Cognitive impairment in multiple system atrophy: Changing concepts

Abrahão, Agessandro; Dutra, Livia Almeida; Braga Neto, Pedro; Pedroso, José Luiz; Oliveira, Ricardo Araújo de; Barsottini, Orlando Graziani Povoas

doi:10.1590/S1980-57642011DN05040008

Abstract

Multiple system atrophy (MSA) is characterized by a variable combination of cerebellar ataxia, parkinsonism and pyramidal signs associated with autonomic failure. Classically, cognitive impairment was not considered a clinical feature of MSA and dementia was pointed out as an exclusion diagnostic criteria. Based on comprehensive neuropsychological assessment, cognitive impairment was found to be a frequent feature in MSA, and clinically-defined dementia is now reported in 14-16% of cases. This article reviews the current data on cognitive impairment in MSA along with its neuropsychological profile and pathophysiology.

Key words:
multiple system atrophy; cognitive impairment; dementia; atypical parkinsonism; neuropsychological evaluation.

Resumo

A Atrofia de Múltiplos Sistemas (AMS) é caracterizada por uma combinação variável de ataxia cerebelar, parkinsonismo e sinais piramidais, associados à disfunção autonômica. Classicamente, o comprometimento cognitivo não é considerado como manifestação clínica da AMS e a demência é apontada como um critério de exclusão para o diagnóstico. Baseado na avaliação neuropsicológica ampla, o comprometimento neuropsicológico revelou-se frequente na AMS e a presença de demência é atualmente descrita em 14-16% dos casos. Este artigo revisa os dados atuais sobre o comprometimento cognitivo na AMS, seu perfil neuropsicológico e fisiopatologia.

Palavras-chave:
atrofia de múltiplos sistemas; comprometimento cognitivo; demência; parkinsonismo atípico; avaliação neuropsicológica.

