Journal of Neurology

, Volume 256, Issue 10, pp 1655–1662 | Cite as

How do cognitive and axial motor signs correlate in Parkinson’s disease? A 6-year prospective study

  • Miguel Fernandes Gago
  • M. C. Garrett
  • M. R. Fonseca
  • M. J. Rosas
  • M. F. Simões
  • S. Vieira
  • F. Botelho
Original Communication

Abstract

Impairment of Parkinson’s disease (PD) axial motor signs (AMS) has been described as a risk factor for dementia. Executive dysfunction is an important feature in recently proposed clinical diagnostic criteria for PD dementia. To clarify the relationship between AMS progression and executive cognitive performance, we conducted a 6-year prospective study in PD patients without AMS impairment at baseline. A hospital-based cohort of PD patients (n = 24) without dementia, in the initial motor stage (Hoehn–Yahr ≤ 2), and matched controls (n = 20) were followed prospectively over a 6-year period. Neuropsychological tests were performed in both groups, and motor function (including AMS: speech, gait, postural instability) was evaluated in the PD group. The PD group had a significantly higher decline in neuropsychological test scores than did the controls. Most of the neuropsychological and motor decline occurred in the last 4 years. In UPDRS III, progression of AMS and especially speech were the most important motor variables related to dementia. There was a correlation between speech impairment progression and declines in MMSE (r = −0.598, p = 0.002), Clock Drawing (r = −0.671, p < 0.001), Semantic Verbal Fluency (r = −0.435, p = 0.034), Alternating Sequences (r = 0.497, p = 0.014), and Raven’s Coloured Progressive Matrices (r = −0.735, p < 0.001). PD patients with higher speech impairment progression showed more rapid declines in some neuropsychological tests. Further studies are needed to clarify the different roles of speech, gait and postural instability on the initial phases of cognitive dysfunction.

Keywords

Parkinson’s disease Dementia Axial motor signs Speech Executive dysfunction Neuropsychology 

