Abstract
Atypical Parkinsonism (AP) syndromes are characterized by a wide spectrum of non-motor symptoms including prominent attentional and executive deficits. However, the cognitive profile of AP and its differences and similarities with that of Parkinson’s Disease (PD) are still a matter of debate. The present meta-analysis aimed at identifying patterns of cognitive impairment in AP by comparing global cognitive functioning, memory, executive functions, visuospatial abilities, language, non-verbal reasoning, and processing speed test performances of patients with AP relative to healthy controls and patients with PD. All investigated cognitive domains showed a substantial impairment in patients with AP compared to healthy controls. When AP syndromes were considered separately, their cognitive functioning was distributed along a continuum from Multiple Systemic Atrophy at one extreme, with the least impaired cognitive profile (similar to that observed in PD) to Progressive Supranuclear Palsy, with the greatest decline in global cognitive and executive functioning (similar to Corticobasal Syndrome). These findings indicate that widespread cognitive impairment could represent an important clinical indicator to distinguish AP from other movement disorders.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of Data and Material
Data from the included primary studies is available in the supplementary tables and figures.
References
Aarsland, D., Litvan, I., Salmon, D., Galasko, D., Wentzel-Larsen, T., & Larsen, J. P. (2003). Performance on the dementia rating scale in Parkinson’s disease with dementia and dementia with Lewy bodies: Comparison with progressive supranuclear palsy and Alzheimer’s disease. Journal of Neurology, Neurosurgery, and Psychiatry, 74(9), 1215–1220. https://doi.org/10.1136/jnnp.74.9.1215
Agosta, F., Sarasso, E., & Filippi, M. (2018). Functional MRI in Atypical Parkinsonisms. International Review of Neurobiology, 142, 149–173. https://doi.org/10.1016/bs.irn.2018.09.002
Apostolova, L. G., Klement, I., Bronstein, Y., Vinters, H. V., & Cummings, J. L. (2006). Multiple system atrophy presenting with language impairment. Neurology, 67(4), 726–727. https://doi.org/10.1212/01.wnl.0000230136.82118.16
Armstrong, M. J., & McFarland, N. (2019). Recognizing and treating atypical Parkinson disorders. Handbook of Clinical Neurology, 167, 301–320. https://doi.org/10.1016/B978-0-12-804766-8.00016-9
Bak, T. H., Rogers, T. T., Crawford, L. M., Hearn, V. C., Mathuranath, P. S., & Hodges, J. R. (2005). Cognitive bedside assessment in atypical parkinsonian syndromes. Journal of Neurology, Neurosurgery, and Psychiatry, 76(3), 420–422. https://doi.org/10.1136/jnnp.2003.029595
Balas, M., Balash, Y., Giladi, N., & Gurevich, T. (2010). Cognition in multiple system atrophy: neuropsychological profile and interaction with mood. Journal of neural transmission (Vienna, Austria: 1996), 117(3), 369–375. https://doi.org/10.1007/s00702-009-0365-z.
Berent, S., Giordani, B., Gilman, S., Trask, C. L., Little, R. J., Johanns, J. R., Junck, L., Kluin, K. J., Heumann, M., & Koeppe, R. A. (2002). Patterns of neuropsychological performance in multiple system atrophy compared to sporadic and hereditary olivopontocerebellar atrophy. Brain and Cognition, 50(2), 194–206. https://doi.org/10.1016/s0278-2626(02)00503-1
Bhatia, K. P., & Stamelou, M. (2017). Nonmotor Features in Atypical Parkinsonism. International Review of Neurobiology, 134, 1285–1301. https://doi.org/10.1016/bs.irn.2017.06.001
Bhidayasiri, R., Sringean, J., Reich, S. G., & Colosimo, C. (2019). Red flags phenotyping: A systematic review on clinical features in atypical parkinsonian disorders. Parkinsonism & Related Disorders, 59, 82–92. https://doi.org/10.1016/j.parkreldis.2018.10.009
Borenstein, M., Hedges, L. V., Higgins, J. P., & Rothstein, H. R. (2011). Introduction to meta-analysis. John Wiley & Sons.
Borroni, B., Turla, M., Bertasi, V., Agosti, C., Gilberti, N., & Padovani, A. (2008). Cognitive and behavioral assessment in the early stages of neurodegenerative extrapyramidal syndromes. Archives of Gerontology and Geriatrics, 47(1), 53–61. https://doi.org/10.1016/j.archger.2007.07.005
Brown, R. G., Lacomblez, L., Landwehrmeyer, B. G., Bak, T., Uttner, I., Dubois, B., et al. (2010). Cognitive impairment in patients with multiple system atrophy and progressive supranuclear palsy. Brain: a journal of neurology, 133(Pt 8), 2382–2393. https://doi.org/10.1093/brain/awq158.
