Journal of Neurology

, Volume 252, Issue 11, pp 1345–1352 | Cite as

Longitudinal evaluation of cerebral morphological changes in Parkinson's disease with and without dementia

  • B. Ramírez–Ruiz
  • M. J. Martí
  • E. Tolosa
  • D. Bartrés–Faz
  • Ch. Summerfield
  • P. Salgado–Pineda
  • B. Gómez–Ansón
  • C. Junqué
ORIGINAL COMMUNICATION

Abstract

Objective

To investigate the pattern of brain atrophy across time in a sample of Parkinson's disease (PD) patients with and without dementia using voxelbased morphometry (VBM) analysis.

Methods

The initial sample comprised thirteen non–demented PD patients and sixteen demented patients. Longitudinal cognitive assessment and structural MRI were performed. The mean follow–up period was 25 months (SD = 5.2). From this initial group, eight PD patients with dementia (5 men and 3 women) and eleven PD patients without dementia (7 men and 4 women) were reevaluated. MRI 3D structural images were acquired and analyzed by means of the optimized VBM procedure with Statistical Parametric Mapping (SPM2).

Results

VBM analysis showed a progressive grey matter volume decrease in patients with PD without dementia in limbic, paralimbic and neocortical associative temporooccipital regions. In patients with dementia the loss mainly involved neocortical regions.

Conclusion

VBM revealed a significant loss of grey matter volume in PD patients with and without dementia with disease progression. The decrease in limbic and paralimbic regions is widespread in non–demented patients. Neocortical volume reduction is the most relevant finding in patients with dementia. This suggests that the neocortex is a substrate for dementia in Parkinson disease.