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References

Papp MI, Kahn JE, Lantos PL. Glial cytoplasmic inclusions in the CNS of patients with multiple system atrophy (striatonigral degeneration, olivopontocerebellar atrophy and Shy-Drager syndrome). J Neurol Sci 1989;94:79-100.
Wakabayashi K, Yoshimoto M, Tsuji S, Takahashi H. Alpha-synuclein immunoreactivity in glial cytoplasmic inclusions in multiple system atrophy. Neurosci Lett 1998;249:180-182.
Stefanova N, Bücke P, Duerr S, Wenning GK. Multiple system atrophy: an update. Lancet Neurol 2009;8:1172-1178.
Déjerine J, Thomas A. L'atrophie olivo-ponto-cerebelleuse. Nouv Iconog de le Salpêtrière. 1900;13:330-370.
Shy GM, Drager GA. A neurological syndrome associated with orthostatic hypotension: a clinical-pathologic study. Arch Neurol 1960;2:511-527.
Quinn N. Multiple system atrophy--the nature of the beast. J Neurol Neurosurg Psychiatry 1989;52(Suppl):78-89.
Eecken Hvd, Adams R, Bogaert LV. Striopallidal-nigral degeneration. A hitherto undescribed lesion in paralysis agitans. J Neuropathol Exp Neurol. 1960;19:159-161.
Adams RD, Vanbogaert L, Vandereecken H. Striato-Nigral Degeneration. J Neuropathol Exp Neurol 1964;23:584-608.
Graham JG, Oppenheimer DR. Orthostatic hypotension and nicotine sensitivity in a case of multiple system atrophy. J Neurol Neurosurg Psychiatry 1969;32:28-34.
Gilman S, Low PA, Quinn N, et al. Consensus statement on the diagnosis of multiple system atrophy. J Neurol Sci 1999;163:94-98.
Gilman S, Wenning GK, Low PA, et al. Second consensus statement on the diagnosis of multiple system atrophy. Neurology; 2008;71:670-676.
American-Psychiatric-Association. Diagnostic and statistical manual of mental disorders (DSM-IV-TR). 4th (text revision); 2000.
Folstein MF, Folstein SE, McHugh PR. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975; 12:189-198.
Wenning GK, Ben-Shlomo Y, Hughes A, Daniel SE, Lees A, Quinn NP. What clinical features are most useful to distinguish definite multiple system atrophy from Parkinson's disease? J Neurol Neurosurg Psychiatry 2000;68:434-440.
Brown RG, Lacomblez L, Landwehrmeyer BG, et al. Cognitive impairment in patients with multiple system atrophy and progressive supranuclear palsy. Brain 2010;133:2382-2393.
O'Sullivan SS, Massey LA, Williams DR, et al. Clinical outcomes of progressive supranuclear palsy and multiple system atrophy. Brain 2008;131.
Köllensperger M, Geser F, Ndayisaba J.P, et al. Presentation, diagnosis, and management of multiple system atrophy in Europe: final analysis of the European multiple system atrophy registry. Mov Disord; 2010;25:2604-12.
Gilman S, May SJ, Shults CW, et al. The North American Multiple System Atrophy Study Group. J Neural Transm; 2005; 112:1687-1694.
Yabe I, Soma H, Takei A, Fujiki N, Yanagihara T, Sasaki H. MSA-C is the predominant clinical phenotype of MSA in Japan: analysis of 142 patients with probable MSA. J Neurol Sci 2006;249:115-121.
Watanabe H, Saito Y, Terao S, et al. Progression and prognosis in multiple system atrophy: an analysis of 230 Japanese patients. Brain ; 2002;125:1070-1083.
Barsottini OG. Parkinsonismo atípico. In: Ferraz B, editor. Doença de Parkinson: prática clínica e terapêutica. São Paulo: Editora Atheneu; 2005.
Wenning GK, Tison F, Ben Shlomo Y, Daniel SE, Quinn NP. Multiple system atrophy: a review of 203 pathologically proven cases. Mov Disord 1997;12:133-147.
Knopp DB, Barsottini OG, Ferraz HB. Multiple system atrophy speech assessment: study of five cases. Arq Neuropsiquiatr 2002;60:619-623.
da Rocha AJ, Maia AC, Jr., da Silva CJ, et al. Pyramidal tract degeneration in multiple system atrophy: the relevance of magnetization transfer imaging. Mov Disord 2007;22:238-244.
Geser F, Seppi K, Stampfer-Kountchev M, et al. The European Multiple System Atrophy-Study Group (EMSA-SG). J Neural Transm 2005;112:1677-1686.
Sullivan EV, De La Paz R, Z ipursky RB, Pfefferbaum A. Neuropsychological deficits accompanying striatonigral degeneration. J Clin Exp Neuropsychol 1991;13:773-788.
Kitayama M, Wada-Isoe K, Irizawa Y, Nakashima K. Assessment of dementia in patients with multiple system atrophy. Eur J Neurol 2009;16:589-594.
Boeve BF, Silber MH, Saper CB, et al. Pathophysiology of REM sleep behaviour disorder and relevance to neurodegenerative disease. Brain 2007;130:2770-2788.
Kawamura K, Shimohata T, Nakayama H, Tomita M, Ozawa T, Nishizawa M. Factors influencing the cognitive function in patients with multiple system atrophy. Mov Disord 2010; 25:2891-2892.
Emre M, Aarsland D, Brown R, et al. Clinical diagnostic criteria for dementia associated with Parkinson's disease. Mov Disord 2007;22:1689-1707.
Berent S, Giordani B, Gilman S, et al. Patterns of neuropsychological performance in multiple system atrophy compared to sporadic and hereditary olivopontocerebellar atrophy. Brain Cogn 2002;50:194-206.
Kao AW, Racine CA, Quitania LC, Kramer JH, Christine CW, Miller BL. Cognitive and neuropsychiatric profile of the synucleinopathies: Parkinson disease, dementia with Lewy bodies, and multiple system atrophy. Alzheimer Dis Assoc Disord 2009;23:365-370.
Miller BL, Cummings JL. Frontal subcortical circuits. In: Miller BL, Cummings JL, editors. The human frontal lobes : functions and disorders. 2nd ed. ed. New York, N.Y. ; London: Guilford Press; 2007:25.
Desmond JE, Gabrieli JD, Wagner AD, Ginier BL, Glover GH. Lobular patterns of cerebellar activation in verbal working-memory and finger-tapping tasks as revealed by functional MRI. J Neurosci 1997;17:9675-9685.
Bellebaum C, Daum I. Cerebellar involvement in executive control. Cerebellum. 2007;6:184-92.
Grasby PM, Frith CD, Friston KJ, Bench C, Frackowiak RS, Dolan RJ. Functional mapping of brain areas implicated in auditory--verbal memory function. Brain 1993;116:1-20.
Petersen SE, Fox PT, Posner MI, Mintun M, Raichle ME. Positron emission tomographic studies of the cortical anatomy of single-word processing. Nature 1988;331(6157):585-589.
Allen G, Buxton RB, Wong EC, Courchesne E. Attentional activation of the cerebellum independent of motor involvement. Science. 1997;275(5308):1940-1943.
Bürk K, Daum I, Rüb U. Cognitive function in multiple system atrophy of the cerebellar type. Mov Disord ; 2006;21:772-6.
Kawai Y, Suenaga M, Takeda A, Ito M, Watanabe H, Tanaka F, et al. Cognitive impairments in multiple system atrophy: MSA-C vs MSA-P. Neurology 2008;70:1390-1396.
Bak TH. Cognitive bedside assessment in atypical parkinsonian syndromes. J Neurol Neurosurg Psychiatr 2005;76:420-422.

