Top

Published in:

01-01-2020 | Original Communication

Cognitive impairment and structural brain damage in multiple system atrophy-parkinsonian variant

Authors: Francesca Caso, Elisa Canu, Milica Jecmenica Lukic, Igor N. Petrovic, Andrea Fontana, Ivan Nikolic, Vladimir S. Kostic, Massimo Filippi, Federica Agosta

Published in: Journal of Neurology | Issue 1/2020

Abstract

In this multiparametric, cross-sectional study, we aimed to investigate cognitive impairment and brain structural changes in patients with multiple system atrophy (MSA)-parkinsonian variant (MSA-p). Twenty-six MSA-p patients and 19 controls underwent clinical and neuropsychological evaluation and 1.5 T brain MRI scan. Cortical thickness measures and volumes of deep grey matter structures were obtained. A regression analysis correlated MRI metrics with clinical features in MSA-p patients. Almost 46% of MSA-p patients showed a mild cognitive impairment involving mainly attentive–executive and memory domains. Apathy and depression were found in half of MSA-p patients. MSA-p patients showed significant cortical thinning of fronto-temporal–parietal regions and atrophy of periaqueductal grey matter, left cerebellar hemisphere, left pallidum and bilateral putamen, compared to controls. Cortical thinning in temporal regions correlated with global cognitive status and memory impairment. Grey matter cerebellar atrophy correlated with motor deficits. MSA-p patients showed a multidomain cognitive impairment with a prominent cortical damage in anterior more than posterior brain regions and grey matter volume reduction in subcortical structures. Cortical and subcortical structural changes might lead to cognitive dysfunction in MSA-p.

Gilman S, Wenning GK, Low PA, Brooks DJ, Mathias CJ, Trojanowski JQ, Wood NW, Colosimo C, Durr A, Fowler CJ, Kaufmann H, Klockgether T, Lees A, Poewe W, Quinn N, Revesz T, Robertson D, Sandroni P, Seppi K, Vidailhet M (2008) Second consensus statement on the diagnosis of multiple system atrophy. Neurology 71:670–676CrossRef

Stankovic I, Krismer F, Jesic A, Antonini A, Benke T, Brown RG, Burn DJ, Holton JL, Kaufmann H, Kostic VS, Ling H, Meissner WG, Poewe W, Semnic M, Seppi K, Takeda A, Weintraub D, Wenning GK, Movement Disorders Society MSASG (2014) Cognitive impairment in multiple system atrophy: a position statement by the neuropsychology task force of the MDS multiple system atrophy (MODIMSA) study group. Mov Disord 29:857–867CrossRef

Valera E, Masliah E (2018) The neuropathology of multiple system atrophy and its therapeutic implications. Auton Neurosci 211:1–6CrossRef

Kawai Y, Suenaga M, Takeda A, Ito M, Watanabe H, Tanaka F, Kato K, Fukatsu H, Naganawa S, Kato T, Ito K, Sobue G (2008) Cognitive impairments in multiple system atrophy: MSA-C vs MSA-P. Neurology 70:1390–1396CrossRef

Lyoo CH, Jeong Y, Ryu YH, Lee SY, Song TJ, Lee JH, Rinne JO, Lee MS (2008) Effects of disease duration on the clinical features and brain glucose metabolism in patients with mixed type multiple system atrophy. Brain 131:438–446CrossRef

Chelban V, Bocchetta M, Hassanein S, Haridy NA, Houlden H, Rohrer JD (2019) An update on advances in magnetic resonance imaging of multiple system atrophy. J Neurol 266:1036–1045CrossRef

Worker A, Blain C, Jarosz J, Chaudhuri KR, Barker GJ, Williams SC, Brown R, Leigh PN, Simmons A (2014) Cortical thickness, surface area and volume measures in Parkinson's disease, multiple system atrophy and progressive supranuclear palsy. PLoS ONE 9:e114167CrossRef

Kim JS, Youn J, Yang JJ, Lee DK, Lee JM, Kim ST, Kim HT, Cho JW (2013) Topographic distribution of cortical thinning in subtypes of multiple system atrophy. Parkinsonism Relat Disord 19:970–974CrossRef

Kim JS, Yang JJ, Lee DK, Lee JM, Youn J, Cho JW (2015) Cognitive impairment and its structural correlates in the Parkinsonian subtype of multiple system atrophy. Neurodegener Dis 15:294–300CrossRef

10.

Mioshi E, Dawson K, Mitchell J, Arnold R, Hodges JR (2006) The Addenbrooke's cognitive examination revised (ACE-R): a brief cognitive test battery for dementia screening. Int J Geriatr Psychiatry 21:1078–1085CrossRef

11.

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 12:189–198CrossRef

12.

Brown RG, Lacomblez L, Landwehrmeyer BG, Bak T, Uttner I, Dubois B, Agid Y, Ludolph A, Bensimon G, Payan C, Leigh NP, Group NS (2010) Cognitive impairment in patients with multiple system atrophy and progressive supranuclear palsy. Brain 133:2382–2393CrossRef

13.

McDonald WM, Holtzheimer PE, Haber M, Vitek JL, McWhorter K, Delong M (2006) Validity of the 30-item geriatric depression scale in patients with Parkinson's disease. Mov Disord 21:1618–1622CrossRef

14.

Leentjens AF, Dujardin K, Marsh L, Richard IH, Starkstein SE, Martinez-Martin P (2011) Anxiety rating scales in Parkinson's disease: a validation study of the Hamilton anxiety rating scale, the Beck anxiety inventory, and the hospital anxiety and depression scale. Mov Disord 26:407–415CrossRef

15.

Cummings JL, Mega M, Gray K, Rosenberg-Thompson S, Carusi DA, Gornbein J (1994) The neuropsychiatric inventory: comprehensive assessment of psychopathology in dementia. Neurology 44:2308–2314CrossRef

16.