Brown, J. A., Hua, A. Y., Trujllo, A., Attygalle, S., Binney, R. J., Spina, S., Lee, S. E., Kramer, J. H., Miller, B. L., Rosen, H. J., Boxer, A. L., & Seeley, W. W. (2017). Advancing functional dysconnectivity and atrophy in progressive supranuclear palsy. NeuroImage. Clinical, 16, 564–574. https://doi.org/10.1016/j.nicl.2017.09.008
Bürk, K., Daum, I., & Rüb, U. (2006). Cognitive function in multiple system atrophy of the cerebellar type. Movement Disorders: Official Journal of the Movement Disorder Society, 21(6), 772–776. https://doi.org/10.1002/mds.20802
Burrell, J. R., Hornberger, M., Villemagne, V. L., Rowe, C. C., & Hodges, J. R. (2013). Clinical profile of PiB-positive corticobasal syndrome. PLoS ONE, 8(4), e61025. https://doi.org/10.1371/journal.pone.0061025
Burrell, J. R., Ballard, K. J., Halliday, G. M., & Hodges, J. R. (2018). Aphasia in Progressive Supranuclear Palsy: As Severe as Progressive Non-Fluent Aphasia. Journal of Alzheimer’s Disease: JAD, 61(2), 705–715. https://doi.org/10.3233/JAD-170743
Chang, C. C., Chang, Y. Y., Chang, W. N., Lee, Y. C., Wang, Y. L., Lui, C. C., Huang, C. W., & Liu, W. L. (2009). Cognitive deficits in multiple system atrophy correlate with frontal atrophy and disease duration. European Journal of Neurology, 16(10), 1144–1150. https://doi.org/10.1111/j.1468-1331.2009.02661.x
Chiu, W. Z., Papma, J. M., de Koning, I., Donker Kaat, L., Seelaar, H., Reijs, A. E., Valkema, R., Hasan, D., Boon, A. J., & van Swieten, J. C. (2012). Midcingulate involvement in progressive supranuclear palsy and tau positive frontotemporal dementia. Journal of Neurology, Neurosurgery, and Psychiatry, 83(9), 910–915. https://doi.org/10.1136/jnnp-2011-302035
Chow, M. L., Brambati, S. M., Gorno-Tempini, M. L., Miller, B. L., & Johnson, J. K. (2010). Sound naming in neurodegenerative disease. Brain and Cognition, 72(3), 423–429. https://doi.org/10.1016/j.bandc.2009.12.003
Cohen, J. (1988). Statistical power analysis for the behavioral sciences. Academic Press.
Collerton, D., Burn, D., McKeith, I., & O’Brien, J. (2003). Systematic review and meta-analysis show that dementia with Lewy bodies is a visual-perceptual and attentional-executive dementia. Dementia and Geriatric Cognitive Disorders, 16(4), 229–237. https://doi.org/10.1159/000072807
Cordato, N. J., Halliday, G. M., Caine, D., & Morris, J. G. (2006). Comparison of motor, cognitive, and behavioral features in progressive supranuclear palsy and Parkinson’s disease. Movement Disorders: Official Journal of the Movement Disorder Society, 21(5), 632–638. https://doi.org/10.1002/mds.20779
Cotelli, M., Borroni, B., Manenti, R., Ginex, V., Calabria, M., Moro, A., Alberici, A., Zanetti, M., Zanetti, O., Cappa, S. F., & Padovani, A. (2007). Universal grammar in the frontotemporal dementia spectrum: Evidence of a selective disorder in the corticobasal degeneration syndrome. Neuropsychologia, 45(13), 3015–3023. https://doi.org/10.1016/j.neuropsychologia.2007.05.012
Crucian, G. P., & Okun, M. S. (2003). Visual-spatial ability in Parkinson’s disease. Frontiers in Bioscience: A Journal and Virtual Library, 8, s992–s997. https://doi.org/10.2741/1171
Dubois, B., Pillon, B., Legault, F., Agid, Y., & Lhermitte, F. (1998). Slowing of cognitive processing in progressive supranuclear palsy. A comparison with Parkinson’s disease. Archives of neurology, 45(11), 1194–1199. https://doi.org/10.1001/archneur.1988.00520350032011.
Duff, K., Beglinger, L. J., Theriault, D., Allison, J., & Paulsen, J. S. (2010). Cognitive deficits in Huntington’s disease on the Repeatable Battery for the Assessment of Neuropsychological Status. Journal of Clinical and Experimental Neuropsychology, 32(3), 231–238. https://doi.org/10.1080/13803390902926184
Dujardin, K., Defebvre, L., Krystkowiak, P., Degreef, J. F., & Destee, A. (2003). Executive function differences in multiple system atrophy and Parkinson’s disease. Parkinsonism & Related Disorders, 9(4), 205–211. https://doi.org/10.1016/s1353-8020(02)00050-0
Dutt, S., Binney, R. J., Heuer, H. W., Luong, P., Attygalle, S., Bhatt, P., Marx, G. A., Elofson, J., Tartaglia, M. C., Litvan, I., McGinnis, S. M., Dickerson, B. C., Kornak, J., Waltzman, D., Voltarelli, L., Schuff, N., Rabinovici, G. D., Kramer, J. H., Jack, C. R., Jr., … AL-108-231 investigators. (2016). Progression of brain atrophy in PSP and CBS over 6 months and 1 year. Neurology, 87(19), 2016–2025. https://doi.org/10.1212/WNL.0000000000003305
Duval, S. (2005). The trim and fill method. In H. R. Rothstein, A. J. Sutton, & M. Borenstein (Eds.), Publication bias in meta-analysis (pp. 11–33). Wiley.
Egger, M., Davey Smith, G., Schneider, M., & Minder, C. (1997). Bias in meta-analysis detected by a simple, graphical test. BMJ (clinical Research Ed.), 315(7109), 629–634. https://doi.org/10.1136/bmj.315.7109.629
Elgh, E., Domellöf, M., Linder, J., Edström, M., Stenlund, H., & Forsgren, L. (2009). Cognitive function in early Parkinson’s disease: A population-based study. European Journal of Neurology, 16(12), 1278–1284. https://doi.org/10.1111/j.1468-1331.2009.02707.x
Endo, H., Shimada, H., Sahara, N., Ono, M., Koga, S., Kitamura, S., Niwa, F., Hirano, S., Kimura, Y., Ichise, M., Shinotoh, H., Zhang, M. R., Kuwabara, S., Dickson, D. W., Toda, T., Suhara, T., & Higuchi, M. (2019). In vivo binding of a tau imaging probe, [11 C]PBB3, in patients with progressive supranuclear palsy. Movement Disorders: Official Journal of the Movement Disorder Society, 34(5), 744–754. https://doi.org/10.1002/md.27643
Esmonde, T., Giles, E., Gibson, M., & Hodges, J. R. (1996). Neuropsychological performance, disease severity, and depression in progressive supranuclear palsy. Journal of Neurology, 243(9), 638–643. https://doi.org/10.1007/BF00878659
Fang, C., Lv, L., Mao, S., Dong, H., & Liu, B. (2020). Cognition Deficits in Parkinson’s Disease: Mechanisms and Treatment. Parkinson’s Disease, 2020, 2076942. https://doi.org/10.1155/2020/2076942
Fiorenzato, E., Weis, L., Falup-Pecurariu, C., Diaconu, S., Siri, C., Reali, E., et al. (2016). Montreal Cognitive Assessment (MoCA) and Mini-Mental State Examination (MMSE) performance in progressive supranuclear palsy and multiple system atrophy. Journal of neural transmission (Vienna, Austria: 1996), 123(12), 1435–1442. https://doi.org/10.1007/s00702-016-1589-3.
