Abstract
Cognitive impairment and dementia are common non-motor symptoms in Parkinson’s disease (PD). To elucidate the potentially typical progression of cognitive decline in PD and its variation, we retrospectively surveyed neuropsychological data obtained at the Parkinson-Klinik Ortenau, Germany in the years 1996–2015. Many of the patients in the surveyed period were repeatedly admitted to our clinic and we were thus able to compile neuropsychological re-test data for 252 patients obtained at varying time intervals. Neuropsychological testing was conducted with the NAI (Nürnberger Alters-Inventar). This battery provides sub-tests that examine cognitive processing speed, executive function, working memory, and verbal/visual memory functions. The re-test time span varied across patients from below 1 year up to about 12 years. Most patients were seen twice, but some patients were tested up to eight times. The steepest rates of cognitive decline were observed for the NAI sub-tests Trail-Making, Maze Test, and Stroop-Word Reading/Color Naming. Intermediate rates of decline were found for Digit Span, Word List—Immediate Recall, and Picture Test. Stroop Test—Interference, Word List—Delayed Recognition, and Figure Test exhibited the slowest decline rates. We did not observe a significant effect of age at diagnosis or gender on the rate of decline. In sum, this study retrospectively evaluated cognitive decline in a sample of patients with PD. Our data suggest a broad cognitive decline that particularly affects the cognitive capacities for processing speed, executive functions, and immediate memory functions.
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Abbreviations
- AD:
-
Alzheimer’s disease
- DLB:
-
Dementia with Lewy bodies
- MCI:
-
Mild cognitive impairment
- PD:
-
Parkinson’s disease
- PDD:
-
Parkinson’s disease dementia
References
Aarsland D, Andersen K, Larsen JP, Lolk A, Kragh-Sorensen P (2003) Prevalence and characteristics of dementia in Parkinson disease: an 8-year prospective study. Arch Neurol 60:387–392. https://doi.org/10.1001/archneur.60.3.387
Aarsland D, Bronnick K, Williams-Gray C, Weintraub D, Marder K, Kulisevsky J, et al (2010) Mild cognitive impairment in Parkinson disease: a multicenter pooled analysis. Neurology 21:1062–1069. https://doi.org/10.1212/WNL.0b013e3181f39d0e
Aretouli E, Brandt J (2010) Episodic memory in dementia: characteristics of new learning that differentiate Alzheimer’s, Huntington’s, and Parkinson’s diseases. Arch Clin Neuropsychol 25:296–309. https://doi.org/10.1093/arclin/acq038
Becker S, Bäumer A, Maetzler W, Nussbaum S, Tkaczynska Z, Sulzer P, Timmers M, Van Nueten L, Salvadore G, Brockmann K, Streffer J, Berg D, Liepelt-Scarfone I (2020) Association of cognitive activities of daily living (ADL) function and nonmotor burden in nondemented Parkinson’s disease patients. Neuropsychology 34:447–455. https://doi.org/10.1037/neu0000627
Braams BR, Duijenvoorde ACK, Peper JS, Crone EA (2015) Longitudinal changes in adolescent risk-taking: a comprehensive study of neural responses to rewards, pubertal development, and risk-taking behavior. J Neurosci 35:7226–7238. https://doi.org/10.1523/jneurosci.4764-14.2015
Bronnick K, Emre M, Lane R, Tekin S, Aarsland D (2007) Profile of cognitive impairment in dementia associated with Parkinson’s disease compared with Alzheimer’s disease. J Neurolog Neurosurg Psychiatry 78:1064–1068. https://doi.org/10.1136/jnnp.2006.108076
