Clinical dementia severity associated with ventricular size is differentially moderated by cognitive reserve in men and women

Shraddha Sapkota, Joel Ramirez, Donald T Stuss, Mario Masellis, Sandra E Black, Shraddha Sapkota, Joel Ramirez, Donald T Stuss, Mario Masellis, Sandra E Black

Abstract

Background: Interindividual differences in cognitive reserve (CR) are associated with complex and dynamic clinical phenotypes observed in cognitive impairment and dementia. We tested whether (1) CR early in life (E-CR; measured by education and IQ), (2) CR later in life (L-CR; measured by occupation), and (3) CR panel (CR-P) with the additive effects of E-CR and L-CR, act as moderating factors between baseline ventricular size and clinical dementia severity at baseline and across 2 years. We further examined whether this moderation is differentially represented by sex.

Methods: We examined a longitudinal model using patients (N = 723; mean age = 70.8 ± 9.4 years; age range = 38-90 years; females = 374) from the Sunnybrook Dementia Study. The patients represented Alzheimer's disease (n = 439), mild cognitive impairment (n = 77), vascular cognitive impairment (n = 52), Lewy body disease (n = 30), and frontotemporal dementia (n = 125). Statistical analyses included (1) latent growth modeling to determine how clinical dementia severity changes over 2 years (measured by performance on the Dementia Rating Scale), (2) confirmatory factor analysis to establish a baseline E-CR factor, and (3) path analysis to predict dementia severity. Baseline age (continuous) and Apolipoprotein E status (ɛ4-/ɛ4+) were included as covariates.

Results: The association between higher baseline ventricular size and dementia severity was moderated by (1) E-CR and L-CR and (2) CR-P. This association was differentially represented in men and women. Specifically, men in only the low CR-P had higher baseline clinical dementia severity with larger baseline ventricular size. However, women in the low CR-P showed the (1) highest baseline dementia severity and (2) fastest 2-year decline with larger baseline ventricular size.

Conclusions: Clinical dementia severity associated with ventricular size may be (1) selectively moderated by complex and additive CR networks and (2) differentially represented by sex.

Trials registration: ClinicalTrials.gov, NCT01800214 . Registered on 27 February 2013.

Keywords: Cognitive impairment; Cognitive reserve; Dementia; Sex; Sunnybrook Dementia Study; Ventricular size.

Conflict of interest statement

Ethics approval and consent to participate

All of this research has been approved continuously by relevant institutional review boards. Certificates are available from and on file at Sunnybrook Health Sciences Centre. All participants have completed and signed informed consent forms.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Conceptual model for baseline ventricular size on baseline Dementia Rating Scale (DRS) performance and 2-year change (A) independently, (B) as moderated by early-life cognitive reserve (E-CR), (C) as moderated by later-life cognitive reserve (L-CR), and (D) as moderated by cognitive reserve panel (CR-P = E-CR + L-CR). Apolipoprotein E (APOE) genotype and baseline age are included as covariates in all analyses. i Intercept, s Slope, T Time point, WAIS Wechsler Adult Intelligence Scale, NART North American Reading Test-Revised
Fig. 2
Fig. 2
Predicted growth curves for baseline ventricular size on Dementia Rating Scale performance and 2-year change as moderated by cognitive reserve panel (early-life cognitive reserve + later-life cognitive reserve) in the overall group: (a) low, (b) intermediate, and (c) high
Fig. 3
Fig. 3
Predicted growth curves for baseline ventricular size on Dementia Rating Scale performance and 2-year change as moderated by cognitive reserve panel (early-life cognitive reserve + later-life cognitive reserve) in men and women: (a) low, (b) intermediate, and (c) high