Fiorenzato, E., Antonini, A., Camparini, V., Weis, L., Semenza, C., & Biundo, R. (2019). Characteristics and progression of cognitive deficits in progressive supranuclear palsy vs. multiple system atrophy and Parkinson’s disease. Journal of neural transmission (Vienna, Austria: 1996), 126(11), 1437–1445. https://doi.org/10.1007/s00702-019-02065-1.
Foley, J. A., Niven, E. H., Paget, A., Bhatia, K. P., Farmer, S. F., Jarman, P. R., Limousin, P., Warner, T. T., Morris, H. R., Bak, T. H., Abrahams, S., & Cipolotti, L. (2018). Sensitivity and Specificity of the ECAS in Parkinson’s Disease and Progressive Supranuclear Palsy. Parkinson’s Disease, 2018, 2426012. https://doi.org/10.1155/2018/2426012
Frommann, I., Schmitz-Hübsch, T., Hoenig, K., Minnerop, M., Daum, I., Wüllner, U., & Wagner, M. (2012). Distinct patterns of cognitive impairment in multiple system atrophy patients of cerebellar and parkinsonian predominance. Basal Ganglia, 2, 91–96. https://doi.org/10.1016/j.baga.2012.02.001
Gainotti, G., Marra, C., Villa, G., Parlato, V., & Chiarotti, F. (1998). Sensitivity and specificity of some neuropsychological markers of Alzheimer dementia. Alzheimer Disease and Associated Disorders, 12(3), 152–162. https://doi.org/10.1097/00002093-199809000-00006
Gerhard, A., Trender-Gerhard, I., Turkheimer, F., Quinn, N. P., Bhatia, K. P., & Brooks, D. J. (2006). In vivo imaging of microglial activation with [11C](R)-PK11195 PET in progressive supranuclear palsy. Movement Disorders: Official Journal of the Movement Disorder Society, 21(1), 89–93. https://doi.org/10.1002/mds.20668
Gerstenecker, A., Mast, B., Duff, K., Ferman, T. J., Litvan, I., & ENGENE-PSP Study Group. (2013). Executive dysfunction is the primary cognitive impairment in progressive supranuclear palsy. Archives of Clinical Neuropsychology: THe Official Journal of the National Academy of Neuropsychologists, 28(2), 104–113. https://doi.org/10.1093/arclin/acs098
Ghosh, B. C., Carpenter, R. H., & Rowe, J. B. (2013). A longitudinal study of motor, oculomotor and cognitive function in progressive supranuclear palsy. PLoS ONE, 8(9), e74486. https://doi.org/10.1371/journal.pone.0074486
Gilman, S., Low, P. A., Quinn, N., Albanese, A., Ben-Shlomo, Y., Fowler, C. J., Kaufmann, H., Klockgether, T., Lang, A. E., Lantos, P. L., Litvan, I., Mathias, C. J., Oliver, E., Robertson, D., Schatz, I., & Wenning, G. K. (1998). Consensus statement on the diagnosis of multiple system atrophy. Journal of the Autonomic Nervous System, 74(2–3), 189–192.
Gilman, S., Wenning, G. K., Low, P. A., Brooks, D. J., Mathias, C. J., Trojanowski, J. Q., Wood, N. W., Colosimo, C., Dürr, A., Fowler, C. J., 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(9), 670–676. https://doi.org/10.1212/01.wnl.0000324625.00404.15
Giordano, A., Tessitore, A., Corbo, D., Cirillo, G., de Micco, R., Russo, A., Liguori, S., Cirillo, M., Esposito, F., & Tedeschi, G. (2013). Clinical and cognitive correlations of regional gray matter atrophy in progressive supranuclear palsy. Parkinsonism & Related Disorders, 19(6), 590–594. https://doi.org/10.1016/j.parkreldis.2013.02.005
Grafman, J., Litvan, I., Gomez, C., & Chase, T. N. (1990). Frontal lobe function in progressive supranuclear palsy. Archives of Neurology, 47(5), 553–558. https://doi.org/10.1001/archneur.1990.00530050077015
Gurnani, A. S., & Gavett, B. E. (2017). The Differential Effects of Alzheimer’s Disease and Lewy Body Pathology on Cognitive Performance: A Meta-analysis. Neuropsychology Review, 27(1), 1–17. https://doi.org/10.1007/s11065-016-9334-0
Hall, S., Janelidze, S., Surova, Y., Widner, H., Zetterberg, H., & Hansson, O. (2018). Cerebrospinal fluid concentrations of inflammatory markers in Parkinson’s disease and atypical parkinsonian disorders. Scientific Reports, 8(1), 13276. https://doi.org/10.1038/s41598-018-31517-z
Hauw, J. J., Daniel, S. E., Dickson, D., Horoupian, D. S., Jellinger, K., Lantos, P. L., McKee, A., Tabaton, M., & Litvan, I. (1994). Preliminary NINDS neuropathologic criteria for Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy). Neurology, 44(11), 2015–2019. https://doi.org/10.1212/wnl.44.11.2015
Heim, B., Krismer, F., & Seppi, K. (2018). Structural Imaging in Atypical Parkinsonism. International Review of Neurobiology, 142, 67–148. https://doi.org/10.1016/bs.irn.2018.08.010
Heyder, K., Suchan, B., & Daum, I. (2004). Cortico-subcortical contributions to executive control. Acta Psychologica, 115(2–3), 271–289. https://doi.org/10.1016/j.actpsy.2003.12.010
Hoehn, M. M., & Yahr, M. D. (1967). Parkinsonism: Onset, progression and mortality. Neurology, 17(5), 427–442. https://doi.org/10.1212/wnl.17.5.427
Hong, H. J., Song, S. K., Lee, P. H., Sohn, Y. H., & Lee, J. E. (2011). Cognitive impairments in multiple system atrophy of the cerebellar type. Journal of movement disorders, 4(1), 41–45. https://doi.org/10.14802/jmd.11007.