References

  1. 1.
    Aarsland D, Andersen K, Larsen JP, Lolk A, Nielsen H, Kragh-Sorensen P (2001) Risk of dementia in Parkinson’s disease: a community-based, prospective study. Neurology 56:730–736PubMedGoogle Scholar
  2. 2.
    Aarsland D, Andersen K, Larsen JP, Perry R, Wentzel-Larsen T, Lolk A, Kragh-Sorensen P (2004) The rate of cognitive decline in Parkinson disease. Arch Neurol 61:1906–1911. doi: 10.1001/archneur.61.12.1906 PubMedCrossRefGoogle Scholar
  3. 3.
    Alves G, Larsen JP, Emre M, Wentzel-Larsen T, Aarsland D (2006) Changes in motor subtype and risk for incident dementia in Parkinson’s disease. Mov Disord 21:1123–1130. doi: 10.1002/mds.20897 PubMedCrossRefGoogle Scholar
  4. 4.
    APA (2000) Diagnostic and statistical manual of mental disorders, 4th edn. American Psychiatric Association, Washington (text revision)Google Scholar
  5. 5.
    Bonnet AM, Loria Y, Saint-Hilaire MH, Lhermitte F, Agid Y (1987) Does long-term aggravation of Parkinson’s disease result from nondopaminergic lesions? Neurology 37:1539–1542PubMedGoogle Scholar
  6. 6.
    Braak H, Rub U, Jansen Steur EN, Del Tredici K, de Vos RA (2005) Cognitive status correlates with neuropathologic stage in Parkinson disease. Neurology 64:1404–1410PubMedGoogle Scholar
  7. 7.
    Brink TL, Yesavage JA, Lum O, Heersema P, Adey MB, Rose TL (1982) Screening tests for geriatric depression. Clin Gerontol 1:37–44. doi: 10.1300/J018v01n01_06 CrossRefGoogle Scholar
  8. 8.
    Brusa L, Tiraboschi P, Koch G, Peppe A, Pierantozzi M, Ruggieri S, Stanzione P (2005) Pergolide effect on cognitive functions in early mild Parkinson’s disease. J Neural Transm 112:231–237. doi: 10.1007/s00702-004-0193-0 PubMedCrossRefGoogle Scholar
  9. 9.
    Burn DJ, Rowan EN, Allan LM, Molloy S, O’Brien JT, McKeith IG (2006) Motor subtype and cognitive decline in Parkinson’s disease, Parkinson’s disease with dementia, and dementia with Lewy bodies. J Neurol Neurosurg Psychiatry 77:585–589. doi: 10.1136/jnnp.2005.081711 PubMedCrossRefGoogle Scholar
  10. 10.
    Carlson MC, Xue QL, Zhou J, Fried LP (2009) Executive decline and dysfunction precedes declines in memory: the Women’s Health and Aging Study II. J Gerontol 64:110–117Google Scholar
  11. 11.
    Dubois B, Pilon B, Lhermitte F, Agid Y (1990) Cholinergic deficiency and frontal dysfunction in Parkinson’s disease. Ann Neurol 28:117–121. doi: 10.1002/ana.410280202 PubMedCrossRefGoogle Scholar
  12. 12.
    Emre M, Aarsland D, Brown R, Burn DJ, Duyckaerts C, Mizuno Y, Broe GA, Cummings J, Dickson DW, Gauthier S, Goldman J, Goetz C, Korczyn A, Lees A, Levy R, Litvan I, McKeith I, Olanow W, Poewe W, Quinn N, Sampaio C, Tolosa E, Dubois B (2007) Clinical diagnostic criteria for dementia associated with Parkinson’s disease. Mov Disord 22:1689–1707. doi: 10.1002/mds.21507 quiz 1837PubMedCrossRefGoogle Scholar
  13. 13.
    Fahn S, Elton RL, Members of the UPDRS Development Committee (1987) Unified Parkinson’s disease rating scale. In: S Fahn, CD Marsden, Calne DB, Lieberman A (eds) Recent developments in Parkinson disease. Macmillan Health Care information, Florham Park, pp 153–163Google Scholar
  14. 14.
    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. doi: 10.1016/0022-3956(75)90026-6 PubMedCrossRefGoogle Scholar
  15. 15.
    Freedman M, Leach L, Kaplan E, Winocur G, Schulman KI, Delis DC (1994) Clock drawing: a neuropsychological analysis. Oxford University Press, New YorkGoogle Scholar
  16. 16.
    Guerreiro M, Silva AP, Botelho MA, Leitão O, Castro-Caldas A, Garcia C (1994) Translation and adaptation to Portuguese population of the mini mental state examination (MMSE). Rev Port Neurol 3(Suppl. 1):9Google Scholar
  17. 17.
    Hobson P, Meara J (2004) Risk and incidence of dementia in a cohort of older subjects with Parkinson’s disease in the United Kingdom. Mov Disord 19:1043–1049. doi: 10.1002/mds.20216 PubMedCrossRefGoogle Scholar
  18. 18.
    Hughes TA, Ross HF, Musa S, Bhattacherjee S, Nathan RN, Mindham RH, Spokes EG (2000) A 10-year study of the incidence of and factors predicting dementia in Parkinson’s disease. Neurology 54:1596–1602PubMedGoogle Scholar
  19. 19.
    Jankovic J, McDermott M, Carter J, Gauthier S, Goetz C, Golbe L, Huber S, Koller W, Olanow C, Shoulson I et al (1990) Variable expression of Parkinson’s disease: a base-line analysis of the DATATOP cohort. The Parkinson study group. Neurology 40:1529–1534PubMedGoogle Scholar
  20. 20.
    Kalbe E, Calabrese P, Kohn N, Hilker R, Riedel O, Wittchen HU, Dodel R, Otto J, Ebersbach G, Kessler J (2008) Screening for cognitive deficits in Parkinson’s disease with the Parkinson neuropsychometric dementia assessment (PANDA) instrument. Parkinsonism Relat Disord 14:93–101. doi: 10.1016/j.parkreldis.2007.06.008 PubMedCrossRefGoogle Scholar