References

    1. Viswanathan A, Rocca WA, Tzourio C. Vascular risk factors and dementia: how to move forward? Neurology. 2009;72:368–374. doi: 10.1212/01.wnl.0000341271.90478.8e.
    1. Rahimi J, Kovacs GG. Prevalence of mixed pathologies in the aging brain. Alzheimers Res Ther. 2014;6:82. doi: 10.1186/s13195-014-0082-1.
    1. Windle G. What is resilience? A review and concept analysis. Rev Clin Gerontol. 2011;21:152–169. doi: 10.1017/S0959259810000420.
    1. Kaup AR, Nettiksimmons J, Harris TB, Sink KM, Satterfield S, Metti AL, et al. Cognitive resilience to apolipoprotein E ε4. JAMA Neurol. 2015;72:340. doi: 10.1001/jamaneurol.2014.3978.
    1. Stern Y. An approach to studying the neural correlates of reserve. Brain Imaging Behav. 2017;11:410–416. doi: 10.1007/s11682-016-9566-x.
    1. Jones RN, Manly J, Glymour MM, Rentz DM, Jefferson AL, Stern Y. Conceptual and measurement challenges in research on cognitive reserve. J Int Neuropsychol Soc. 2011;17:593–601. doi: 10.1017/S1355617710001748.
    1. Stern Y, Gurland B, Tatemichi TK, Tang MX, Wilder D, Mayeux R. Influence of education and occupation on the incidence of Alzheimer’s disease. JAMA. 1994;271:1004–1010. doi: 10.1001/jama.1994.03510370056032.
    1. Stern Y, Albert S, Tang MX, Tsai WY. Rate of memory decline in AD is related to education and occupation: cognitive reserve? Neurology. 1999;53:1942–1947. doi: 10.1212/WNL.53.9.1942.
    1. Scarmeas N, Stern Y. Cognitive reserve and lifestyle. J Clin Exp Neuropsychol. 2003;25:625–633. doi: 10.1076/jcen.25.5.625.14576.
    1. M. Tucker A, Stern Y. Cognitive reserve in aging. Curr Alzheimer Res. 2011;8:354–360. doi: 10.2174/156720511795745320.
    1. Ceci S. How much does schooling influence general intelligence and its cognitive components? A reassessment of the evidence. Dev Psychol. 1991;27:703–722. doi: 10.1037/0012-1649.27.5.703.
    1. Stern Y. Cognitive reserve: implications for assessment and intervention. Folia Phoniatr. Logop. NIH Public Access; 2013;65:49–54.
    1. Andersen K, Launer LJ, Dewey ME, Letenneur L, Ott A, Copeland JR, et al. Gender differences in the incidence of AD and vascular dementia: the EURODEM studies. Neurology. 1999;53:1992–1997. doi: 10.1212/WNL.53.9.1992.
    1. Miller IN, Cronin-Golomb A. Gender differences in Parkinson’s disease: clinical characteristics and cognition. Mov Disord. 2010;25:2695–2703. doi: 10.1002/mds.23388.
    1. Ruitenberg A, Ott A, van Swieten JC, Hofman A, Breteler MM. Incidence of dementia: does gender make a difference? Neurobiol Aging. 2001;22:575–580. doi: 10.1016/S0197-4580(01)00231-7.
    1. Perneczky R, Diehl-Schmid J, Förstl H, Drzezga A, Kurz A. Male gender is associated with greater cerebral hypometabolism in frontotemporal dementia: evidence for sex-related cognitive reserve. Int J Geriatr Psychiatry. 2007;22:1135–1140. doi: 10.1002/gps.1803.
    1. Laws KR, Irvine K, Gale TM. Sex differences in cognitive impairment in Alzheimer’s disease. World J Psychiatry. 2016;6:54–65. doi: 10.5498/wjp.v6.i1.54.
    1. Janicki SC, Schupf N. Hormonal influences on cognition and risk for Alzheimer’s disease. Curr Neurol Neurosci Rep. 2010;10:359–366. doi: 10.1007/s11910-010-0122-6.
    1. Sundermann EE, Biegon A, Rubin LH, Lipton RB, Mowrey W, Landau S, et al. Better verbal memory in women than men in MCI despite similar levels of hippocampal atrophy. Neurology. 2006;86:1368–1376. doi: 10.1212/WNL.0000000000002570.
