Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
Journal of Neurology
Published in: Journal of Neurology 11/2018

01-11-2018 | Original Communication

Comparative cognitive and neuropsychiatric profiles between Parkinson’s disease, multiple system atrophy and progressive supranuclear palsy

Authors: Gabriella Santangelo, Sofia Cuoco, Maria Teresa Pellecchia, Roberto Erro, Paolo Barone, Marina Picillo

Published in: Journal of Neurology | Issue 11/2018

Login to get access

Abstract

Background

Parkinsonian syndromes are characterized by a wide spectrum of non-motor symptoms. A few studies explored cognitive deficits and neuropsychiatric symptoms in atypical parkinsonism compared to Parkinson’s disease (PD). The study was performed to identify cognitive and neuropsychiatric differences between PD, multiple system atrophy (MSA) and progressive supranuclear palsy (PSP) and to evaluate the influence of clinical features, depressive symptomatology and apathy on cognitive performances in the three groups.

Methods

Fifty-five PD, 44 MSA and 42 PSP patients underwent cognitive tests assessing attention, language, memory, visuospatial and executive functions as well as scales assessing depression and apathy. Out of these patients, 20 PD, 20 MSA and 20 PSP patients were selected to be matched for age, education and global cognitive status. Within each whole patients group, correlational analysis was performed between clinical, behavioural and cognitive parameters.

Results

The main difference among the groups matched was on cognitive tests exploring verbal learning, executive and linguistic functions. The PSP group was more impaired than the PD and MSA groups on cognitive tests assessing executive functions. On the other hand, MSA group obtained similar cognitive performance to the PD group. As to behavioural symptoms, in whole PSP and MSA groups, apathy and depression were more severe than in PD group, while apathy (but not depression) were more severe in the PSP group as compared to the MSA group.

