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      Age-related cognitive decline and associations with sex, education and apolipoprotein E genotype across ethnocultural groups and geographic regions: a collaborative cohort study

      research-article
      1 , 1 , 1 , 1 , 1 , 1 , 2 , 2 , 3 , 4 , 5 , 5 , 6 , 7 , 6 , 8 , 9 , 10 , 8 , 9 , 8 , 9 , 11 , 12 , 13 , 14 , 15 , 16 , 15 , 17 , 17 , 17 , 18 , 19 , 20 , 18 , 21 , 22 , 22 , 22 , 23 , 24 , 25 , 26 , 27 , 27 , 1 , 1 , 28 , 29 , 30 , 29 , 31 , 29 , 32 , 1 , 28 , * , Cohort Studies of Memory in an International Consortium (COSMIC)
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          Abstract

          Background

          The prevalence of dementia varies around the world, potentially contributed to by international differences in rates of age-related cognitive decline. Our primary goal was to investigate how rates of age-related decline in cognitive test performance varied among international cohort studies of cognitive aging. We also determined the extent to which sex, educational attainment, and apolipoprotein E ε4 allele ( APOE*4) carrier status were associated with decline.

          Methods and findings

          We harmonized longitudinal data for 14 cohorts from 12 countries (Australia, Brazil, France, Greece, Hong Kong, Italy, Japan, Singapore, Spain, South Korea, United Kingdom, United States), for a total of 42,170 individuals aged 54–105 y (42% male), including 3.3% with dementia at baseline. The studies began between 1989 and 2011, with all but three ongoing, and each had 2–16 assessment waves (median = 3) and a follow-up duration of 2–15 y. We analyzed standardized Mini-Mental State Examination (MMSE) and memory, processing speed, language, and executive functioning test scores using linear mixed models, adjusted for sex and education, and meta-analytic techniques. Performance on all cognitive measures declined with age, with the most rapid rate of change pooled across cohorts a moderate -0.26 standard deviations per decade (SD/decade) (95% confidence interval [CI] [-0.35, -0.16], p < 0.001) for processing speed. Rates of decline accelerated slightly with age, with executive functioning showing the largest additional rate of decline with every further decade of age (-0.07 SD/decade, 95% CI [-0.10, -0.03], p = 0.002). There was a considerable degree of heterogeneity in the associations across cohorts, including a slightly faster decline ( p = 0.021) on the MMSE for Asians (-0.20 SD/decade, 95% CI [-0.28, -0.12], p < 0.001) than for whites (-0.09 SD/decade, 95% CI [-0.16, -0.02], p = 0.009). Males declined on the MMSE at a slightly slower rate than females (difference = 0.023 SD/decade, 95% CI [0.011, 0.035], p < 0.001), and every additional year of education was associated with a rate of decline slightly slower for the MMSE (0.004 SD/decade less, 95% CI [0.002, 0.006], p = 0.001), but slightly faster for language (-0.007 SD/decade more, 95% CI [-0.011, -0.003], p = 0.001). APOE*4 carriers declined slightly more rapidly than non-carriers on most cognitive measures, with processing speed showing the greatest difference (-0.08 SD/decade, 95% CI [-0.15, -0.01], p = 0.019). The same overall pattern of results was found when analyses were repeated with baseline dementia cases excluded. We used only one test to represent cognitive domains, and though a prototypical one, we nevertheless urge caution in generalizing the results to domains rather than viewing them as test-specific associations. This study lacked cohorts from Africa, India, and mainland China.

          Conclusions

          Cognitive performance declined with age, and more rapidly with increasing age, across samples from diverse ethnocultural groups and geographical regions. Associations varied across cohorts, suggesting that different rates of cognitive decline might contribute to the global variation in dementia prevalence. However, the many similarities and consistent associations with education and APOE genotype indicate a need to explore how international differences in associations with other risk factors such as genetics, cardiovascular health, and lifestyle are involved. Future studies should attempt to use multiple tests for each cognitive domain and feature populations from ethnocultural groups and geographical regions for which we lacked data.

          Abstract

          In a collaborative cohort study, Darren Lipnicki and colleagues investigate associations between age-related cognitive decline and sex, education, and apolipoprotein E genotype across ethnocultural groups and geographic regions.

          Author summary

          Why was this study done?
          • The prevalence of dementia varies around the world, but it is not known whether international differences in rates of cognitive decline contribute to this.