    1. Sundermann EE, Maki PM, Rubin LH, Lipton RB, Landau S, Biegon A, et al. Female advantage in verbal memory. Neurology. 2016;87:1916–1924. doi: 10.1212/WNL.0000000000003288.
    1. Breteler MMB, Van Amerongen NM, Van Swieten JC, Claus JJ, Grobbee DE, Van Gijn J, et al. Cognitive correlates of ventricular enlargement and cerebral white matter lesions on magnetic resonance imaging the Rotterdam study. Stroke. 1994;25:1109–1115. doi: 10.1161/01.STR.25.6.1109.
    1. Nestor SM, Rupsingh R, Borrie M, Smith M, Accomazzi V, Wells JL, et al. Ventricular enlargement as a possible measure of Alzheimer’s disease progression validated using the Alzheimer’s disease neuroimaging initiative database. Brain. 2008;131:2443–2454. doi: 10.1093/brain/awn146.
    1. Luxenberg JS, Haxby JV, Creasey H, Sundaram M, Rapoport SI. Rate of ventricular enlargement in dementia of the Alzheimer type correlates with rate of neuropsychological deterioration. Neurology. 1987;37:1135–1140. doi: 10.1212/WNL.37.7.1135.
    1. Barulli D, Stern Y. Efficiency, capacity, compensation, maintenance, plasticity: emerging concepts in cognitive reserve. Trends Cogn Sci. 2013;17:502–509. doi: 10.1016/j.tics.2013.08.012.
    1. Yokoyama JS, Evans DS, Coppola G, Kramer JH, Tranah GJ, Yaffe K. Genetic modifiers of cognitive maintenance among older adults. Hum Brain Mapp. 2014;35:4556–4565. doi: 10.1002/hbm.22494.
    1. Ansiau D, Marquié JC, Soubelet A, Ramos S. Relationships between cognitive characteristics of the job, age, and cognitive efficiency. Int Congr Ser. 2005;1280:43–48. doi: 10.1016/j.ics.2005.01.020.
    1. Chapko D, McCormack R, Black C, Staff R, Murray A. Life-course determinants of cognitive reserve (CR) in cognitive aging and dementia – a systematic literature review. Aging Ment Health. 2017. 10.1080/13607863.2017.1348471.
    1. Potter GG, Helms MJ, Plassman BL. Associations of job demands and intelligence with cognitive performance among men in late life. Neurology. 2008;70:1803–1808. doi: 10.1212/01.wnl.0000295506.58497.7e.
    1. Baldivia B, Baldivia B, Andrade VM, Francisco O, Bueno A. Contribution of education, occupation and cognitively stimulating activities to the formation of cognitive reserve. Dement Neuropsychol. 2008;2:173–182. doi: 10.1590/S1980-57642009DN20300003.
    1. Stern Y. Cognitive reserve and Alzheimer disease. Alzheimer Dis Assoc Disord. 2006;20:112–117. doi: 10.1097/01.wad.0000213815.20177.19.
    1. Bozzali M, Dowling C, Serra L, Spanò B, Torso M, Marra C, et al. The impact of cognitive reserve on brain functional connectivity in Alzheimer’s disease. J Alzheimers Dis. 2015;44:243–250. doi: 10.3233/JAD-141824.
    1. Elbejjani M, Fuhrer R, Abrahamowicz M, Mazoyer B, Crivello F, Tzourio C, et al. Life-course socioeconomic position and hippocampal atrophy in a prospective cohort of older adults. Psychosom Med. 2017;79:14–23. doi: 10.1097/PSY.0000000000000365.
    1. Serra L, Musicco M, Cercignani M, Torso M, Spanò B, Mastropasqua C, et al. Cognitive reserve and the risk for Alzheimer’s disease: a longitudinal study. Neurobiol Aging. 2015;36:592–600. doi: 10.1016/j.neurobiolaging.2014.10.010.
    1. Negash S, Xie S, Davatzikos C, Clark CM, Trojanowski JQ, Shaw LM, et al. Cognitive and functional resilience despite molecular evidence of Alzheimer’s disease pathology. Alzheimers Dement. 2013;9:e89–e95. doi: 10.1016/j.jalz.2012.01.009.