Hong, J. Y., Yun, H. J., Sunwoo, M. K., Ham, J. H., Lee, J. M., Sohn, Y. H., & Lee, P. H. (2015). Comparison of regional brain atrophy and cognitive impairment between pure akinesia with gait freezing and Richardson’s syndrome. Frontiers in Aging Neuroscience, 7, 180. https://doi.org/10.3389/fnagi.2015.00180
Horta-Barba, A., Pagonabarraga, J., Martínez-Horta, S., Busteed, L., Pascual-Sedano, B., Illán-Gala, I., Marin-Lahoz, J., Aracil-Bolaños, I., Pérez-Pérez, J., Sampedro, F., Bejr-Kasem, H., & Kulisevsky, J. (2021). Cognitive and behavioral profile of progressive supranuclear palsy and its phenotypes. Journal of Neurology. https://doi.org/10.1007/s00415-021-10511-y. Advance online publication.
Hua, M. S., & Lu, C. S. (1994). Multiple system atrophy and visuospatial function. Neuropsychology, 8(1), 91–94. https://doi.org/10.1037/0894-4105.8.1.91
Huedo-Medina, T. B., Sánchez-Meca, J., Marín-Martínez, F., & Botella, J. (2006). Assessing heterogeneity in meta-analysis: Q statistic or I2 index? Psychological Methods, 11(2), 193–206. https://doi.org/10.1037/1082-989X.11.2.193
Isella, V., Rucci, F., Traficante, D., Mapelli, C., Ferri, F., & Appollonio, I. M. (2013). The applause sign in cortical and cortical-subcortical dementia. Journal of Neurology, 260(4), 1099–1103. https://doi.org/10.1007/s00415-012-6767-0
Johnson, K. A., Sperling, R. A., Holman, B. L., Nagel, J. S., & Growdon, J. H. (1992). Cerebral perfusion in progressive supranuclear palsy. Journal of Nuclear Medicine: Official Publication, Society of Nuclear Medicine, 33(5), 704–709.
Kao, A. W., Racine, C. A., Quitania, L. C., Kramer, J. H., Christine, C. W., & Miller, B. L. (2009). Cognitive and neuropsychiatric profile of the synucleinopathies: Parkinson disease, dementia with Lewy bodies, and multiple system atrophy. Alzheimer Disease and Associated Disorders, 23(4), 365–370. https://doi.org/10.1097/WAD.0b013e3181b5065d
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(16 Pt 2), 1390–1396. https://doi.org/10.1212/01.wnl.0000310413.04462.6a
Kawamura, K., Shimohata, T., Nakayama, H., Tomita, M., Ozawa, T., & Nishizawa, M. (2010). Factors influencing the cognitive function in patients with multiple system atrophy. Movement Disorders: Official Journal of the Movement Disorder Society, 25(16), 2891–2892. https://doi.org/10.1002/mds.23260
Kim, H. J., Jeon, B. S., Kim, Y. E., Kim, J. Y., Kim, Y. K., Sohn, C. H., Yun, J. Y., Jeon, S., Lee, J. M., & Lee, J. Y. (2013). Clinical and imaging characteristics of dementia in multiple system atrophy. Parkinsonism & Related Disorders, 19(6), 617–621. https://doi.org/10.1016/j.parkreldis.2013.02.012
Kim, J. S., Yang, J. J., Lee, D. K., Lee, J. M., Youn, J., & Cho, J. W. (2015). Cognitive Impairment and Its Structural Correlates in the Parkinsonian Subtype of Multiple System Atrophy. Neuro-Degenerative Diseases, 15(5), 294–300. https://doi.org/10.1159/000430953-
Krishnan, S., Mathuranath, P. S., Sarma, S., & Kishore, A. (2006). Neuropsychological functions in progressive supranuclear palsy, multiple system atrophy and Parkinson’s disease. Neurology India, 54(3), 268–272. https://doi.org/10.4103/0028-3886.27150
Kumfor, F., Sapey-Triomphe, L. A., Leyton, C. E., Burrell, J. R., Hodges, J. R., & Piguet, O. (2014). Degradation of emotion processing ability in corticobasal syndrome and Alzheimer’s disease. Brain: a journal of neurology, 137(Pt 11), 3061–3072. https://doi.org/10.1093/brain/awu246.
Lagarde, J., Valabrègue, R., Corvol, J. C., Pineau, F., Le Ber, I., Vidailhet, M., Dubois, B., & Levy, R. (2013). Are frontal cognitive and atrophy patterns different in PSP and bvFTD? A comparative neuropsychological and VBM study. PLoS ONE, 8(11), e80353. https://doi.org/10.1371/journal.pone.0080353
Lange, K. W., Tucha, O., Alders, G. L., Preier, M., Csoti, I., Merz, B., et al. (2003). Differentiation of parkinsonian syndromes according to differences in executive functions. Journal of neural transmission (Vienna, Austria: 1996), 110(9), 983–995. https://doi.org/10.1007/s00702-003-0011-0.