          • The extent to which risk and protective factors such as sex, education, and apolipoprotein E ε4 allele ( APOE*4) carrier status have different associations with dementia in different ethnocultural groups and geographic regions is also not known.

          What did the researchers do and find?
          • We analyzed cognitive performance data from 42,170 mostly elderly individuals, provided by 14 studies of aging representing 12 countries (Australia, Brazil, France, Greece, Hong Kong, Italy, Japan, Singapore, Spain, South Korea, United Kingdom, United States).

          • The Mini-Mental State Examination (MMSE) and memory, processing speed, language, and executive functioning test scores all declined with age, and rates of decline accelerated with age.

          • The 14 studies showed different rates of decline, and decline in MMSE scores was faster for Asians than whites, females than males, and APOE*4 carriers than non-carriers. APOE*4 carriers also declined faster than non-carriers on test of memory, processing speed, and language.

          What do these findings mean?
          • International differences in rates of cognitive decline might contribute to the global variation in dementia prevalence.

          • Further research is needed to determine whether cardiovascular health, lifestyle, and other risk factors for dementia have different associations with cognitive decline in different ethnocultural groups and geographic regions.

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          Most cited references43

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          Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families.

          The apolipoprotein E type 4 allele (APOE-epsilon 4) is genetically associated with the common late onset familial and sporadic forms of Alzheimer's disease (AD). Risk for AD increased from 20% to 90% and mean age at onset decreased from 84 to 68 years with increasing number of APOE-epsilon 4 alleles in 42 families with late onset AD. Thus APOE-epsilon 4 gene dose is a major risk factor for late onset AD and, in these families, homozygosity for APOE-epsilon 4 was virtually sufficient to cause AD by age 80.
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            • Abstract: found
            • Article: not found

            The Alzheimer's Disease Centers' Uniform Data Set (UDS): the neuropsychologic test battery.

            The neuropsychologic test battery from the Uniform Data Set (UDS) of the Alzheimer's Disease Centers (ADC) program of the National Institute on Aging consists of brief measures of attention, processing speed, executive function, episodic memory, and language. This paper describes development of the battery and preliminary data from the initial UDS evaluation of 3268 clinically cognitively normal men and women collected over the first 24 months of utilization. The subjects represent a sample of community-dwelling, individuals who volunteer for studies of cognitive aging. Subjects were considered "clinically cognitively normal" based on clinical assessment, including the Clinical Dementia Rating scale and the Functional Assessment Questionnaire. The results demonstrate performance on tests sensitive to cognitive aging and to the early stages of Alzheimer disease in a relatively well-educated sample. Regression models investigating the impact of age, education, and sex on test scores indicate that these variables will need to be incorporated in subsequent normative studies. Future plans include: (1) determining the psychometric properties of the battery; (2) establishing normative data, including norms for different ethnic minority groups; and (3) conducting longitudinal studies on cognitively normal subjects, individuals with mild cognitive impairment, and individuals with Alzheimer disease and other forms of dementia.
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              Is Open Access

              Clinical epidemiology of Alzheimer’s disease: assessing sex and gender differences