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 4:134–139CrossRef

17.

Litvan I, Goldman JG, Troster AI, Schmand BA, Weintraub D, Petersen RC, Mollenhauer B, Adler CH, Marder K, Williams-Gray CH, Aarsland D, Kulisevsky J, Rodriguez-Oroz MC, Burn DJ, Barker RA, Emre M (2012) Diagnostic criteria for mild cognitive impairment in Parkinson's disease: movement disorder society task force guidelines. Mov Disord 27:349–356CrossRef

18.

Bak TH, Crawford LM, Hearn VC, Mathuranath PS, Hodges JR (2005) Subcortical dementia revisited: similarities and differences in cognitive function between progressive supranuclear palsy (PSP), corticobasal degeneration (CBD) and multiple system atrophy (MSA). Neurocase 11:268–273CrossRef

19.

Fischl B, Dale AM (2000) Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA 97:11050–11055CrossRef

20.

Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9:179–194CrossRef

21.

Desikan RS, Segonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killiany RJ (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31:968–980CrossRef

22.

Ashburner J (2007) A fast diffeomorphic image registration algorithm. Neuroimage 38:95–113CrossRef

23.

Wenning GK, Tison F, Ben Shlomo Y, Daniel SE, Quinn NP (1997) Multiple system atrophy: a review of 203 pathologically proven cases. Mov Disord 12:133–147CrossRef

24.

Siri C, Duerr S, Canesi M, Delazer M, Esselink R, Bloem BR, Gurevich T, Balas M, Giladi N, Santacruz P, Marti F, Tolosa E, Rubino A, Meco G, Poewe W, Pezzoli G, Wenning G, Antonini A (2013) A cross-sectional multicenter study of cognitive and behavioural features in multiple system atrophy patients of the parkinsonian and cerebellar type. J Neural Transm (Vienna) 120:613–618CrossRef

25.

Auzou N, Dujardin K, Biundo R, Foubert-Samier A, Barth C, Duval F, Tison F, Defebvre L, Antonini A, Meissner WG (2015) Diagnosing dementia in multiple system atrophy by applying Movement Disorder Society diagnostic criteria for Parkinson's disease dementia. Parkinsonism Relat Disord 21:1273–1277CrossRef

26.

Koga S, Parks A, Uitti RJ, van Gerpen JA, Cheshire WP, Wszolek ZK, Dickson DW (2017) Profile of cognitive impairment and underlying pathology in multiple system atrophy. Mov Disord 32:405–413CrossRef

27.

Fiorenzato E, Weis L, Seppi K, Onofrj M, Cortelli P, Zanigni S, Tonon C, Kaufmann H, Shepherd TM, Poewe W, Krismer F, Wenning G, Antonini A, Biundo R, Movement Disorders Society MSAN, Imaging Study G (2017) Brain structural profile of multiple system atrophy patients with cognitive impairment. J Neural Transm (Vienna) 124:293–302CrossRef

28.

Bell B, Lin JJ, Seidenberg M, Hermann B (2011) The neurobiology of cognitive disorders in temporal lobe epilepsy. Nat Rev Neurol 7:154–164CrossRef

29.

You H, Wang J, Wang H, Zang YF, Zheng FL, Meng CL, Feng F (2011) Altered regional homogeneity in motor cortices in patients with multiple system atrophy. Neurosci Lett 502:18–23CrossRef

30.

Rosskopf J, Gorges M, Muller HP, Pinkhardt EH, Ludolph AC, Kassubek J (2018) Hyperconnective and hypoconnective cortical and subcortical functional networks in multiple system atrophy. Parkinsonism Relat Disord 49:75–80CrossRef

31.

Yao Q, Zhu D, Li F, Xiao C, Lin X, Huang Q, Shi J (2017) Altered functional and causal connectivity of cerebello-cortical circuits between multiple system atrophy (Parkinsonian type) and Parkinson's disease. Front Aging Neurosci 9:266CrossRef

32.

Chang CC, Chang YY, Chang WN, Lee YC, Wang YL, Lui CC, Huang CW, Liu WL (2009) Cognitive deficits in multiple system atrophy correlate with frontal atrophy and disease duration. Eur J Neurol 16:1144–1150CrossRef

33.

Paviour DC, Price SL, Jahanshahi M, Lees AJ, Fox NC (2006) Longitudinal MRI in progressive supranuclear palsy and multiple system atrophy: rates and regions of atrophy. Brain 129:1040–1049CrossRef

Title: Cognitive impairment and structural brain damage in multiple system atrophy-parkinsonian variant
Authors: Francesca Caso
Elisa Canu
Milica Jecmenica Lukic
Igor N. Petrovic
Andrea Fontana
Ivan Nikolic
Vladimir S. Kostic
Massimo Filippi
Federica Agosta
Publication date: 01-01-2020
Publisher: Springer Berlin Heidelberg
Published in: Journal of Neurology / Issue 1/2020
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI: https://doi.org/10.1007/s00415-019-09555-y

At a glance: The STEP trials

Springer Medicine

Cognitive impairment and structural brain damage in multiple system atrophy-parkinsonian variant

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2020

Intracerebral haemorrhage on the acute stroke unit

New awakenings: current understanding of sleep dysfunction and its treatment in Parkinson’s disease

Lost or unavailable? Exploring mechanisms that affect retrograde memory in mild cognitive impairment and Alzheimer's disease patients

Chemosensory decrease in different forms of olfactory dysfunction

Sex-related differences in olfactory function and evaluation of possible confounding factors among patients with Parkinson’s disease

Apathy as a behavioural marker of cognitive impairment in Parkinson’s disease: a longitudinal analysis