  21. 21.
    Kompoliti K, Wang QE, Goetz CG, Leurgans S, Raman R (2000) Effects of central dopaminergic stimulation by apomorphine on speech in Parkinson’s disease. Neurology 54:458–462PubMedGoogle Scholar
  22. 22.
    Lees AJ, Smith E (1983) Cognitive deficits in the early stages of Parkinson’s disease. Brain 106(Pt 2):257–270. doi: 10.1093/brain/106.2.257 PubMedCrossRefGoogle Scholar
  23. 23.
    Levy G, Tang MX, Cote LJ, Louis ED, Alfaro B, Mejia H, Stern Y, Marder K (2000) Motor impairment in PD: relationship to incident dementia and age. Neurology 55:539–544PubMedGoogle Scholar
  24. 24.
    Lezak MD (1995) Neuropsychological Assessment. Oxford University Press, OxfordGoogle Scholar
  25. 25.
    Locascio JJ, Corkin S, Growdon JH (2003) Relation between clinical characteristics of Parkinson’s disease and cognitive decline. J Clin Exp Neuropsychol 25:94–109. doi: 10.1076/jcen.25.1.94.13624 PubMedCrossRefGoogle Scholar
  26. 26.
    Lyros E, Messinis L, Papathanasopoulos P (2008) Does motor subtype influence neurocognitive performance in Parkinson’s disease without dementia? Eur J Neurol 15:262–267. doi: 10.1111/j.1468-1331.2007.02046.x PubMedCrossRefGoogle Scholar
  27. 27.
    Mayeux R, Chen J, Mirabello E, Marder K, Bell K, Dooneief G, Cote L, Stern Y (1990) An estimate of the incidence of dementia in idiopathic Parkinson’s disease. Neurology 40:1513–1517PubMedGoogle Scholar
  28. 28.
    Molloy SA, Rowan EN, O’Brien JT, McKeith IG, Wesnes K, Burn DJ (2006) Effect of levodopa on cognitive function in Parkinson’s disease with and without dementia and dementia with Lewy bodies. J Neurol Neurosurg Psychiatry 77:1323–1328. doi: 10.1136/jnnp.2006.098079 PubMedCrossRefGoogle Scholar
  29. 29.
    Pillon B, Dubois B, Cusimano G, Bonnet AM, Lhermitte F, Agid Y (1989) Does cognitive impairment in Parkinson’s disease result from non-dopaminergic lesions? J Neurol Neurosurg Psychiatry 52:201–206. doi: 10.1136/jnnp.52.2.201 PubMedCrossRefGoogle Scholar
  30. 30.
    Raven J (2000) The Raven’s progressive matrices: change and stability over culture and time. Cogn Psychol 41:1–48. doi: 10.1006/cogp.1999.0735 PubMedCrossRefGoogle Scholar
  31. 31.
    Riecker A, Mathiak K, Wildgruber D, Erb M, Hertrich I, Grodd W, Ackermann H (2005) fMRI reveals two distinct cerebral networks subserving speech motor control. Neurology 64:700–706PubMedGoogle Scholar
  32. 32.
    Riedel O, Klotsche J, Spottke A, Deuschl G, Forstl H, Henn F, Heuser I, Oertel W, Reichmann H, Riederer P, Trenkwalder C, Dodel R, Wittchen HU (2008) Cognitive impairment in 873 patients with idiopathic Parkinson’s disease. Results from the German Study on Epidemiology of Parkinson’s Disease with Dementia (GEPAD). J Neurol 255:255–264. doi: 10.1007/s00415-008-0720-2 PubMedCrossRefGoogle Scholar
  33. 33.
    Schwab RS, England AC (1969) Projection technique for evaluating surgery in Parkinson’s disease. In: Gillingham FJ, Donaldson IML (eds) Third Symposium in Parkinson’s Disease. Livingstone, Edinburgh, pp 152–157Google Scholar
  34. 34.
    Shulman KI (2000) Clock-drawing: is it the ideal cognitive screening test? Int J Geriatr Psychiatry 15:548–561. doi: 10.1002/1099-1166(200006)15:6<548::AID-GPS242>3.0.CO;2-U PubMedCrossRefGoogle Scholar
  35. 35.
    Strub RL, Black FW (2000) The mental status examination in neurology. FA Davis Company, PhiladelphiaGoogle Scholar
  36. 36.
    Taylor JP, Rowan EN, Lett D, O’Brien JT, McKeith IG, Burn DJ (2008) Poor attentional function predicts cognitive decline in patients with non-demented Parkinson’s disease independent of motor phenotype. J Neurol Neurosurg Psychiatry 79:1318–1323. doi: 10.1136/jnnp.2008.147629 PubMedCrossRefGoogle Scholar
  37. 37.
    Verbaan D, Marinus J, Visser M, van Rooden SM, Stiggelbout AM, Middelkoop HA, van Hilten JJ (2007) Cognitive impairment in Parkinson’s disease. J Neurol Neurosurg Psychiatry 78:1182–1187. doi: 10.1136/jnnp.2006.112367 PubMedCrossRefGoogle Scholar
  38. 38.
    Wechsler D (1997) Wechsler adult intelligence scale-III. The Psychological Corporation, San AntonioGoogle Scholar
  39. 39.
    Williams-Gray CH, Foltynie T, Brayne CE, Robbins TW, Barker RA (2007) Evolution of cognitive dysfunction in an incident Parkinson’s disease cohort. Brain 130:1787–1798. doi: 10.1093/brain/awm111 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Miguel Fernandes Gago
    • 1
    • 2
  • M. C. Garrett
    • 1
  • M. R. Fonseca
    • 1
  • M. J. Rosas
    • 1
  • M. F. Simões
    • 1
  • S. Vieira
    • 1
  • F. Botelho
    • 1
  1. 1.Departments of Neurology and Neurosurgery, Faculdade de Medicina da Universidade do PortoHospital de São João E.P.EPortoPortugal
  2. 2.Alameda Prof. Hernâni MonteiroPortoPortugal

Personalised recommendations