Lee, M. J., Shin, J. H., Seoung, J. K., Lee, J. H., Yoon, U., Oh, J. H., Jung, D. S., & Kim, E. J. (2016a). Cognitive impairments associated with morphological changes in cortical and subcortical structures in multiple system atrophy of the cerebellar type. European Journal of Neurology, 23(1), 92–100. https://doi.org/10.1111/ene.12796
Lee, Y. E., Williams, D. R., & Anderson, J. F. (2016b). Frontal deficits differentiate progressive supranuclear palsy from Parkinson’s disease. Journal of Neuropsychology, 10(1), 1–14. https://doi.org/10.1111/jnp.12053
Litvan, I., Agid, Y., Calne, D., Campbell, G., Dubois, B., Duvoisin, R. C., Goetz, C. G., Golbe, L. I., Grafman, J., Growdon, J. H., Hallett, M., Jankovic, J., Quinn, N. P., Tolosa, E., & Zee, D. S. (1996). Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome): Report of the NINDS-SPSP international workshop. Neurology, 47(1), 1–9. https://doi.org/10.1212/wnl.47.1.1
Litvan, I., Goldman, J. G., Tröster, A. I., Schmand, B. A., Weintraub, D., Petersen, R. C., Mollenhauer, B., Adler, C. H., Marder, K., Williams-Gray, C. H., Aarsland, D., Kulisevsky, J., Rodriguez-Oroz, M. C., Burn, D. J., Barker, R. A., & Emre, M. (2012). Diagnostic criteria for mild cognitive impairment in Parkinson’s disease: Movement Disorder Society Task Force guidelines. Movement Disorders: Official Journal of the Movement Disorder Society, 27(3), 349–356. https://doi.org/10.1002/mds.24893
Magerova, H., Vyhnalek, M., Laczo, J., Andel, R., Rektorova, I., Kadlecova, A., Bojar, M., & Hort, J. (2014). Odor identification in frontotemporal lobar degeneration subtypes. American Journal of Alzheimer’s Disease and Other Dementias, 29(8), 762–768. https://doi.org/10.1177/1533317514539033
Manuel, A. L., Foxe, D., Bradshaw, N., Cordato, N. J., Hodges, J. R., Burrell, J. R., & Piguet, O. (2019). Sustained attention failures on a 3-min reaction time task is a sensitive marker of dementia. Journal of Neurology, 266(6), 1323–1331. https://doi.org/10.1007/s00415-019-09261-9
Matsuda, K., Satoh, M., Tabei, K. I., Ueda, Y., Taniguchi, A., Matsuura, K., Asahi, M., Ii, Y., Niwa, A., & Tomimoto, H. (2020). Impairment of intermediate somatosensory function in corticobasal syndrome. Scientific Reports, 10(1), 11155. https://doi.org/10.1038/s41598-020-67991-7
McFarland, N. R., & Hess, C. W. (2017). Recognizing Atypical Parkinsonisms: “Red Flags” and Therapeutic Approaches. Seminars in Neurology, 37(2), 215–227. https://doi.org/10.1055/s-0037-1602422
Meco, G., Gasparini, M., & Doricchi, F. (1996). Attentional functions in multiple system atrophy and Parkinson’s disease. Journal of Neurology, Neurosurgery, and Psychiatry, 60(4), 393–398. https://doi.org/10.1136/jnnp.60.4.393
Misch, M. R., Mitchell, S., Francis, P. L., Sherborn, K., Meradje, K., McNeely, A. A., Honjo, K., Zhao, J., Scott, C. J., Caldwell, C. B., Ehrlich, L., Shammi, P., MacIntosh, B. J., Bilbao, J. M., Lang, A. E., Black, S. E., & Masellis, M. (2014). Differentiating between visual hallucination-free dementia with Lewy bodies and corticobasal syndrome on the basis of neuropsychology and perfusion single-photon emission computed tomography. Alzheimer’s Research & Therapy, 6(9), 71. https://doi.org/10.1186/s13195-014-0071-4
Modesti, P. A., Reboldi, G., Cappuccio, F. P., Agyemang, C., Remuzzi, G., Rapi, S., Perruolo, E., Parati, G., & ESH Working Group on CV Risk in Low Resource Settings. (2016). Panethnic Differences in Blood Pressure in Europe: A Systematic Review and Meta-Analysis. PLoS ONE, 11(1), e0147601. https://doi.org/10.1371/journal.pone.0147601
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & PRISMA Group. (2009). Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Medicine, 6(7), e1000097. https://doi.org/10.1371/journal.pmed.1000097
Moher, D., Shamseer, L., Clarke, M., Ghersi, D., Liberati, A., Petticrew, M., Shekelle, P., Stewart, L. A., & PRISMA-P Group. (2015). Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Systematic Reviews, 4(1), 1. https://doi.org/10.1186/2046-4053-4-1
Monza, D., Soliveri, P., Radice, D., Fetoni, V., Testa, D., Caffarra, P., Caraceni, T., & Girotti, F. (1998). Cognitive dysfunction and impaired organization of complex motility in degenerative parkinsonian syndromes. Archives of Neurology, 55(3), 372–378. https://doi.org/10.1001/archneur.55.3.372
Murueta-Goyena, A., Del Pino, R., Galdós, M., Arana, B., Acera, M., Carmona-Abellán, M., Fernández-Valle, T., Tijero, B., Lucas-Jiménez, O., Ojeda, N., Ibarretxe-Bilbao, N., Peña, J., Cortes, J., Ayala, U., Barrenechea, M., Gómez-Esteban, J. C., & Gabilondo, I. (2021). Retinal Thickness Predicts the Risk of Cognitive Decline in Parkinson Disease. Annals of Neurology, 89(1), 165–176. https://doi.org/10.1002/ana.25944
Noe, E., Marder, K., Bell, K. L., Jacobs, D. M., Manly, J. J., & Stern, Y. (2004). Comparison of dementia with Lewy bodies to Alzheimer’s disease and Parkinson’s disease with dementia. Movement Disorders: Official Journal of the Movement Disorder Society, 19(1), 60–67. https://doi.org/10.1002/mds.10633
O’Keeffe, F. M., Murray, B., Coen, R. F., Dockree, P. M., Bellgrove, M. A., Garavan, H., et al. (2007). Loss of insight in frontotemporal dementia, corticobasal degeneration and progressive supranuclear palsy. Brain: a journal of neurology, 130(Pt 3), 753–764. https://doi.org/10.1093/brain/awl367.