Conclusions

The present study underlined the pervasiveness of cognitive deficits, apathy and depressive symptoms in PSP, whereas little cognitive differences were found between PD and MSA. The findings indirectly supported a dysfunction of prefronto-subcortical circuitries (i.e., dorsolateral prefrontal and limbic circuits) in PSP and PD. Cognitive similarities between MSA and PD reinforced the pivotal role of altered basal ganglia and corresponding frontal deafferentation in the occurrence of the cognitive deficits.
Appendix
Available only for authorised users
Literature
1.
Gerstenecker A (2017) The neuropsychology (broadly conceived) of multiple system atrophy, progressive supranuclear palsy, and corticobasal degeneration. Arch Clin Neuropsychol 32(7):861–875CrossRef
2.
Kehagia AA, Barker RA, Robbins TW (2010) Neuropsychological and clinical heterogeneity of cognitive impairment and dementia in patients with Parkinson’s disease. Lancet Neurol 9(12):1200–1213CrossRef
3.
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(4):268–273CrossRef
4.
Brown RG, Lacomblez L, Landwehrmeyer BG et al (2010) Cognitive impairment in patients with multiple system atrophy and progressive supranuclear palsy. Brain 133(Pt 8):2382–2393CrossRef
5.
Leiguarda RC, Pramstaller PP, Merello M, Starkstein S, Lees AJ, Marsden CD (1997) Apraxia in Parkinson’s disease, progressive supranuclear palsy, multiple system atrophy and neuroleptic-induced parkinsonism. Brain 120(Pt 1):75–90CrossRef
6.
Pillon B, Gouider-Khouja N, Deweer B et al (1995) Neuropsychological pattern of striatonigral degeneration: comparison with Parkinson’s disease and progressive supranuclear palsy. J Neurol Neurosurg Psychiatry 58(2):174–179CrossRef
7.
Krishnan S, Mathuranath PS, Sarma S, Kishore A (2006) Neuropsychological functions in progressive supranuclear palsy, multiple system atrophy and Parkinson’s disease. Neurol India 54(3):268–272CrossRef
8.
Lange KW, Tucha O, Alders GL et al (2003) Differentiation of parkinsonian syndromes according to differences in executive functions. J Neural Transm (Vienna) 110(9):983–995CrossRef
9.
Monza D, Soliveri P, Radice D et al (1998) Cognitive dysfunction and impaired organization of complex motility in degenerative parkinsonian syndromes. Arch Neurol 55(3):372–378CrossRef
10.
Robbins TW, James M, Owen AM et al (1994) Cognitive deficits in progressive supranuclear palsy, Parkinson’s disease, and multiple system atrophy in tests sensitive to frontal lobe dysfunction. J Neurol Neurosurg Psychiatry 57(1):79–88CrossRef
11.
Aarsland D, Litvan I, Larsen JP (2001) Neuropsychiatric symptoms of patients with progressive supranuclear palsy and Parkinson’s disease. J Neuropsychiatry Clin Neurosci 13(1):42–49CrossRef
12.
Schrag A, Sheikh S, Quinn NP et al (2010) A comparison of depression, anxiety, and health status in patients with progressive supranuclear palsy and multiple system atrophy. Mov Disord 25(8):1077–1081CrossRef
13.
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(3):181–184CrossRef
14.
Gilman S, Wenning GK, Low PA et al (2008) Second consensus statement on the diagnosis of multiple system atrophy. Neurology 71(9):670–676CrossRef
15.
Litvan I, Agid Y, Jankovic J et al (1996) Accuracy of clinical criteria for the diagnosis of progressive supranuclear palsy (Steele–Richardson–Olszewski syndrome). Neurology 46(4):922–930CrossRef
16.
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(15):2649–2653CrossRef
17.
18.
Lawton MP, Brody EM (1969) Assessment of older people: Self-maintaining and instrumental activities of daily living. Gerontologist 9:179–186CrossRef
19.
Fahn S, Elton RL, Members of the UPDRS Development Committee (1987) Unified Parkinson’s disease rating scale. In: Fahn S, Marsden CD, Calne D, Goldstein M (eds) Recent developments in Parkinson’s disease. MacMillan, Florham Park, pp 153–304
20.
Wenning GK, Tison F, Seppi K et al (2004) Development and validation of the Unified Multiple System Atrophy Rating Scale (UMSARS). Mov Disord 19(12):1391–1402CrossRef
21.
Golbe LI, Ohman-Strickland PA (2007) A clinical rating scale for progressive supranuclear palsy. Brain 130(Pt 6):1552–1565CrossRef
22.
Santangelo G, Siciliano M, Pedone R et al (2015) Normative data for the Montreal Cognitive Assessment in an Italian population sample. Neurol Sci 36(4):585–591CrossRef
23.
Giovagnoli AR, Del Pesce M, Mascheroni S, Simoncelli M, Laiacona M, Capitani E (1996) Trail making test: normative values from 287 normal adult controls. Ital J Neurol Sci 17(4):305–309CrossRef
24.
Caltagirone C, Gainotti G, Masullo C, Miceli G (1979) Validity of some neuropsychological test in the assessment of mental deterioration. Acta Psychiatr Scand 60:50–56CrossRef
25.
Barbarotto R, Laiacona M, Frosio R, Vecchio M, Farinato A, Capitani E (1998) A normative study on visual reaction times and two Stroop colour-word tests. Ital J Neurol Sci 19(3):161–170CrossRef
26.
Siciliano M, Santangelo G, D’Iorio A et al (2016) Rouleau version of the Clock Drawing Test: age- and education-adjusted normative data from a wide Italian sample. Clin Neuropsychol 30(sup1):1501–1516CrossRef
27.
Caffarra P, Vezzadini G, Dieci F, Zonato F, Venneri A (2002) Rey–Osterrieth complex figure: normative values in an Italian population sample. Neurol Sci 22(6):443–447CrossRef
28.
Novelli G, Papagno C, Capitani E, Laiacona M, Vallar G, Cappa SF (1986) Tre test clinici di ricerca e produzione lessicale. Taratura su soggetti normali. Arch Psicol Neurol Psichiatria 47(4):477–506
29.
Capasso R, Miceli G (2001) Esame Neuropsicologico per l’Afasia, ENPA. Springer, Milan
30.
Ferracuti S, Sacco R, Cannoni E, Hufty AM, Silvan AB, Hamster KDeS, Varney NR, Spreen O (2000) Contributi per un Assessment Neuropsicologico di Benton AL. Organizzazioni Speciali, Florence
31.