Publication Dates

Publication in this collection
Oct-Dec 2011

History

Received
03 July 2011
Accepted
02 Nov 2011

This is an open-access article distributed under the terms of the Creative Commons Attribution License

[1] Papp MI, Kahn JE, Lantos PL. Glial cytoplasmic inclusions in the CNS of patients with multiple system atrophy (striatonigral degeneration, olivopontocerebellar atrophy and Shy-Drager syndrome). J Neurol Sci 1989;94:79-100.

[2] Wakabayashi K, Yoshimoto M, Tsuji S, Takahashi H. Alpha-synuclein immunoreactivity in glial cytoplasmic inclusions in multiple system atrophy. Neurosci Lett 1998;249:180-182.

[3] Stefanova N, Bücke P, Duerr S, Wenning GK. Multiple system atrophy: an update. Lancet Neurol 2009;8:1172-1178.

[4] Déjerine J, Thomas A. L'atrophie olivo-ponto-cerebelleuse. Nouv Iconog de le Salpêtrière. 1900;13:330-370.

[5] Shy GM, Drager GA. A neurological syndrome associated with orthostatic hypotension: a clinical-pathologic study. Arch Neurol 1960;2:511-527.

[6] Quinn N. Multiple system atrophy--the nature of the beast. J Neurol Neurosurg Psychiatry 1989;52(Suppl):78-89.

[7] Eecken Hvd, Adams R, Bogaert LV. Striopallidal-nigral degeneration. A hitherto undescribed lesion in paralysis agitans. J Neuropathol Exp Neurol. 1960;19:159-161.

[8] Adams RD, Vanbogaert L, Vandereecken H. Striato-Nigral Degeneration. J Neuropathol Exp Neurol 1964;23:584-608.

[9] Graham JG, Oppenheimer DR. Orthostatic hypotension and nicotine sensitivity in a case of multiple system atrophy. J Neurol Neurosurg Psychiatry 1969;32:28-34.

[10] Gilman S, Low PA, Quinn N, et al. Consensus statement on the diagnosis of multiple system atrophy. J Neurol Sci 1999;163:94-98.

[11] Gilman S, Wenning GK, Low PA, et al. Second consensus statement on the diagnosis of multiple system atrophy. Neurology; 2008;71:670-676.

[12] American-Psychiatric-Association. Diagnostic and statistical manual of mental disorders (DSM-IV-TR). 4th (text revision); 2000.

[13] Folstein MF, Folstein SE, McHugh PR. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975; 12:189-198.

[14] Wenning GK, Ben-Shlomo Y, Hughes A, Daniel SE, Lees A, Quinn NP. What clinical features are most useful to distinguish definite multiple system atrophy from Parkinson's disease? J Neurol Neurosurg Psychiatry 2000;68:434-440.

[15] Brown RG, Lacomblez L, Landwehrmeyer BG, et al. Cognitive impairment in patients with multiple system atrophy and progressive supranuclear palsy. Brain 2010;133:2382-2393.

[16] O'Sullivan SS, Massey LA, Williams DR, et al. Clinical outcomes of progressive supranuclear palsy and multiple system atrophy. Brain 2008;131.

[17] Köllensperger M, Geser F, Ndayisaba J.P, et al. Presentation, diagnosis, and management of multiple system atrophy in Europe: final analysis of the European multiple system atrophy registry. Mov Disord; 2010;25:2604-12.

[18] Gilman S, May SJ, Shults CW, et al. The North American Multiple System Atrophy Study Group. J Neural Transm; 2005; 112:1687-1694.

[19] Yabe I, Soma H, Takei A, Fujiki N, Yanagihara T, Sasaki H. MSA-C is the predominant clinical phenotype of MSA in Japan: analysis of 142 patients with probable MSA. J Neurol Sci 2006;249:115-121.