    1. Latimer CS, Keene CD, Flanagan ME, Hemmy LS, Lim KO, White LR, et al. Resistance to Alzheimer disease neuropathologic changes and apparent cognitive resilience in the Nun and Honolulu-Asia aging studies. J Neuropathol Exp Neurol. 2017;76:458–466. doi: 10.1093/jnen/nlx030.
    1. Nettiksimmons J, Harvey D, Brewer J, Carmichael O, DeCarli C, Jack CR, et al. Subtypes based on cerebrospinal fluid and magnetic resonance imaging markers in normal elderly predict cognitive decline. Neurobiol Aging. 2010;31:1419–1428. doi: 10.1016/j.neurobiolaging.2010.04.025.
    1. Ruan Q, D’Onofrio G, Sancarlo D, Bao Z, Greco A, Yu Z. Potential neuroimaging biomarkers of pathologic brain changes in mild cognitive impairment and Alzheimer’s disease: a systematic review. BMC Geriatr. 2016;16:104. doi: 10.1186/s12877-016-0281-7.
    1. Ewers M, Sperling RA, Klunk WE, Weiner MW, Hampel H. Neuroimaging markers for the prediction and early diagnosis of Alzheimer’s disease dementia. Trends Neurosci. 2011;34:430–442. doi: 10.1016/j.tins.2011.05.005.
    1. Jack CR, Shiung MM, Weigand SD, O’Brien PC, Gunter JL, Boeve BF, et al. Brain atrophy rates predict subsequent clinical conversion in normal elderly and amnestic MCI. Neurology. 2005;65:1227–1231. doi: 10.1212/01.wnl.0000180958.22678.91.
    1. Carlson NE, Moore MM, Dame A, Howieson D, Silbert LC, Quinn JF, et al. Trajectories of brain loss in aging and the development of cognitive impairment. Neurology. 2008;70:828–833. doi: 10.1212/01.wnl.0000280577.43413.d9.
    1. Carmichael OT, Kuller LH, Lopez OL, Thompson PM, Dutton RA, Lu A, et al. Ventricular volume and dementia progression in the cardiovascular health study. Neurobiol Aging. 2007;28:389–397. doi: 10.1016/j.neurobiolaging.2006.01.006.
    1. Hua X, Hibar DP, Lee S, Toga AW, Jack CR, Jr, Weiner MW, et al. Sex and age differences in atrophic rates: an ADNI study with N=1368 MRI scans. Neubiol Aging. 2010;31:1463–1480. doi: 10.1016/j.neurobiolaging.2010.04.033.
    1. Gutman BA, Hua X, Rajagopalan P, Chou YY, Wang Y, Yanovsky I, et al. Maximizing power to track Alzheimer’s disease and MCI progression by LDA-based weighting of longitudinal ventricular surface features. Neuroimage. 2013;70:386–401. doi: 10.1016/j.neuroimage.2012.12.052.
    1. Shay KA, Duke LW, Conboy T, Harrell LE, Callaway R, Folks DG. The clinical validity of the Mattis dementia rating scale in staging Alzheimer’s dementia. Top Geriatr. 1991;4:18–25. doi: 10.1177/089198879100400104.
    1. Rascovsky K, Salmon DP, Hansen LA, Galasko D. Distinct cognitive profiles and rates of decline on the Mattis Dementia Rating Scale in autopsy-confirmed frontotemporal dementia and Alzheimer’s disease. J Int Neuropsychol Soc. 2008;14:373–383. doi: 10.1017/S135561770808051X.
    1. Nestor SM, Mišić B, Ramirez J, Zhao J, Graham SJ, NPLG V, et al. Small vessel disease is linked to disrupted structural network covariance in Alzheimer’s disease. Alzheimers Dement. 2017;13:749–760. doi: 10.1016/j.jalz.2016.12.007.
    1. McKhann GM, Knopman DS, Chertkow H, e a. The diagnosis of dementia due to Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic. Alzheimers Dement. 2011;7:263–269. doi: 10.1016/j.jalz.2011.03.005.
