova I, Middel B, Dubayova T, Gdovinova Z, Groothoff JW, van Dijk JP (2008) Clinical and psychosocial factors associated with fatigue in patients with Parkinson’s disease. Parkinsonism Relat Disord 14:187–192

    Article  PubMed  Google Scholar 

  12. Hagell P, Brundin L (2009) Towards an understanding of fatigue in Parkinson disease. J Neurol Neurosurg Psychiatry 80:489–492

    Article  PubMed  CAS  Google Scholar 

  13. Karlsen K, Larsen JP, Tandberg E, Jorgensen K (1999) Fatigue in patients with Parkinson’s disease. Mov Disord 14:237–241

    Article  PubMed  CAS  Google Scholar 

  14. Lou JS, Kearns G, Oken B, Sexton G, Nutt J (2001) Exacerbated physical fatigue and mental fatigue in Parkinson’s disease. Mov Disord 16:190–196

    Article  PubMed  CAS  Google Scholar 

  15. Schifitto G, Friedman JH, Oakes D, Schulman L, Comella CL, Marek K, Fahn S (2008) Fatigue in levodopa-naive subjects with Parkinson disease. Neurology 71:481–485

    Article  PubMed  CAS  Google Scholar 

  16. Alves G, Wentzel-Larsen T, Larsen JP (2004) Is fatigue an independent and persistent symptom in patients with Parkinson’s disease? Neurology 63:1908–1911

    Article  PubMed  CAS  Google Scholar 

  17. 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 17:1428–1436

    Article  PubMed  CAS  Google Scholar 

  18. PVA (1998) Fatigue and multiple sclerosis: evidence-based management strategies for fatigue in multiple sclerosis. Paralyzed Veterans Association of America, Washington, DC

    Google Scholar 

  19. 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 

  20. Pavese N, Metta V, Bose SK, Chaudhuri KR, Brooks DJ (2010) Fatigue in Parkinson’s disease is linked to striatal and limbic serotonergic dysfunction. Brain 133:3434–3443

    Article  PubMed  Google Scholar 

  21. 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 55:181–184

    Article  PubMed  CAS  Google Scholar 

  22. Folstein MF, Folstein SE, McHugh PR (1975) Mini-mental state: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198

    Article  PubMed  CAS  Google Scholar 

  23. Friedman JH, Alves G, Hagell P et al (2010) Fatigue rating scales critique and recommendations by the movement disorders society task force on rating scales for Parkinson’s disease. Mov Disord 7:805–822

    Article  Google Scholar 

  24. Schrag A, Barone P, Brown RG et al (2007) Depression rating scales in Parkinson’s disease: critique and recommendations. Mov Disord 8:1077–1092

    Article  Google Scholar 

  25. Leentjens AFG, Dujardin K, Marsh L et al (2008) Anxiety rating scales in Parkinson’s disease: critique and recommendations. Mov Disord 14:2015–2025

    Article  Google Scholar 

  26. Hoegl B, Arnulf I, Comella C et al (2010) Scales to assess sleep impairment in Parkinson’s disease: critique and recommendations. Mov Disord 16:2704–2716

    Article  Google Scholar 

  27. Fahn S, Elton RL, Members of the UPDRS Development Committee (1987) Unified Parkinson’s disease rating scale. In: Fahn S, Marsden CD, Calne DB, Lieberman A (eds) Recent developments in Parkinson’s disease, vol 2. MacMillan Healthcare Information, Florham Park, pp 153–163

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  29. 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 25:2649–2653

    Article  PubMed  Google Scholar 

  30. Beck AT, Steer RA, Ball R, Ranieri W (1996) Comparison of Beck Depression Inventories -IA and -II in psychiatric outpatients. J Pers Assess 3:588–597

