Examining the Reserve Hypothesis in Parkinson's Disease: A Longitudinal Study.
Parkinson's disease
cohort study
education
progression
reserve
Journal
Movement disorders : official journal of the Movement Disorder Society
ISSN: 1531-8257
Titre abrégé: Mov Disord
Pays: United States
ID NLM: 8610688
Informations de publication
Date de publication:
11 2019
11 2019
Historique:
received:
20
02
2019
revised:
13
08
2019
accepted:
13
08
2019
pubmed:
14
9
2019
medline:
9
7
2020
entrez:
14
9
2019
Statut:
ppublish
Résumé
Whether reserve plays a role in Parkinson's disease (PD) patients has received less attention than in dementia and has been mainly examined in relation with cognitive function. To investigate whether reserve plays a role in the severity and progression of motor, cognitive, and nonmotor PD symptoms by examining whether education level (proxy of reserve) is associated with baseline performance and rate of progression. We used data from a longitudinal cohort of PD patients (≤5-year disease duration at baseline) annually followed up to 5 years (n = 393; 41% women; mean age = 62.3 years, standard deviation = 10.0; mean disease duration = 2.6 years, standard deviation = 1.5). We examined the relationship of education with time to reach Hoehn and Yahr stage ≥3 using Cox regression and with baseline severity and progression of motor (Movement Disorder Society-Unified Parkinson's Disease Rating Scale parts II and III, gait speed), cognitive (Mini-Mental State Examination), and nonmotor (depression, anxiety, nonmotor symptoms scale, quality of life) symptoms using mixed models. Education level was not associated with age at onset or diagnosis. Compared with the low-education group, the incidence of Hoehn and Yahr ≥3.0 was 0.42 times lower (95% confidence interval, 0.22-0.82, P = 0.012) in the high-education group. Higher education was associated with better baseline motor function (P < 0.001), but not with the rate of motor decline (P > 0.15). Similar results were observed for cognition. Education was not associated with nonmotor symptoms. Higher education is associated with better baseline motor/cognitive function in PD, but not with rate of decline, and with a lower risk of reaching Hoehn and Yahr ≥3 during the follow-up. Our observations are consistent with a passive reserve hypothesis for motor/cognitive symptoms. © 2019 International Parkinson and Movement Disorder Society.
Sections du résumé
BACKGROUND
Whether reserve plays a role in Parkinson's disease (PD) patients has received less attention than in dementia and has been mainly examined in relation with cognitive function.
OBJECTIVE
To investigate whether reserve plays a role in the severity and progression of motor, cognitive, and nonmotor PD symptoms by examining whether education level (proxy of reserve) is associated with baseline performance and rate of progression.
METHODS
We used data from a longitudinal cohort of PD patients (≤5-year disease duration at baseline) annually followed up to 5 years (n = 393; 41% women; mean age = 62.3 years, standard deviation = 10.0; mean disease duration = 2.6 years, standard deviation = 1.5). We examined the relationship of education with time to reach Hoehn and Yahr stage ≥3 using Cox regression and with baseline severity and progression of motor (Movement Disorder Society-Unified Parkinson's Disease Rating Scale parts II and III, gait speed), cognitive (Mini-Mental State Examination), and nonmotor (depression, anxiety, nonmotor symptoms scale, quality of life) symptoms using mixed models.
RESULTS
Education level was not associated with age at onset or diagnosis. Compared with the low-education group, the incidence of Hoehn and Yahr ≥3.0 was 0.42 times lower (95% confidence interval, 0.22-0.82, P = 0.012) in the high-education group. Higher education was associated with better baseline motor function (P < 0.001), but not with the rate of motor decline (P > 0.15). Similar results were observed for cognition. Education was not associated with nonmotor symptoms.