    1. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM. Clinical diagnosis of Alzheimer’s disease: report of the NINCDS-ADRDA work group under the auspices of Department of Health and Human Services Task Force on Alzheimer’s disease. Neurology. 1984;34:939–944. doi: 10.1212/WNL.34.7.939.
    1. Petersen RC. Mild cognitive impairment as a diagnostic entity. J Intern Med. 2004;256:183–194. doi: 10.1111/j.1365-2796.2004.01388.x.
    1. Winblad B, Palmer K, Kivipelto M, Jelic V, Fratiglioni L, Wahlund LO, et al. Mild cognitive impairment - beyond controversies, towards a consensus: report of the international working group on mild cognitive impairment. J Intern Med. 2004;256:240–246. doi: 10.1111/j.1365-2796.2004.01380.x.
    1. Román GC, Tatemichi TK, Erkinjuntti T, Cummings JL, Masdeu JC, Garcia JH, et al. Vascular dementia: diagnostic criteria for research studies: report of the NINDS-AIREN international workshop. Neurology. 1993;43:250–260. doi: 10.1212/WNL.43.2.250.
    1. McKeith IG, Dickson DW, Lowe J, Emre M, O’Brien JT, Feldman H, et al. Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium. Neurology. 2005;65:1863–1872. doi: 10.1212/01.wnl.0000187889.17253.b1.
    1. Gorno-Tempini ML, Hillis AE, Weintraub S, Kertesz A, Mendez M, Cappa SF, et al. Classification of primary progressive aphasia and its variants. Neurology. 2011;76:1006–1014. doi: 10.1212/WNL.0b013e31821103e6.
    1. Rascovsky K, Hodges JR, Knopman D, Mendez MF, Kramer JH, Neuhaus J, et al. Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. Brain. 2011;134:2456–2477. doi: 10.1093/brain/awr179.
    1. Ramirez J, Gibson E, Quddus A, Lobaugh NJ, Feinstein A, Levine B, et al. Lesion explorer: a comprehensive segmentation and parcellation package to obtain regional volumetrics for subcortical hyperintensities and intracranial tissue. Neuroimage. 2011;54:963–973. doi: 10.1016/j.neuroimage.2010.09.013.
    1. Ramirez J, McNeely AA, Scott CJ, Stuss DT, Black SE. Subcortical hyperintensity volumetrics in Alzheimer’s disease and normal elderly in the Sunnybrook Dementia Study: correlations with atrophy, executive function, mental processing speed, and verbal memory. Alzheimers Res Ther. 2014;6:49. doi: 10.1186/alzrt279.
    1. Dade LA, Gao FQ, Kovacevic N, Roy P, Rockel C, O’Toole CM, et al. Semiautomatic brain region extraction: a method of parcellating brain regions from structural magnetic resonance images. Neuroimage. 2004;22:1492–1502. doi: 10.1016/j.neuroimage.2004.03.023.
    1. Satz P, Cole MA, Hardy DJ, Rassovsky Y. Brain and cognitive reserve: mediator(s) and construct validity, a critique. J Clin Exp Neuropsychol. 2011;33:121–130. doi: 10.1080/13803395.2010.493151.
    1. Harada CN, Natelson Love MC, Triebel KL. Normal cognitive aging. Clin Geriatr Med. 2013;29:737–752. doi: 10.1016/j.cger.2013.07.002.
    1. Hollingshead Four Factor Index of Socioeconomic Status. Yale J Sociol. 1975;8:21–52.
    1. Wechsler D. Manual for the Wechsler Adult Intelligence Scale. Corp: New York: Psychological; 1955.
    1. Nelson HE. The National Adult Reading Test (NART): test manual. Windsor: NFER-Nelson; 1982.
    1. Springer MV, McIntosh AR, Winocur G, Grady CL. The relation between brain activity during memory tasks and years of education in young and older adults. Neuropsychology. 2005;19:181–192. doi: 10.1037/0894-4105.19.2.181.
    1. Mattis S. Dementia rating scale. Lutz: Psychological Assessment Resources; 1988.