    Article  Google Scholar 

  31. Zigmond AS, Snaith RP (1983) The hospital anxiety and depression scale. Acta Psychiatr Scand 67:361–370

    Article  PubMed  CAS  Google Scholar 

  32. Johns MW (1991) A new method for measuring daytime sleepiness: the Epworth sleepiness scale. Sleep 14:540–545

    PubMed  CAS  Google Scholar 

  33. Buysse DJ, Reynolds CF 3rd, Monk TH, Berman SR, Kupfer DJ (1989) The Pittsburgh sleep quality index: a new instrument for psychiatric practice and research. Psychiatry Res 28:193–213

    Article  PubMed  CAS  Google Scholar 

  34. Smets EMA, Grassen B, Bonke B, De Haes JCJM (1995) The multidimensional fatigue inventory (MFI) psychometric qualities of an instrument to assess fatigue. J Psychosom Res 39:315–325

    Article  PubMed  CAS  Google Scholar 

  35. Elbers RG, van Wegen EEH, Verhoef J, Kwakkel G (2012) Reliability and structural validity of the multidimensional fatigue inventory (MFI) in patients with idiopathic Parkinson’s disease. Parkinsonism Relat Disord 18:532–536

    Article  PubMed  Google Scholar 

  36. Reeves WC, Wagner D, Nisenbaum R et al (2005) Chronic fatigue syndrome—a clinically empirical approach to its definition and study. BMC Med 3:19

    Article  PubMed  Google Scholar 

  37. Avlund K (2010) Fatigue in older adults: an early indicator of the aging process? Aging Clin Exp Res 2:100–115

    Google Scholar 

  38. Herlofson K, Ongre SO, Enger LK, Tysnes OB, Larsen JP (2012) Fatigue in early Parkinson’s disease. Minor inconvenience or major distress? Eur J Neurol 19:963–968

    Article  PubMed  CAS  Google Scholar 

  39. Martinez-Martin P, Pecurariu CF, Odin P, van Hilten JJ, Antonini A, Rojo-Abuin JM, Borges V, Trenkwalder C, Aarsland D, Brooks J, Chaudhuri KR (2012) Gender-related differences in the burden of non-motor symptoms in Parkinson’s disease. J Neurol 259:1639–1647

    Article  PubMed  Google Scholar 

  40. Abe K, Takanashi M, Yanagihara T, Sakoda S (2001) Pergolide mesilate may improve fatigue in patients with Parkinson’s disease. Behav Neurol 13:117–121

    Article  PubMed  Google Scholar 

  41. 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 18:1108–1114

    Article  PubMed  Google Scholar 

  42. Hauser RA, Nausieda PA, Surmann E, Moran K, Barone P (2012) Rotigotine transdermal patch improved neuropsychiatric features (apathy, anhedonia, anxiety, and depression) and fatigue in patients with Parkinson’s disease: Post hoc analysis of five double-blind placebo-controlled studies. Mov Disord 27(suppl.1):S271–S272

    Google Scholar 

  43. 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 

  44. Mendonca D, Menezes K, Jog MS (2007) Methylphenidate improves fatigue scores in Parkinson’s disease: a randomized controlled trial. Mov Disord 22:2070–2076

    Article  PubMed  Google Scholar 

  45. Zesiewicz TA, Sullivan KL, Arnulf I et al (2010) Practice Parameter: treatment of non-motor symptoms of Parkinson disease: report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology 74:924–931

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by the Slovak Research and Development Agency under contract no. APVV-20-038305 (20 %) and APVV-0220-10 (60 %). Furthermore, this work was partially supported by the Agency of the Slovak Ministry of the Education, Science, Research and Sport of the Slovak Republic for the Structural Funds of the EU under project no. ITMS: 26220120058 (20 %).

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The authors declare that they have no conflict of interest.

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This study was performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki.

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Correspondence to Matej Skorvanek.

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Skorvanek, M., Nagyova, I., Rosenberger, J. et al. Clinical determinants of primary and secondary fatigue in patients with Parkinson’s disease. J Neurol 260, 1554–1561 (2013). https://doi.org/10.1007/s00415-012-6828-4

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  • DOI: https://doi.org/10.1007/s00415-012-6828-4

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