CONCLUSIONS
Higher education is associated with better baseline motor/cognitive function in PD, but not with rate of decline, and with a lower risk of reaching Hoehn and Yahr ≥3 during the follow-up. Our observations are consistent with a passive reserve hypothesis for motor/cognitive symptoms. © 2019 International Parkinson and Movement Disorder Society.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1663-1671Informations de copyright
© 2019 International Parkinson and Movement Disorder Society.
Références
de Lau LM, Breteler MM. Epidemiology of Parkinson's disease. Lancet Neurol 2006;5(6):525-535.
Maetzler W, Liepelt I, Berg D. Progression of Parkinson's disease in the clinical phase: potential markers. Lancet Neurol 2009;8(12):1158-1171.
Zahodne LB, Glymour MM, Sparks C, et al. Education does not slow cognitive decline with aging: 12-year evidence from the Victoria Longitudinal Study. J Int Neuropsychol Soc 2011;17(6):1039-1046.
Meng X, D'Arcy C. Education and dementia in the context of the cognitive reserve hypothesis: a systematic review with meta-analyses and qualitative analyses. PloS ONE 2012;7(6):e38268.
Sharp ES, Gatz M. Relationship between education and dementia: an updated systematic review. Alzheimer Dis Assoc Disord 2011;25(4):289-304.
Stern Y. Cognitive reserve. Neuropsychologia 2009;47(10):2015-2028.
Stern Y. What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc 2002;8(3):448-460.
Gottesman RF, Rawlings AM, Sharrett AR, et al. Impact of differential attrition on the association of education with cognitive change over 20 years of follow-up: the ARIC Neurocognitive Study. Am J Epidemiol 2014 ;179(8):956-966.
Wilson RS, Li Y, Aggarwal NT, et al. Education and the course of cognitive decline in Alzheimer disease. Neurology 2004;63(7):1198-1202.
Hall CB, Derby C, LeValley A, Katz MJ, Verghese J, Lipton RB. Education delays accelerated decline on a memory test in persons who develop dementia. Neurology 2007;69(17):1657-1664.
Elbaz A, Vicente-Vytopilova P, Tavernier B, et al. Motor function in the elderly: evidence for the reserve hypothesis. Neurology 2013;81(5):417-426.
Hindle JV, Martyr A, Clare L. Cognitive reserve in Parkinson's disease: a systematic review and meta-analysis. Parkinson Relat Disord 2014;20(1):1-7.
Souza CO, Voos MC, Francato DV, Chien HF, Barbosa ER. Influence of educational status on executive function and functional balance in individuals with Parkinson disease. Cogn Behav Neurol 2013;26(1):6-13.
Kotagal V, Bohnen NI, Muller ML, et al. Educational attainment and motor burden in Parkinson's disease. Mov Disord 2015;30(8):1143-1147.
Sunwoo MK, Hong JY, Lee JJ, Lee PH, Sohn YH. Does education modify motor compensation in Parkinson's disease? J Neurol Sci 2016;362:118-120.
Blume J, Rothenfusser E, Schlaier J, Bogdahn U, Lange M. Educational attainment and motor burden in advanced Parkinson's disease-the emerging role of education in motor reserve. J Neurol Sci 2017;381:141-143.
Corvol JC, Artaud F, Cormier-Dequaire F, et al. Longitudinal analysis of impulse control disorders in Parkinson disease. Neurology 2018 ;91(3):e189-e201.
Li X, Xing Y, Martin-Bastida A, Piccini P, Auer DP. Patterns of grey matter loss associated with motor subscores in early Parkinson's disease. NeuroImage Clin 2018;17:498-504.
Stebbins GT, Goetz CG, Burn DJ, Jankovic J, Khoo TK, Tilley BC. How to identify tremor dominant and postural instability/gait difficulty groups with the Movement Disorder Society Unified Parkinson's Disease Rating Scale: comparison with the Unified Parkinson's Disease Rating Scale. Mov Disord 2013;28(5):668-670.
Zigmond AS, Snaith RP. The Hospital Anxiety and Depression Scale. Acta Psychiatr Scand 1983;67(6):361-370.