    1. Meiran N, Stuss DT, Guzman DA, Lafleche G, Willmer J. Diagnosis of dementia: methods for interpretation of scores of 5 neuropsychological tests. Arch Neurol. 1996;53:1043–1054. doi: 10.1001/archneur.1996.00550100129022.
    1. Monsch AU, Bondi MW, Salmon DP, Butters N, Thal LJ, Hansen LA, et al. Clinical validity of the Mattis Dementia Rating Scale in detecting dementia of the Alzheimer type: a double cross-validation and application to a community-dwelling sample. Arch. Neurol. 1995;52:899–904.
    1. Muthén L, Muthén B. Mplus user’s guide. 7th ed. Muthén & Muthén: Los Angeles, CA; 1998.
    1. Kline RB. Principles and practice of structural equation modeling. 3rd ed. New York: Guilford Press; 2010.
    1. McFall GP, Wiebe SA, Vergote D, Westaway D, Jhamandas J, Bäckman L, et al. ApoE and pulse pressure interactively influence level and change in the aging of episodic memory: protective effects among ε2 carriers. Neuropsychology. 2015;29:388–401. doi: 10.1037/neu0000150.
    1. McFall GP, Sapkota S, McDermott KL, Dixon RA. Risk-reducing apolipoprotein E and Clusterin genotypes protect against the consequences of poor vascular health on executive function performance and change in nondemented older adults. Neurobiol Aging. 2016;42:91–100. doi: 10.1016/j.neurobiolaging.2016.02.032.
    1. Sapkota S, Bäckman L, Dixon RA. Executive function performance and change in aging is predicted by apolipoprotein E, intensified by catechol-O-methyltransferase and brain-derived neurotrophic factor, and moderated by age and lifestyle. Neurobiol Aging. 2017;52:81–89. doi: 10.1016/j.neurobiolaging.2016.12.022.
    1. Sapkota S, Dixon RA. A network of genetic effects on non-demented cognitive aging: Alzheimer’s genetic risk (CLU + CR1 + PICALM) intensifies cognitive aging genetic risk (COMT + BDNF) selectively for APOEϵ4 carriers. J Alzheimers Dis. 2018;62:887–900. doi: 10.3233/JAD-170909.
    1. Risacher SL, Kim S, Nho K, Foroud T, Shen L, Petersen RC, et al. APOE effect on Alzheimer’s disease biomarkers in older adults with significant memory concern. Alzheimers Dement. 2015;11:1417–1429. doi: 10.1016/j.jalz.2015.03.003.
    1. Liu CC, Liu CC, Kanekiyo T, Xu H, Bu G. Apolipoprotein E and Alzheimer disease: risk, mechanisms and therapy. Nat Rev Neurol. 2013;9:106–118. doi: 10.1038/nrneurol.2012.263.
    1. Raber J, Huang Y, Ashford JW. ApoE genotype accounts for the vast majority of AD risk and AD pathology. Neurobiol Aging. 2004;25:641–650. doi: 10.1016/j.neurobiolaging.2003.12.023.
    1. Brainerd CJ, Reyna VF, Petersen RC, Smith GE, Taub ES. Is the apolipoprotein e genotype a biomarker for mild cognitive impairment? Findings from a nationally representative study. Neuropsychology. 2011;25:679–689. doi: 10.1037/a0024483.
    1. Brainerd CJ, Reyna VF, Petersen RC, Smith GE, Kenney AE, Gross CJ, et al. The apolipoprotein E genotype predicts longitudinal transitions to mild cognitive impairment but not to Alzheimer’s dementia: findings from a nationally representative study. Neuropsychology. 2013;27:86–94. doi: 10.1037/a0030855.
    1. Fotuhi M, Hachinski V, Whitehouse PJ. Changing perspectives regarding late-life dementia. Nat Rev Neurol. 2009;5:649–658. doi: 10.1038/nrneurol.2009.175.
    1. Topiwala A, Allan CL, Valkanova V, Zsoldos E, Filippini N, Sexton CE, et al. Resilience and MRI correlates of cognitive impairment in community-dwelling elders. Br J Psychiatry. 2015;207:435–439. doi: 10.1192/bjp.bp.114.152363.