Pellicano, C., Assogna, F., Cellupica, N., Piras, F., Pierantozzi, M., Stefani, A., Cerroni, R., Mercuri, B., Caltagirone, C., Pontieri, F. E., & Spalletta, G. (2017). Neuropsychiatric and cognitive profile of early Richardson’s syndrome, Progressive Supranuclear Palsy-parkinsonism and Parkinson’s disease. Parkinsonism & Related Disorders, 45, 50–56. https://doi.org/10.1016/j.parkreldis.2017.10.002
Peterson, K. A., Patterson, K., & Rowe, J. B. (2021). Language impairment in progressive supranuclear palsy and corticobasal syndrome. Journal of Neurology, 268(3), 796–809. https://doi.org/10.1007/s00415-019-09463-1
Petrova, M., Mehrabian-Spasova, S., Aarsland, D., Raycheva, M., & Traykov, L. (2015). Clinical and Neuropsychological Differences between Mild Parkinson’s Disease Dementia and Dementia with Lewy Bodies. Dementia and Geriatric Cognitive Disorders Extra, 5(2), 212–220. https://doi.org/10.1159/000375363
Pillon, B., Gouider-Khouja, N., Deweer, B., Vidailhet, M., Malapani, C., Dubois, B., & Agid, Y. (1995). Neuropsychological pattern of striatonigral degeneration: Comparison with Parkinson’s disease and progressive supranuclear palsy. Journal of Neurology, Neurosurgery, and Psychiatry, 58(2), 174–179. https://doi.org/10.1136/jnnp.58.2.174
Ramanan, S., Strikwerda-Brown, C., Mothakunnel, A., Hodges, J. R., Piguet, O., & Irish, M. (2019). Fronto-parietal contributions to episodic retrieval-evidence from neurodegenerative disorders. Learning & memory (Cold Spring Harbor, N.Y.), 26(7), 262–271. https://doi.org/10.1101/lm.048454.118.
Rittman, T., Ghosh, B. C., McColgan, P., Breen, D. P., Evans, J., Williams-Gray, C. H., Barker, R. A., & Rowe, J. B. (2013). The Addenbrooke’s Cognitive Examination for the differential diagnosis and longitudinal assessment of patients with parkinsonian disorders. Journal of Neurology, Neurosurgery, and Psychiatry, 84(5), 544–551. https://doi.org/10.1136/jnnp-2012-303618
Robbins, T. W., James, M., Lange, K. W., Owen, A. M., Quinn, N. P., & Marsden, C. D. (1992). Cognitive performance in multiple system atrophy. Brain: a journal of neurology, 115(Pt 1), 271–291. https://doi.org/10.1093/brain/115.1.271.
Robbins, T. W., James, M., Owen, A. M., Lange, K. W., Lees, A. J., Leigh, P. N., Marsden, C. D., Quinn, N. P., & Summers, B. A. (1994). Cognitive deficits in progressive supranuclear palsy, Parkinson’s disease, and multiple system atrophy in tests sensitive to frontal lobe dysfunction. Journal of Neurology, Neurosurgery, and Psychiatry, 57(1), 79–88. https://doi.org/10.1136/jnnp.57.1.79
Rohrer, J. D., Paviour, D., Bronstein, A. M., O’Sullivan, S. S., Lees, A., & Warren, J. D. (2010). Progressive supranuclear palsy syndrome presenting as progressive nonfluent aphasia: A neuropsychological and neuroimaging analysis. Movement Disorders: Official Journal of the Movement Disorder Society, 25(2), 179–188. https://doi.org/10.1002/mds.22946
Rothstein, H. R., Sutton, A. J., & Borenstein, M. (2005). Publication bias in meta-analysis. Wiley.
Rusz, J., Bonnet, C., Klempíř, J., Tykalová, T., Baborová, E., Novotný, M., Rulseh, A., & Růžička, E. (2015). Speech disorders reflect differing pathophysiology in Parkinson’s disease, progressive supranuclear palsy and multiple system atrophy. Journal of Neurology, 262(4), 992–1001. https://doi.org/10.1007/s00415-015-7671-1
Saeed, U., Compagnone, J., Aviv, R. I., Strafella, A. P., Black, S. E., Lang, A. E., & Masellis, M. (2017). Imaging biomarkers in Parkinson’s disease and Parkinsonian syndromes: Current and emerging concepts. Translational Neurodegeneration, 6, 8. https://doi.org/10.1186/s40035-017-0076-6
Sajjadi, S. A., Acosta-Cabronero, J., Patterson, K., Diaz-de-Grenu, L. Z., Williams, G. B., & Nestor, P. J. (2013). Diffusion tensor magnetic resonance imaging for single subject diagnosis in neurodegenerative diseases. Brain: a journal of neurology, 136(Pt 7), 2253–2261. https://doi.org/10.1093/brain/awt118.