Cnaan A, Laird NM, Slasor P (1997) Tutorial in biostatistics: using the general linear mixed model to analyse unbalanced repeated measures and longitudinal data. Stat Med 16:2349–2380. https://doi.org/10.1002/(sici)1097-0258(19971030)16:20%3c2349::aid-sim667%3e3.0.co;2-e
Dubois B, Burn D, Goetz C et al (2007) Diagnostic procedures for Parkinson’s disease dementia: recommendations from the movement disorder society task force. Mov Disord 22:2314–2324. https://doi.org/10.1002/mds.21844
Emre M, Aarsland D, Brown R et al (2007) Clinical diagnostic criteria for dementia associated with Parkinson’s disease. Mov Disord 22:1689–1707. https://doi.org/10.1002/mds.21507
Emre M, Poewe W, De Deyn PP, Barone P, Kulisevsky J, Pourcher E et al (2014) Long-term safety of rivastigmine in Parkinson disease dementia: an open-label, randomized study. Clin Neuropharmacol 37:9–16. https://doi.org/10.1097/wnf.0000000000000010
Field A, Miles J, Field Z (2012) Discovering statistics using R. Sage Publications, London
Garcia TP, Marder K (2017) Statistical approaches to longitudinal data analysis in neurodegenerative diseases: Huntington’s disease as a model. Curr Neurol Neurosci Rep 17:14. https://doi.org/10.1007/s11910-017-0723-4
Gibb WRG, Lees AJ (1988) The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson’s disease. J Neurol Neurosurg Psychiatry 51:745–752. https://doi.org/10.1136/jnnp.51.6.745
Goldman JG, Holly W, Stebbins G, Bernard B, Goetz CG (2013) Clinical differences among mild cognitive impairment subtypes in Parkinson’s disease. Mov Disord 28:1972–1979. https://doi.org/10.1002/mds.25062
Green J, McDonald WM, Vitek JL, Evatt M, Freeman A, Haber M et al (2002) Cognitive impairments in advanced PD without dementia. Neurology 59:1320–1324. https://doi.org/10.1212/01.wnl.0000031426.21683.e2
Hely MA, Morris JGL, Reid WGJ, Trafficante R (2005) Sydney multicenter of Parkinson’s disease: non-L-dopa-responsive problems dominate at 15 years. Mov Disord 20:190–199. https://doi.org/10.1002/mds.20324
Hely MA, Reid WGJ, Adena MA, Halliday GM, Morris JGL (2008) The Sydney multicenter of Parkinson’s disease: the inevitability of dementia at 20 years. Mov Disord 23:837–844. https://doi.org/10.1002/mds.21956
Kalbe E, Rehberg SP, Heber I et al (2016) Subtypes of mild cognitive impairment in patients with Parkinson’s disease: evidence from the LANDSCAPE study. J Neurol Neurosurg Psychiatry 87:1099–1105. https://doi.org/10.1136/jnnp-2016-313838
Kalbe E, Aarsland D, Folkerts A-K (2018) Cognitive interventions in Parkinson’s disease: where we want to go within 20 years. J Park Dis 8:S107–S113. https://doi.org/10.3233/jpd-181473
Kang H (2013) The prevention and handling of the missing data. Korean J Anesthesiol 64:402–406. https://doi.org/10.4097/kjae.2013.64.5.402
Kang GA, Bronstein JM, Masterman DL, Redeling M, Crum JA, Ritz B (2005) Clinical characteristics in early Parkinson’s disease in a central California based population-based study. Mov Disord 20:1133–1142. https://doi.org/10.1002/mds.20513
Kehagia AA, Barker RA, Robbins TW (2010) Neuropsychological and clinical heterogeneity of cognitive impairment and dementia in patients with Parkinson’s disease. The Lancet Neurology 9:1200–1213. https://doi.org/10.1016/S1474-4422(10)70212-X
Koerts J, Tucha L, Lange KW, Tucha O (2013) The influence of cognitive reserve on cognition in Parkinson’s disease. J Neural Transm 12:593–593. https://doi.org/10.1007/s00702-012-0916-6
Kramberger MG, Auestad B, Garcia-Ptacek S, Abdelnour C, Olmo JG, Walker Z et al (2017) Long-term cognitive decline in dementia with Lewy bodies in a large multicenter, international cohort. J Alzheimers Dis 57:787–795. https://doi.org/10.3233/JAD-161109