    1. Vemuri P, Weigand SD, Przybelski SA, Knopman DS, Smith GE, Trojanowski JQ, et al. Cognitive reserve and Alzheimer’s disease biomarkers are independent determinants of cognition. Brain. 2011;134:1479–1492. doi: 10.1093/brain/awr049.
    1. Kuller LH, Lopez OL, Becker JT, Chang Y, Newman AB. Risk of dementia and death in the long-term follow-up of the Pittsburgh Cardiovascular Health Study–Cognition Study. Alzheimers Dement. 2016;12:170–183. doi: 10.1016/j.jalz.2015.08.165.
    1. Soldan A, Pettigrew C, Lu Y, Wang MC, Selnes O, Albert M, et al. Relationship of medial temporal lobe atrophy, APOE genotype, and cognitive reserve in preclinical Alzheimer’s disease. Hum Brain Mapp. 2015;36:2826–2841. doi: 10.1002/hbm.22810.
    1. Schuff N, Woerner N, Boreta L, Kornfield T, Shaw LM, Trojanowski JQ, et al. MRI of hippocampal volume loss in early Alzheimer’s disease in relation to ApoE genotype and biomarkers. Brain. 2008;132:1067–1077. doi: 10.1093/brain/awp007.
    1. Boots EA, Schultz SA, Almeida RP, Oh JM, Koscik RL, Dowling MN, et al. Occupational complexity and cognitive reserve in a middle-aged cohort at risk for Alzheimer’s disease. Arch Clin Neuropsychol. 2015;30:634–642. doi: 10.1093/arclin/acv041.
    1. Perneczky R, Drzezga A, Diehl-Schmid J, Li Y, Kurz A. Gender differences in brain reserve. J Neurol. 2007;254:1395–1400. doi: 10.1007/s00415-007-0558-z.
    1. Li CY, Wu SC, Sung FC. Lifetime principal occupation and risk of cognitive impairment among the elderly. Ind Health. 2002;40:7–13. doi: 10.2486/indhealth.40.7.
    1. Stern Y. Cognitive reserve in ageing and Alzheimer’s disease. Lancet Neurol. 2012;11:1006–1012. doi: 10.1016/S1474-4422(12)70191-6.
    1. Rusmaully J, Dugravot A, Moatti J-P, Marmot MG, Elbaz A, Kivimaki M, et al. Contribution of cognitive performance and cognitive decline to associations between socioeconomic factors and dementia: a cohort study. PLoS Med. 2017;14:e1002334. doi: 10.1371/journal.pmed.1002334.
    1. Arenaza-Urquijo EM, Bejanin A, Gonneaud J, Wirth M, La Joie R, Mutlu J, et al. Association between educational attainment and amyloid deposition across the spectrum from normal cognition to dementia: neuroimaging evidence for protection and compensation. Neurobiol Aging. 2017;59:72–79. doi: 10.1016/j.neurobiolaging.2017.06.016.
    1. Ramirez J, McNeely AA, Berezuk C, Gao F, Black SE. Dynamic progression of white matter hyperintensities in Alzheimer’s disease and normal aging: results from the Sunnybrook dementia study. Front Aging Neurosci. 2016;8:62. doi: 10.3389/fnagi.2016.00062.
    1. Murray AD, Staff RT. McNeil CJ, Salarirad S, Ahearn TS, Mustafa N, et al. The balance between cognitive reserve and brain imaging biomarkers of cerebrovascular and Alzheimer’s diseases. Brain. 2011;134:3687–3696. doi: 10.1093/brain/awr259.
    1. Kroger E, Andel R, Lindsay J, Benounissa Z, Verreault R, Laurin D. Is complexity of work associated with risk of dementia? The Canadian Study of Health and Aging. Am J Epidemiol. 2008;167:820–830. doi: 10.1093/aje/kwm382.
    1. Berezuk C, Ramirez J, Black SE, Zakzanis KK, Alzheimer’s Disease Neuroimaging Initiative Managing money matters: managing finances is associated with functional independence in MCI. Int J Geriatr Psychiatry. 2018;33:517–522. doi: 10.1002/gps.4817.

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