Santangelo, G., Cuoco, S., Pellecchia, M. T., Erro, R., Barone, P., & Picillo, M. (2018). Comparative cognitive and neuropsychiatric profiles between Parkinson’s disease, multiple system atrophy and progressive supranuclear palsy. Journal of Neurology, 265(11), 2602–2613. https://doi.org/10.1007/s00415-018-9038-x
Santangelo, G., Cuoco, S., Picillo, M., Erro, R., Squillante, M., Volpe, G., Cozzolino, A., Cicarelli, G., Barone, P., & Pellecchia, M. T. (2020). Evolution of neuropsychological profile in motor subtypes of multiple system atrophy. Parkinsonism & Related Disorders, 70, 67–73. https://doi.org/10.1016/j.parkreldis.2019.12.010
Santos-Santos, M. A., Mandelli, M. L., Binney, R. J., Ogar, J., Wilson, S. M., Henry, M. L., Hubbard, H. I., Meese, M., Attygalle, S., Rosenberg, L., Pakvasa, M., Trojanowski, J. Q., Grinberg, L. T., Rosen, H., Boxer, A. L., Miller, B. L., Seeley, W. W., & Gorno-Tempini, M. L. (2016). Features of Patients With Nonfluent/Agrammatic Primary Progressive Aphasia With Underlying Progressive Supranuclear Palsy Pathology or Corticobasal Degeneration. JAMA Neurology, 73(6), 733–742. https://doi.org/10.1001/jamaneurol.2016.0412
Schmahmann, J. D., & Sherman, J. C. (1998). The cerebellar cognitive affective syndrome. Brain: a journal of neurology, 121(Pt 4), 561–579. https://doi.org/10.1093/brain/121.4.561.
Schönecker, S., Hell, F., Bötzel, K., Wlasich, E., Ackl, N., Süßmair, C., German FTLD Consortium, Otto, M., Anderl-Straub, S., Ludolph, A., Kassubek, J., Huppertz, H. J., Diehl-Schmid, J., Riedl, L., Roßmeier, C., Fassbender, K., Lyros, E., Kornhuber, J., Oberstein, T. J., Fliessbach, K., & … Danek, A. (2019). The applause sign in frontotemporal lobar degeneration and related conditions. Journal of Neurology, 266(2), 330–338. https://doi.org/10.1007/s00415-018-9134-y
Siri, C., Duerr, S., Canesi, M., Delazer, M., Esselink, R., Bloem, B. R., et al. (2013). A cross-sectional multicenter study of cognitive and behavioural features in multiple system atrophy patients of the parkinsonian and cerebellar type. Journal of neural transmission (Vienna, Austria: 1996), 120(4), 613–618. https://doi.org/10.1007/s00702-013-0997-x.
Sitek, E. J., Wieczorek, D., Konkel, A., Dąbrowska, M., & Sławek, J. (2017). The pattern of verbal, visuospatial and procedural learning in Richardson variant of progressive supranuclear palsy in comparison to Parkinson’s disease. Psychiatria polska, 51(4), 647–659. https://doi.org/10.12740/PP/OnlineFirst/62804.
Soliveri, P., Monza, D., Paridi, D., Radice, D., Grisoli, M., Testa, D., Savoiardo, M., & Girotti, F. (1999). Cognitive and magnetic resonance imaging aspects of corticobasal degeneration and progressive supranuclear palsy. Neurology, 53(3), 502–507. https://doi.org/10.1212/wnl.53.3.502
Soliveri, P., Monza, D., Paridi, D., Carella, F., Genitrini, S., Testa, D., & Girotti, F. (2000). Neuropsychological follow up in patients with Parkinson’s disease, striatonigral degeneration-type multisystem atrophy, and progressive supranuclear palsy. Journal of Neurology, Neurosurgery, and Psychiatry, 69(3), 313–318. https://doi.org/10.1136/jnnp.69.3.313
Soliveri, P., Piacentini, S., & Girotti, F. (2005). Limb apraxia in corticobasal degeneration and progressive supranuclear palsy. Neurology, 64(3), 448–453. https://doi.org/10.1212/01.WNL.0000150732.92567.BA
Southi, N., Honan, C. A., Hodges, J. R., Piguet, O., & Kumfor, F. (2019). Reduced capacity for empathy in corticobasal syndrome and its impact on carer burden. International Journal of Geriatric Psychiatry, 34(3), 497–503. https://doi.org/10.1002/gps.5045
Stamelou, M., & Bhatia, K. (2014). Dementia in Parkinson’s Disease and Atypical Parkinsonism. In M. Merello & S. Starkstein (Eds.), Movement Disorders in Dementias (pp. 179–197). Springer.