Lawson RA, Yarnall AJ, Duncan DP, Khoo TK, Williams-Gray CH, Barker RA et al (2017) Stability of mild cognitive impairment in newly diagnosed Parkinson’s disease. J Neurol Neurosurg Psychiatry 88:648–652. https://doi.org/10.1136/jnnp-2016-315099
Leroi I, McDonald K, Pantula H, Harbishettar V (2012) Cognitive impairment in Parkinson disease: impact on quality of life, disability, and caregiver burden. J Geriatr Psychiatry Neurol 25:208–214. https://doi.org/10.1177/0891988712464823
Leung IHK, Walton CC, Hallock H, Lewis SJG, Velenzuela M, Lampit A (2015) Cognitive training in Parkinson disease. Neurology 85:1843–1851. https://doi.org/10.1212/wnl.0000000000002145
Liepelt-Scarfone I, Gräber S, Feseker A, Baysal G, Godau J, Gaenslen A, Maetzler W, Berg D (2011) Influence of different cut-off values on the diagnosis of mild cognitive impairment in Parkinson’s disease. Park Dis 2011:540843. https://doi.org/10.4061/2011/540843
Liepelt-Scarfone I, Gräber S, Fruhmann Berger M, Feseker A, Baysal G, Csoti I et al (2012) Cognitive profiles in Parkinson’s disease and their relation to dementia: a data-driven approach. Int J Alzheimer Dis 2012:910757. https://doi.org/10.1155/2012/910757
Liepelt-Scarfone I, Gräber S, Kalbe E, Riedel O, Ringendahl H, Schmidt N, Witt K, Roeske S (2021) Guidelines for the neuropsychological assessment of patients with Parkinson’s Disease. Fortschr Neurol Psychiatr. https://doi.org/10.1055/a-1099-9332
Litvan I, Goldman JG, Troster AI et al (2012) Diagnostic criteria for mild cognitive impairment in Parkinson’s disease: movement Disorder Society task force guidelines. Mov Disord 27:349–356. https://doi.org/10.1002/mds.24893
Locascio JJ, Atri A (2011) An overview of longitudinal data analysis methods for neurological research. Dement Geriatr Cogn Disord Extra 1:330–357. https://doi.org/10.1159/000330228
Martinez-Horta S, Kulisevsky J (2019) Mild cognitive impairment in Parkinson’s disease. J Neural Transm 126:897–904. https://doi.org/10.1007/s00702-019-02003-1
Muslimovic D, Schmand B, Speelman JD, De Haan RJ (2007) Course of cognitive decline in Parkinson’s disease: a meta-analysis. J Int Neuropsychol Soc 13:920–932. https://doi.org/10.1017/S1355617707071160
Orgeta V, McDonald KR, Poliakoff E, Hindle JV, Clare L, Leroi I (2020) Cognitive training interventions for dementia and mild cognitive impairment in Parkinson’s disease. Cochrane Database Syst Rev 2020:CD011961. https://doi.org/10.1002/14651858.cd011961.pub2
Oswald WD, Fleischmann UM (1995) Nürnberger-Alters-Inventar, 3rd edn. Hogrefe, Göttingen
Oswald WD, Fleischmann UM (1999) Nürnberger-Alters-Inventar, 4th edn. Hogrefe, Göttingen
Rau A, Koschel J, Egger K, Jost WH (2021) The final diagnoses of patients with clinically suspected atypical parkinsonian syndromes. Parkinsonism Relat Disord 85:57–58. https://doi.org/10.1016/j.parkreldis.2021.03.001
Reid WGJ, Hely MA, Morris JGL, Halliday GM (2011) Dementia in Parkinson´s disease: A 20-year neuropsychological study (Sydney Multicentre Study). J Neurol Neurosurg Psych 82:1033–1136. https://doi.org/10.1136/jnnp.2010.232678
Roheger M, Kalbe E, Liepelt-Scarfone I (2018) Progression of cognitive decline in Parkinson’s disease. J Parkinsons Dis 8:183–193. https://doi.org/10.3233/jpd-181306
Rongve A, Soennesyn H, Skogseth R, Oesterhus R, Hortobagyi T, Ballard C et al (2016) Cognitive decline in dementia with Lewy bodies: a 5-year prospective cohort study. BMJ Open 6:e010357. https://doi.org/10.1136/bmjopen-2015-010357