Key words

Parkinson's disease dementia MRI voxel–based morphometry longitudinal study 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Aarsland D, Tandberg E, Larsen JP, Cummings JL (1996) Frequency of dementia in Parkinson disease. Arch Neurol 53(6):538–542PubMedGoogle Scholar
  2. 2.
    Aarsland D, Andersen K, Larsen JP, Lolk A, Kragh–Sørensen P (2003) Prevalence and characteristics of dementia in Parkinson disease. An 8–year prospective study. Arch Neurol 60:387–392Google Scholar
  3. 3.
    American Psychiatric Association (2003) Manual diagnóstico y estadístico de los trastornos mentales, Cuarta edición revisada: DSM–IV–TR. Masson SA, BarcelonaGoogle Scholar
  4. 4.
    Apaydin H, Ahlskog JE, Parisi JE, Boeve BF, Dickson DW (2002) Parkinson disease neuropathology. Laterdeveloping dementia and loss of the levodopa response. Arch Neurol 59:102–112CrossRefPubMedGoogle Scholar
  5. 5.
    Braak H, Braak E, Yilmazer D, de Vos RA, Jansen EN, Bohl J, Jellinger K (1994) Amygdala pathology in Parkinson’s disease. Acta Neuropathol (Berl) 88:493–500PubMedGoogle Scholar
  6. 6.
    Braak H, Braak E (2000) Pathoanatomy of Parkinson’s disease. J Neurol 247 (Suppl 2):II/3–II/10Google Scholar
  7. 7.
    Braak H, Del Tredici K, Rüb U, de Vos RA, Jansen Steur EN, Braak E (2003) Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24:197–211CrossRefPubMedGoogle Scholar
  8. 8.
    Burn DJ (2004) Cortical Lewy body disease. J Neurol Neurosurg Psychiatry 75:175–178CrossRefPubMedGoogle Scholar
  9. 9.
    Burton EJ, McKeith IG, Burn DJ, Williams ED, O’Brien JT (2004) Cerebral atrophy in Parkinson’s disease with and without dementia: a comparison with Alzheimer’s disease, dementia with Lewy bodies and controls. Brain 127:791–800. DOI: 10.1093/brain/awh088CrossRefPubMedGoogle Scholar
  10. 10.
    Calopa M, Tolosa E, Ferrer I, Rey MJ, Cardozo A, Martí MJ, Ribalta T (2002) Cortical Lewy bodies in Parkinson’s disease with dementia. In: Tolosa E, Schulz JB, McKeith IG, Ferrer I (eds) Neurodegenerative disorders associated with α–Synuclein pathology. Medicina stm Editores, SL, Barcelona, pp 127–134Google Scholar
  11. 11.
    Camicioli R, Moore MM, Kinney A, Corbridge E, Glassberg K, Kaye JA (2003) Parkinson's disease is associated with hippocampal atrophy. Mov Disord 18(7):784–790CrossRefPubMedGoogle Scholar
  12. 12.
    Daniel SE, Lees AJ (1993) Parkinson's Disease Society Brain Bank, London: overview and research. J Neural Transm Suppl 39:165–172PubMedGoogle Scholar
  13. 13.
    de la Monte SM, Wells SE, Hedley– Whyte ET, Growdon JH (1989) Neuropathological distinction between Parkinson’s dementia and Parkinson’s plus Alzheimer's disease. Ann Neurol 26:309–320CrossRefPubMedGoogle Scholar
  14. 14.
    De Vos RA, Jansen EN, Stam FC, Ravid R, Swaab DF (1995) 'Lewy body disease': clinico–pathological correlations in 18 consecutive cases of Parkinson's disease with and without dementia. Clin Neurol Neurosurg 97:13–22PubMedGoogle Scholar
  15. 15.
    Diederich NJ, Goetz CG, Stebbins GT (2005) Repeated visual hallucinations in Parkinson's disease as disturbed external/internal perceptions: focused review and a new integrative model. Mov Disord 20(2):130–140. DOI: 10.1002/mds 0.20308PubMedGoogle Scholar
  16. 16.
    Dubois B, Pillon B (1997) Cognitive deficits in Parkinson's disease. J Neurol 244:2–8Google Scholar
  17. 17.
    Factor SA, Feustel PJ, Friedman JH, Comella CL, Goetz CG, Kurlan R, Parsa M, Pfeiffer R and the Parkinson Study Group (2003) Longitudinal outcome of Parkinson's disease patients with psychosis. Neurology 60:1756–1761PubMedGoogle Scholar
  18. 18.