[20] Watanabe H, Saito Y, Terao S, et al. Progression and prognosis in multiple system atrophy: an analysis of 230 Japanese patients. Brain ; 2002;125:1070-1083.

[21] Barsottini OG. Parkinsonismo atípico. In: Ferraz B, editor. Doença de Parkinson: prática clínica e terapêutica. São Paulo: Editora Atheneu; 2005.

[22] Wenning GK, Tison F, Ben Shlomo Y, Daniel SE, Quinn NP. Multiple system atrophy: a review of 203 pathologically proven cases. Mov Disord 1997;12:133-147.

[23] Knopp DB, Barsottini OG, Ferraz HB. Multiple system atrophy speech assessment: study of five cases. Arq Neuropsiquiatr 2002;60:619-623.

[24] da Rocha AJ, Maia AC, Jr., da Silva CJ, et al. Pyramidal tract degeneration in multiple system atrophy: the relevance of magnetization transfer imaging. Mov Disord 2007;22:238-244.

[25] Geser F, Seppi K, Stampfer-Kountchev M, et al. The European Multiple System Atrophy-Study Group (EMSA-SG). J Neural Transm 2005;112:1677-1686.

[26] Sullivan EV, De La Paz R, Z ipursky RB, Pfefferbaum A. Neuropsychological deficits accompanying striatonigral degeneration. J Clin Exp Neuropsychol 1991;13:773-788.

[27] Kitayama M, Wada-Isoe K, Irizawa Y, Nakashima K. Assessment of dementia in patients with multiple system atrophy. Eur J Neurol 2009;16:589-594.

[28] Boeve BF, Silber MH, Saper CB, et al. Pathophysiology of REM sleep behaviour disorder and relevance to neurodegenerative disease. Brain 2007;130:2770-2788.

[29] Kawamura K, Shimohata T, Nakayama H, Tomita M, Ozawa T, Nishizawa M. Factors influencing the cognitive function in patients with multiple system atrophy. Mov Disord 2010; 25:2891-2892.

[30] Emre M, Aarsland D, Brown R, et al. Clinical diagnostic criteria for dementia associated with Parkinson's disease. Mov Disord 2007;22:1689-1707.

[31] Berent S, Giordani B, Gilman S, et al. Patterns of neuropsychological performance in multiple system atrophy compared to sporadic and hereditary olivopontocerebellar atrophy. Brain Cogn 2002;50:194-206.

[32] Kao AW, Racine CA, Quitania LC, Kramer JH, Christine CW, Miller BL. Cognitive and neuropsychiatric profile of the synucleinopathies: Parkinson disease, dementia with Lewy bodies, and multiple system atrophy. Alzheimer Dis Assoc Disord 2009;23:365-370.

[33] Miller BL, Cummings JL. Frontal subcortical circuits. In: Miller BL, Cummings JL, editors. The human frontal lobes : functions and disorders. 2nd ed. ed. New York, N.Y. ; London: Guilford Press; 2007:25.

[34] Desmond JE, Gabrieli JD, Wagner AD, Ginier BL, Glover GH. Lobular patterns of cerebellar activation in verbal working-memory and finger-tapping tasks as revealed by functional MRI. J Neurosci 1997;17:9675-9685.

[35] Bellebaum C, Daum I. Cerebellar involvement in executive control. Cerebellum. 2007;6:184-92.

[36] Grasby PM, Frith CD, Friston KJ, Bench C, Frackowiak RS, Dolan RJ. Functional mapping of brain areas implicated in auditory--verbal memory function. Brain 1993;116:1-20.

[37] Petersen SE, Fox PT, Posner MI, Mintun M, Raichle ME. Positron emission tomographic studies of the cortical anatomy of single-word processing. Nature 1988;331(6157):585-589.

[38] Allen G, Buxton RB, Wong EC, Courchesne E. Attentional activation of the cerebellum independent of motor involvement. Science. 1997;275(5308):1940-1943.

[39] Bürk K, Daum I, Rüb U. Cognitive function in multiple system atrophy of the cerebellar type. Mov Disord ; 2006;21:772-6.

[40] Kawai Y, Suenaga M, Takeda A, Ito M, Watanabe H, Tanaka F, et al. Cognitive impairments in multiple system atrophy: MSA-C vs MSA-P. Neurology 2008;70:1390-1396.

[41] Bak TH. Cognitive bedside assessment in atypical parkinsonian syndromes. J Neurol Neurosurg Psychiatr 2005;76:420-422.

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