Stankovic, I., Krismer, F., Jesic, A., Antonini, A., Benke, T., Brown, R. G., Burn, D. J., Holton, J. L., Kaufmann, H., Kostic, V. S., Ling, H., Meissner, W. G., Poewe, W., Semnic, M., Seppi, K., Takeda, A., Weintraub, D., Wenning, G. K., & Movement Disorders Society MSA (MODIMSA) Study Group. (2014). Cognitive impairment in multiple system atrophy: A position statement by the Neuropsychology Task Force of the MDS Multiple System Atrophy (MODIMSA) study group. Movement Disorders: Official Journal of the Movement Disorder Society, 29(7), 857–867. https://doi.org/10.1002/mds.25880
Sulena, G., & D., Sharma, A. K., & Kumar, N. (2017). Clinical Profile of Cognitive Decline in Patients with Parkinson’s Disease, Progressive Supranuclear Palsy, and Multiple System Atrophy. Journal of Neurosciences in Rural Practice, 8(4), 562–568. https://doi.org/10.4103/jnrp.jnrp_154_17
Teichmann, M., Epelbaum, S., Samri, D., Levy Nogueira, M., Michon, A., Hampel, H., Lamari, F., & Dubois, B. (2017). Free and Cued Selective Reminding Test - accuracy for the differential diagnosis of Alzheimer’s and neurodegenerative diseases: A large-scale biomarker-characterized monocenter cohort study (ClinAD). Alzheimer’s & Dementia: THe Journal of the Alzheimer’s Association, 13(8), 913–923. https://doi.org/10.1016/j.jalz.2016.12.014
Tessitore, A., Giordano, A., Caiazzo, G., Corbo, D., De Micco, R., Russo, A., Liguori, S., Cirillo, M., Esposito, F., & Tedeschi, G. (2014). Clinical correlations of microstructural changes in progressive supranuclear palsy. Neurobiology of Aging, 35(10), 2404–2410. https://doi.org/10.1016/j.neurobiolaging.2014.03.028
Testa, D., Fetoni, V., Soliveri, P., Musicco, M., Palazzini, E., & Girotti, F. (1993). Cognitive and motor performance in multiple system atrophy and Parkinson’s disease compared. Neuropsychologia, 31(2), 207–210. https://doi.org/10.1016/0028-3932(93)90048-5
Tomlinson, C. L., Stowe, R., Patel, S., Rick, C., Gray, R., & Clarke, C. E. (2010). Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Movement Disorders: Official Journal of the Movement Disorder Society, 25(15), 2649–2653. https://doi.org/10.1002/mds.23429
Tse, N. Y., Chen, Y., Irish, M., Cordato, N. J., Landin-Romero, R., Hodges, J. R., Piguet, O., & Ahmed, R. M. (2020). Cerebellar contributions to cognition in corticobasal syndrome and progressive supranuclear palsy. Brain Communications, 2(2), fcaa194. https://doi.org/10.1093/braincomms/fcaa194
Turaga, S. P., Mridula, R., & Borgohain, R. (2013). Cerebral glucose metabolism, clinical, neuropsychological, and radiological profile in patients with corticobasal syndrome. Neurology India, 61(1), 7–11. https://doi.org/10.4103/0028-3886.107916
Vaccaro, M. G., Sarica, A., Quattrone, A., Chiriaco, C., Salsone, M., Morelli, M., & Quattrone, A. (2020). Neuropsychological assessment could distinguish among different clinical phenotypes of progressive supranuclear palsy: A Machine Learning approach. Journal of Neuropsychology. https://doi.org/10.1111/jnp.12232. Advance online publication.
Vanvoorst, W. A., Greenaway, M. C., Boeve, B. F., Ivnik, R. J., Parisi, J. E., Eric Ahlskog, J., Knopman, D. S., Dickson, D. W., Petersen, R. C., Smith, G. E., & Josephs, K. A. (2008). Neuropsychological findings in clinically atypical autopsy confirmed corticobasal degeneration and progressive supranuclear palsy. Parkinsonism & Related Disorders, 14(4), 376–378. https://doi.org/10.1016/j.parkreldis.2007.09.006
Wagshal, D., Sankaranarayanan, S., Guss, V., Hall, T., Berisha, F., Lobach, I., Karydas, A., Voltarelli, L., Scherling, C., Heuer, H., Tartaglia, M. C., Miller, Z., Coppola, G., Ahlijanian, M., Soares, H., Kramer, J. H., Rabinovici, G. D., Rosen, H. J., Miller, B. L., & Boxer, A. L. (2015). Divergent CSF τ alterations in two common tauopathies: Alzheimer’s disease and progressive supranuclear palsy. Journal of Neurology, Neurosurgery, and Psychiatry, 86(3), 244–250. https://doi.org/10.1136/jnnp-2014-308004
Whitwell, J. L., Jack, C. R., Jr., Boeve, B. F., Parisi, J. E., Ahlskog, J. E., Drubach, D. A., Senjem, M. L., Knopman, D. S., Petersen, R. C., Dickson, D. W., & Josephs, K. A. (2010). Imaging correlates of pathology in corticobasal syndrome. Neurology, 75(21), 1879–1887. https://doi.org/10.1212/WNL.0b013e3181feb2e8
Yang, Y., Tang, B. S., & Guo, J. F. (2016). Parkinson’s disease and cognitive impairment. Parkinson’s Disease, 2016, 6734678. https://doi.org/10.1155/2016/6734678.
Yildiz, F. G., Saka, E., Elibol, B., & Temucin, C. M. (2018). Modulation of cerebellar-cortical connections in multiple system atrophy type c by cerebellar repetitive transcranial magnetic stimulation. Neuromodulation: Journal of the International Neuromodulation Society, 21(4), 402–408. https://doi.org/10.1111/ner.12589
Yoon, J. H., Lee, J. E., Yong, S. W., Moon, S. Y., & Lee, P. H. (2014). The mild cognitive impairment stage of dementia with Lewy bodies and Parkinson disease: A comparison of cognitive profiles. Alzheimer Disease and Associated Disorders, 28(2), 151–155. https://doi.org/10.1097/WAD.0000000000000007
Yousaf, T., Dervenoulas, G., Valkimadi, P. E., & Politis, M. (2019). Neuroimaging in Lewy body dementia. Journal of Neurology, 266(1), 1–26. https://doi.org/10.1007/s00415-018-8892-x
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Author information
Authors and Affiliations
Contributions
Conceptualization and Design: Simona Raimo, Mariachiara Gaita, Maria Cropano, Giusi Mautone, Alfonsina D’Iorio; Acquisition of Data: Simona Raimo, Mariachiara Gaita, Maria Cropano, Giusi Mautone; Formal analysis and investigation: Simona Raimo, Mariachiara Gaita, Maria Cropano, Giusi Mautone, Luigi Trojano, Gabriella Santangelo; Writing—original draft preparation: Simona Raimo, Mariachiara Gaita, Maria Cropano, Alfonsina D’Iorio; Writing—review and editing: Simona Raimo, Mariachiara Gaita, Maria Cropano, Luigi Trojano, Gabriella Santangelo.
Corresponding author
Ethics declarations
Conflicts of Interest/Competing Interests
None.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Raimo, S., Gaita, M., Cropano, M. et al. The Cognitive Profile of Atypical Parkinsonism: A Meta-Analysis. Neuropsychol Rev 33, 514–543 (2023). https://doi.org/10.1007/s11065-022-09551-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11065-022-09551-6