    Fahn S, Elton RL and members of the UPDRS development committee (1987) Unified Idiopathic Parkinson's disease Rating Scale. In: Fahn S, Marsden CD, Calne D, Goldstein M (eds) Recent developments in Parkinson's disease (Vol. 2). Florham Park, New Jersey, Mac Millan Healthcare Information, USA, pp 153–164Google Scholar
  19. 19.
    Fearnley JM, Lees AJ (1991) Ageing and Parkinson's disease: substantia nigra regional selectivity. Brain 114:2283–2301PubMedGoogle Scholar
  20. 20.
    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(3):189–198CrossRefPubMedGoogle Scholar
  21. 21.
    Goetz CG, Leurgans S, Pappert EJ, Raman R, Stemer AB (2001) Prospective longitudinal assessment of hallucinations in Parkinson's disease. Neurology 57:2078–2082PubMedGoogle Scholar
  22. 22.
    Goldman WP, Baty JD, Buckles VD, Sahrmann S, Morris JC (1998) Cognitive and motor functioning in Parkinson disease. Arch Neurol 55:674–680CrossRefPubMedGoogle Scholar
  23. 23.
    Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, Frackowiak RS (2001) A voxel–based morphometric study of ageing in 465 normal adult human brains. Neuroimage 14:21–36. DOI: 10.1006/nimg 0.2001.0786PubMedGoogle Scholar
  24. 24.
    Hamilton M (1960) A rating scale for depression. J Neurol Neurosurg Psychiatry 23:56–62PubMedGoogle Scholar
  25. 25.
    Harding AJ, Broe GA, Halliday GM (2002) Visual hallucinations in Lewy body disease relate to Lewy bodies in the temporal lobe. Brain 125:391–403PubMedGoogle Scholar
  26. 26.
    Hu MT, White SJ, Chaudhuri KR, Morris RG, Bydder GM, Brooks DJ (2001) Correlating rates of cerebral atrophy in Parkinson's disease with measures of cognitive decline. J Neural Transm 108:571–580CrossRefPubMedGoogle Scholar
  27. 27.
    Hurtig HI, Trojanowski JQ, Galvin J, Ewbank D, Schmidt ML, Lee VM, Clark CM, Glosser G, Stern MB, Gollomp SM, Arnold SE (2000) Alpha–synuclein cortical Lewy bodies correlate with dementia in Parkinson's disease. Neurology 54(10):1916–1921PubMedGoogle Scholar
  28. 28.
    Jankovic J, McDermott M, Carter J, Gauthier S, Goetz C, Golbe L, Huber S, Koller W, Olanow C, Shoulson I, Stern M, Tanner C, Weiner W and the Parkinson Study Group (1990) Variable expression of Parkinson's disease: A base–line analysis of the DATATOP cohort. Neurology 40:1529–1534PubMedGoogle Scholar
  29. 29.
    Kaasinen V, Aalto S, Någren K, Hietala J, Sonninen P, Rinne JO (2003) Extrastriatal dopamine D2 receptors in Parkinson's disease: a longitudinal study. J Neural Transm 110:591–601. DOI: 10.1007/s00702–003–0816–xCrossRefPubMedGoogle Scholar
  30. 30.
    Kawabata K, Tachibana H, Sugita M (1991) Cerebral blood flow and dementia in Parkinson's disease. J Geriatr Psychiatry Neurol 4(4):194–203PubMedGoogle Scholar
  31. 31.
    Kikuchi A, Takeda A, Kimpara T, Nakagawa M, Kawashima R, Sugiura M, Kinomura S, Fukuda H, Chida K, Okita N, Takase S, Itoyama Y (2001) Hypoperfusion in the supplementary motor area, dorsolateral prefrontal cortex and insular cortex in Parkinson's disease. J Neurol Sci 193:29–36CrossRefPubMedGoogle Scholar
  32. 32.
    Levy G, Jacobs DM, Tang M, Côté LJ, Louis ED, Alfaro B, Mejia H, Stern Y, Marder K (2002a) Memory and executive function impairment predict dementia in Parkinson's disease. Mov Disord 17(6):1221–1226. DOI: 10.1002/mds 0.10280Google Scholar
  33. 33.
    Levy G, Schupf N, Tang M, Cote LJ, Louis ED, Mejia H, Stern Y, Marder K (2002b) Combined effect of age and severity on the risk of dementia in Parkinson's disease. Ann Neurol 51:722–729. DOI: 10.1002/ana 0.10219Google Scholar
  34. 34.
    Lezak MD, Howieson DB, Loring DW, Hannay HJ, Fischer JS (2004) Neuropsychological assessment. 4th ed. Oxford University Press Inc., New YorkGoogle Scholar
  35. 35.
    Marttila RJ, Rinne UK (1976) Epidemiology of Parkinson's disease in Finland. Acta Neurol Scand 53(2):81–102PubMedGoogle Scholar
  36. 36.