Spinnler H, Tognoni G (1987) Standardizzazione e taratura italiana di una batteria di test neuropsicologici. Ital J Neurol Sci 8:1–120
32.
Ghisi M, Flebus GB, Montano A, Sanavio E, Sica C (2006) Beck Depression Inventory-Second Edition. Adattamento italiano: Manuale. Organizzazioni Speciali, Florence
33.
Santangelo G, Barone P, Cuoco S et al (2014) Apathy in untreated, de novo patients with Parkinson’s disease: validation study of Apathy Evaluation Scale. J Neurol 261(12):2319–2328CrossRef
34.
Pitman EJG (1948) Lecture notes on nonparametric statistical inference: lectures given for the University of North Carolina. Columbia University, New York
35.
Boxer AL, Yu JT, Golbe LI, Litvan I, Lang AE, Höglinger GU (2017) Advances in progressive supranuclear palsy: new diagnostic criteria, biomarkers, and therapeutic approaches. Lancet Neurol 16(7):552–563CrossRef
36.
Stankovic I, Krismer F, Jesic A et al (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(7):857–867CrossRef
37.
Houghton DJ, Litvan I (2007) Unraveling progressive supranuclear palsy: from the bedside back to the bench. Parkinson Relat Disord Suppl 3:S341–S346CrossRef
38.
Rosskopf J, Gorges M, Müller HP et al (2017) Intrinsic functional connectivity alterations in progressive supranuclear palsy: differential effects in frontal cortex, motor, and midbrain networks. Mov Disord 32(7):1006–1015CrossRef
39.
Messina D, Cerasa A, Condino F et al (2011) Patterns of brain atrophy in Parkinson’s disease, progressive supranuclear palsy and multiple system atrophy. Parkinson Relat Disord 17(3):172–176CrossRef
40.
Schulz JB, Skalej M, Wedekind D et al (1999) Magnetic resonance imaging-based volumetry differentiates idiopathic Parkinson’s syndrome from multiple system atrophy and progressive supranuclear palsy. Ann Neurol 45(1):65–74CrossRef
41.
Rusz J, Bonnet C, Klempíř J et al (2015) Speech disorders reflect differing pathophysiology in Parkinson’s disease, progressive supranuclear palsy and multiple system atrophy. J Neurol 262(4):992–1001CrossRef
42.
Daniele A, Barbier A, Di Giuda D et al (2013) Selective impairment of action-verb naming and comprehension in progressive supranuclear palsy. Cortex 49(4):948–960CrossRef
43.
Rodríguez-Ferreiro J, Menéndez M, Ribacoba R, Cuetos F (2009) Action naming is impaired in Parkinson disease patients. Neuropsychologia 47(14):3271–3274CrossRef
44.
Silveri MC, Ciccarelli N, Baldonero E, Piano C, Zinno M, Soleti F, Bentivoglio AR, Albanese A, Daniele A (2012) Effects of stimulation of the subthalamic nucleus on naming and reading nouns and verbs in Parkinson’s disease. Neuropsychologia 50(8):1980–1989CrossRef
45.
Litvan I, Mega MS, Cummings JL, Fairbanks L (1996) Neuropsychiatric aspects of progressive supranuclear palsy. Neurology 47(5):1184–1189CrossRef
46.
Santangelo G, Vitale C, Trojano L et al (2015) Relationship between apathy and cognitive dysfunctions in de novo untreated Parkinson’s disease: a prospective longitudinal study. Eur J Neurol 22(2):253–260CrossRef
47.
48.
49.
Santangelo G, Vitale C, Picillo M et al (2015) Apathy and striatal dopamine transporter levels in de-novo, untreated Parkinson’s disease patients. Parkinson Relat Disord 21(5):489–493CrossRef
50.
Levy ML, Cummings JL, Fairbanks LA, Masterman D, Miller BL, Craig AH, Paulsen JS, Litvan I (1998) Apathy is not depression. J Neuropsychiatry Clin Neurosci 10(3):314–319CrossRef
51.
Cordato NJ, Halliday GM, Caine D et al (2006) Comparison of motor, cognitive, and behavioral features in progressive supranuclear palsy and Parkinson’s disease. Mov Disord 21:632–638CrossRef
52.
Lee CN, Kim M, Lee HM, Jang JW, Lee SM, Kwon DY, Park KW, Koh SB (2013) The interrelationship between non-motor symptoms in Atypical Parkinsonism. J Neurol Sci 327(1–2):15–21CrossRef
53.
Cordato NJ, Pantelis C, Halliday GM et al (2002) Frontal atrophy correlates with behavioural changes in progressive supranuclear palsy. Brain 125:789–800CrossRef
54.
Wenning GK, Ben-Shlomo BY, Megalhães M et al (1994) Clinical features and natural history of multiple system atrophy: an analysis of 100 cases. Brain 117:835–845CrossRef
55.
Tison F, Yekhlef F, Chrysostome V (2006) Depression and self-reported depressive symptoms in multiple system atrophy compared to Parkinson’s disease. Mov Disord 21(7):1056–1057CrossRef
56.
Duff K, Gerstenecker A, Litvan I, Investigators and Coordinators of the ENGENE-PSP Study Group (2013) Functional impairment in progressive supranuclear palsy. Neurology 80(4):380–384CrossRef
57.
58.
Höglinger GU, Respondek G, Stamelou M et al (2017) Clinical diagnosis of progressive supranuclear palsy: the movement disorder society criteria. Mov Disord 32(6):853–864CrossRef
Metadata
Title
Comparative cognitive and neuropsychiatric profiles between Parkinson’s disease, multiple system atrophy and progressive supranuclear palsy
Authors
Gabriella Santangelo
Sofia Cuoco
Maria Teresa Pellecchia
Roberto Erro
Paolo Barone
Marina Picillo
Publication date
01-11-2018
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 11/2018
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-018-9038-x

Other articles of this Issue 11/2018

Journal of Neurology 11/2018 Go to the issue

Original Communication

Affinities of human NMDA receptor autoantibodies: implications for disease mechanisms and clinical diagnostics

Original Communication

StartReact during gait initiation reveals differential control of muscle activation and inhibition in patients with corticospinal degeneration

Original Communication

Significance of CSF NfL and tau in ALS

Original Communication

Correlation of phenotype with genotype and protein structure in RYR1-related disorders

Letter to the Editors

Vertigo and impaired pursuit eye movements in a small medial superior temporal infarction

Original Communication

Treatment course and outcomes after revascularization surgery for moyamoya disease in adults