Leentjens AF, Dujardin K, Marsh L, Richard IH, Starkstein SE, Martinez-Martin P. 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 2011;26(3):407-415.
Chaudhuri KR, Martinez-Martin P, Schapira AH, et al. International multicenter pilot study of the first comprehensive self-completed nonmotor symptoms questionnaire for Parkinson's disease: the NMSQuest study. Mov Disord 2006;21(7):916-923.
Peto V, Jenkinson C, Fitzpatrick R, Greenhall R. The development and validation of a short measure of functioning and well being for individuals with Parkinson's disease. Qual Life Res 1995;4(3):241-248.
Elbaz A, Artaud F, Dugravot A, Tzourio C, Singh-Manoux A. The gait speed advantage of taller stature is lost with age. Sci Rep 2018;8(1):1485.
Jacqmin-Gadda H, Fabrigoule C, Commenges D, Dartigues JF. A 5-year longitudinal study of the Mini-Mental State Examination in normal aging. Am J Epidemiol 1997;145(6):498-506.
Vivot A, Power MC, Glymour MM, et al. Jump, hop, or skip: modeling practice effects in studies of determinants of cognitive change in older adults. Am J Epidemiol 2016;183(4):302-314.
Benjamini Y, Hochberg Y. Controlling the false discovery rate-a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodol) 1995;57:11.
Storey J. The positive false discovery rate: a Bayesian interpretation and the q-value. Ann Stat 2003;31(6):22.
Nagin DS, Jones BL, Lima Passos V, Tremblay RE. Group-based multi-trajectory modeling. Stat Methods Med Res 2018;27:2015-2023.
Tucker AM, Stern Y. Cognitive reserve in aging. Curr Alzheimer Res 2011;8(4):354-360.
Stern Y. Cognitive reserve: implications for assessment and intervention. Folia Phoniatr Logo 2013;65(2):49-54.
Stringhini S, Carmeli C, Jokela M, et al. Socioeconomic status, non-communicable disease risk factors, and walking speed in older adults: multi-cohort population based study. BMJ 2018;360:k1046.
Fleischman DA, Yang J, Arfanakis K, et al. Physical activity, motor function, and white matter hyperintensity burden in healthy older adults. Neurology 2015;84(13):1294-1300.
Hindle JV, Hurt CS, Burn DJ, et al. The effects of cognitive reserve and lifestyle on cognition and dementia in Parkinson's disease-a longitudinal cohort study. Int J Geriatr Psychiatry 2016;31(1):13-23.
Glymour MM, Weuve J, Berkman LF, Kawachi I, Robins JM. When is baseline adjustment useful in analyses of change? An example with education and cognitive change. Am J Epidemiol 2005;162(3):267-278.
Bezard E, Dovero S, Belin D, et al. Enriched environment confers resistance to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine and cocaine: involvement of dopamine transporter and trophic factors. J Neurosci 2003;23(35):10999-11007.
Faherty CJ, Raviie Shepherd K, Herasimtschuk A, Smeyne RJ. Environmental enrichment in adulthood eliminates neuronal death in experimental parkinsonism. Brain Res Mol Brain Res 2005;134(1):170-179.
Nithianantharajah J, Hannan AJ. Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci 2006;7(9):697-709.
Valenzuela MJ, Breakspear M, Sachdev P. Complex mental activity and the aging brain: molecular, cellular and cortical network mechanisms. Brain Res Rev2007;56(1):198-213.
Lieberman A. Depression in Parkinson's disease-a review. Acta Neurol Scand 2006;113(1):1-8.
Menza MA, Robertson-Hoffman DE, Bonapace AS. Parkinson's disease and anxiety: comorbidity with depression. Biol Psychiatry 1993;34(7):465-470.
Lawson RA, Yarnall AJ, Duncan GW, et al. Cognitive decline and quality of life in incident Parkinson's disease: the role of attention. Parkinson Relat Disord 2016;27:47-53.