    Matsuda H, Kitayama N, Ohnishi T, Asada T, Nakano S, Sakamoto S, Imabayashi E, Katoh A (2002) Longitudinal evaluation of both morphologic and functional changes in the same individuals with Alzheimer's disease. J Nucl Med 43:304–311PubMedGoogle Scholar
  37. 37.
    Mattila PM, Rinne JO, Helenius H, Dickson DW, Röyttä M (2000) Alphasynuclein– immunoreactive cortical Lewy bodies are associated with cognitive impairment in Parkinson's disease. Acta Neuropathol (Berl)100:285–290CrossRefPubMedGoogle Scholar
  38. 38.
    Mayeux R, Denaro J, Hemenegildo N, Marder K, Tang MX, Cote LJ, Stern Y (1992) A population–based investigation of Parkinson's disease with and without dementia. Relationship to age and gender. Arch Neurol 49(5):492–497PubMedGoogle Scholar
  39. 39.
    Nurmi E, Bergman J, Eskola O, Solin O, Vahlberg T, Sonninen P, Rinne JO (2003) Progression of dopaminergic hypofunction in striatal subregions in Parkinson's Disease using [18F]CFT PET. Synapse 48:109–115. DOI: 10.1002/syn 0.10192CrossRefPubMedGoogle Scholar
  40. 40.
    Perry EK, Curtis M, Dick DJ, Candy JM, Atack JR, Bloxham CA, Blessed G, Fairbairn A, Tomlinson BE, Perry RH (1985) Cholinergic correlates of cognitive impairment in Parkinson's disease: comparisons with Alzheimer's disease. J Neurol Neurosurg Psychiatry 48:413–421PubMedCrossRefGoogle Scholar
  41. 41.
    Resnick SM, Pham DL, Kraut MA, Zonderman AB, Davatzikos C (2003) Longitudinal magnetic resonance imaging studies of older adults: a shrinking brain. J Neurosci 23(8):3295–3301PubMedGoogle Scholar
  42. 42.
    Staffen W, Mair A, Unterrainer J, Trinka E, Ladurner G (2000) Measuring the progression of idiopathic Parkinson's disease with [123 I] β–CIT SPECT. J Neural Transm 107:543–552CrossRefPubMedGoogle Scholar
  43. 43.
    Summerfield C, Junqué C, Tolosa E, Salgado–Pineda P, Gómez–Ansón B, Martí MJ, Pastor P, Ramírez–Ruiz B, Mercader J (2005) Structural brain changes in Parkinson disease with dementia. A voxel–based morphometry study. Arch Neurol 62:281–285CrossRefPubMedGoogle Scholar
  44. 44.
    Tachibana H, Kawabata K, Tomino Y, Sugita M, Fukuchi M (1993) Brain perfusion imaging in Parkinson's disease and Alzheimer's disease demonstrated by three–dimensional surface display with 123I–iodoamphetamine. Dementia 4(6):334–341PubMedGoogle Scholar
  45. 45.
    Tisserand DJ, van Boxtel MP, Pruessner JC, Hofman P, Evans AC, Jolles J (2004) A Voxel–based morphometric study to determine differences in gray matter density associated with age and cognitive change over time. Cereb Cortex 14:966–973; DOI: 10.1093/cercor/bhh057CrossRefPubMedGoogle Scholar
  46. 46.
    Visser PJ, Verhey FR, Hofman PA, Scheltens P, Jolles J (2002) Medial temporal lobe atrophy predicts Alzheimer's disease in patients with minor cognitive impairment. J Neurol Neurosurg Psychiatry 72:491–497PubMedGoogle Scholar
  47. 47.
    Zweig RM, Cardillo JE, Cohen M, Giere S, Hedreen, JC (1993) The locus ceruleus and dementia in Parkinson's disease. Neurology 43:986–991PubMedGoogle Scholar

Copyright information

© Steinkopff-Verlag 2005

Authors and Affiliations

  • B. Ramírez–Ruiz
    • 1
    • 2
  • M. J. Martí
    • 2
    • 3
  • E. Tolosa
    • 2
    • 3
  • D. Bartrés–Faz
    • 1
    • 2
  • Ch. Summerfield
    • 1
    • 2
  • P. Salgado–Pineda
    • 1
    • 2
  • B. Gómez–Ansón
    • 2
    • 4
  • C. Junqué
    • 1
    • 2
  1. 1.Dept. of Psychiatry and Clinical PsychobiologyUniversity of BarcelonaBarcelonaSpain
  2. 2.Institut d'Investigacions BiomèdiquesAugust Pi i Sunyer (IDIBAPS)BarcelonaSpain
  3. 3.Department of Neurology, Institut Clínic de Malalties del SistemaNerviós (ICMSN), Hospital Clínic de BarcelonaBarcelonaSpain
  4. 4.Centre de Diagnòstic per la Imatge (CDI)Hospital Clínic de BarcelonaBarcelonaSpain

Personalised recommendations