Santangelo G, Vitale C, Picillo M, Moccia M, Cuoco S, Longo K (2015) Mild cognitive impairment in newly diagnosed Parkinson’s disease: a longitudinal prospective study. Parkinsonism Relat Disord 21:1219–1226. https://doi.org/10.1016/j.parkreldis.2015.08.024
Svenningsson P, Westman E, Ballard C, Aarsland D (2012) Cognitive impairments in patients with Parkinson’s disease: diagnosis, biomarkers, and treatment. Lancet Neurol 11:697–707. https://doi.org/10.1016/S1474-4422(12)70152-7
van der Burgh HK, Westeneng H-J, Walhout R, van Veenhuijzen THGH, Meier JM et al (2020) Multimodal longitudinal study of structural brain involvement in amyotrophic lateral sclerosis. Neurol 94:e2592–e2604. https://doi.org/10.1212/WNL.0000000000009498
Vasconcellos LFR, Pereira JS (2015) Parkinson’s disease dementia: diagnostic criteria and risk factor review. J Clin Exp Neuropsych 37:988–993. https://doi.org/10.1080/13803395.2015.1073227
Vossius C, Larsen JP, Janvin C, Aarsland D (2011) The economic impact of cognitive impairment in Parkinson’s disease. Mov Disord 26:1541–1544. https://doi.org/10.1002/mds.23661
Weintraub D, Caspell-Garcia C, Simuni T, Cho HR, Coffey CS, Aarsland D et al (2020) Neuropsychiatric symptoms and cognitive abilities over the initial quinquennium of Parkinson disease. Ann Clin Transl Neurol 7:449–461. https://doi.org/10.1002/acn3.51022
Williams-Gray CH, Evans JR, Goris A, Foltynie T, Ban M, Robbins TW, Barker RA (2009) The distinct cognitive syndromes of Parkinson’s disease: 5-year follow-up of the CamPaIGN cohort. Brain 132:2958–2969. https://doi.org/10.1093/brain/awp245
Willis AW, Schootman M, Knug N et al (2012) Predictors of survival in patients with Parkinson disease. Arch Neurol 69:601–607. https://doi.org/10.1001/archneurol.2011.2370
Wills AM, Elm JJ, Ye R, Chou KL, Parashos SA, Hauser RA et al (2016) Cognitive function in 1736 participants in NINDS exploratory trials in PD Long-term Study-1. Parkinsonism Relat Disord 33:127–133. https://doi.org/10.1016/j.parkreldis.2016.10.005
Wojtala J, Heber IA, Neuser P, Heller J, Kalbe E, Rehberg SP et al (2019) Cognitive decline in Parkinson’s disease: the impact of the motor phenotype on cognition. J Neurol Neurosurg Psychiatry 90:171–179. https://doi.org/10.1136/jnnp-2018-319008
Wyman-Chick KA, Martin PK, Weintraub D, Sperling SA, Erickson LO, Manning CA, Barrett MJ (2018) Selection of normative group affects rates of mild cognitive impairment in Parkinson’s disease. Mov Disord 33:839–843. https://doi.org/10.1002/mds.27335
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CFA and WHJ designed and conceptualized the study. CFA, KT, and DE performed data collection and analysis. CFA wrote the first draft of the manuscript; KT, DE, and WHJ made substantial contributions to the writing and editing of the final draft. All authors read and approved the final manuscript.
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WHJ is advisor and speaker for Abbvie, Bial, Desitin, Stada, UCB, and Zambon. CFA, KT, and DE declare that they have no conflict of interest.
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All procedures were in accordance with the ethical guidelines laid down in the Declaration of Helsinki, 1964, and approved by the ethics committee of the State Medical Chamber of Baden-Württemberg, Germany (F-2021-080).
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Altmann, C.F., Trubelja, K., Emmans, D. et al. Time-course of decline in different cognitive domains in Parkinson’s disease: a retrospective study. J Neural Transm 129, 1179–1187 (2022). https://doi.org/10.1007/s00702-021-02441-w
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DOI: https://doi.org/10.1007/s00702-021-02441-w