              With the aging of the population, the burden of Alzheimer’s disease (AD) is rapidly expanding. More than 5 million people in the US alone are affected with AD and this number is expected to triple by 2050. While men may have a higher risk of mild cognitive impairment (MCI), an intermediate stage between normal aging and dementia, women are disproportionally affected with AD. One explanation is that men may die of competing causes of death earlier in life, so that only the most resilient men may survive to older ages. However, many other factors should also be considered to explain the sex differences. In this review, we discuss the differences observed in men versus women in the incidence and prevalence of MCI and AD, in the structure and function of the brain, and in the sex-specific and gender-specific risk and protective factors for AD. In medical research, sex refers to biological differences such as chromosomal differences (eg, XX versus XY chromosomes), gonadal differences, or hormonal differences. In contrast, gender refers to psychosocial and cultural differences between men and women (eg, access to education and occupation). Both factors play an important role in the development and progression of diseases, including AD. Understanding both sex- and gender-specific risk and protective factors for AD is critical for developing individualized interventions for the prevention and treatment of AD.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS Med
                PLoS Med
                plos
                plosmed
                PLoS Medicine
                Public Library of Science (San Francisco, CA USA )
                1549-1277
                1549-1676
                21 March 2017
                March 2017
                : 14
                : 3
                : e1002261
                Affiliations
                [1 ]Centre for Healthy Brain Ageing, University of New South Wales, Sydney, Australia
                [2 ]Rene Rachou Research Institute, Oswaldo Cruz Foundation, Rio de Janeiro, Brazil
                [3 ]Department of Public Health and Primary Care, Cambridge University, Cambridge, United Kingdom
                [4 ]MRC Biostatistics Unit, Institute of Public Health, Cambridge, United Kingdom
                [5 ]Institute of Health and Society, Newcastle University, Newcastle upon Tyne, United Kingdom
                [6 ]Saul B. Korey Department of Neurology, Albert Einstein College of Medicine, Yeshiva University, New York City, New York, United States of America
                [7 ]Department of Epidemiology and Population Health, Albert Einstein College of Medicine, Yeshiva University, New York City, New York, United States of America
                [8 ]Inserm, U1061 Neuropsychiatry: Epidemiological and Clinical Research, La Colombière Hospital, Montpellier, France
                [9 ]Université de Montpellier, Montpellier, France
                [10 ]Centre for Clinical Brain Sciences, University of Edinburgh, Edinburgh, United Kingdom
                [11 ]National and Kapodistrian University of Athens, Athens, Greece
                [12 ]Columbia University, New York City, New York, United States of America
                [13 ]Harokopio University, Athens, Greece
                [14 ]University of Thessaly, Larissa, Greece
                [15 ]Department of Psychiatry, The Chinese University of Hong Kong, Hong Kong SAR, China
                [16 ]Department of Psychiatry, Tai Po Hospital, Hong Kong SAR, China
                [17 ]GolgiCenci Foundation, Abbiategrasso, Milan, Italy
                [18 ]Department of Neuropsychiatry, Seoul National University Bundang Hospital, Seongnam, Korea
                [19 ]Department of Psychiatry, Seoul National University, College of Medicine, Seoul, Korea
                [20 ]Department of Brain and Cognitive Science, Seoul National University College of Natural Sciences, Seoul, Korea
                [21 ]Department of Psychiatry, Yonsei University Wonju Severance Christian Hospital, Wonju, Korea
                [22 ]Centre for Research on Ageing, Health and Wellbeing, College of Medicine, Biology and Environment, The Australian National University, Canberra, Australia
                [23 ]Institute of Psychiatry and LIM-23, Clinics Hospital, University of São Paulo, São Paulo, Brazil
                [24 ]Faculty of Arts and Science, Kyushu University, Kasuga City, Japan
                [25 ]Xiangya School of Nursing, Central South University, Changsha, China
                [26 ]Faculty of Socio-Environmental Studies, Fukuoka Institute of Technology, Fukuoka City, Japan
                [27 ]Gerontology Research Programme, Department of Psychological Medicine, Yong Loo Lin School of Medicine, National University of Singapore, Singapore
                [28 ]Dementia Collaborative Research Centre, University of New South Wales, Sydney, Australia
                [29 ]Centro de Investigación Biomédica en Red de Salud Mental (CIBERSAM), Ministry of Science and Innovation, Madrid, Spain
                [30 ]Department of Medicine and Psychiatry, Universidad de Zaragoza, Zaragoza, Spain
                [31 ]Centro de Investigación Biomédica en Red de Salud Mental, CIBERSAM, Spanish Ministry of Economy and Competitiveness, Madrid, Spain
                [32 ]Department of Microbiology, Preventive Medicine and Public Health, University of Zaragoza, Spain
                University of California San Francisco Memory and Aging Center, UNITED STATES
                Author notes

                I have read the journal's policy and the authors of this manuscript have the following competing interests: JDC is supported by the National Health and Medical Research Council of Australia (NHMRC Program Grant ID 568969). CB is a member of the Editorial Board of PLOS Medicine. FEM is a member of the Editorial Board of PLOS Medicine. RBL is the Edwin S. Lowe Professor of Neurology at the Albert Einstein College of Medicine in New York and receives research support from the NIH; receives support from the Migraine Research Foundation and the National Headache Foundation and serves on the editorial board of Neurology and as senior advisor to Headache; has reviewed for the NIA and NINDS, holds stock options in eNeura Therapeutics; serves as consultant, advisory board member, or has received honoraria from American Academy of Neurology, Alder, Allergan, American Headache Society, Amgen, Autonomic Technologies, Avanir, Biohaven, Biovision, Boston Scientific, Colucid, Dr. Reddy’s, Electrocore, Eli Lilly, eNeura Therapeutics, GlaxoSmithKlein (formerly Novartis), Merck, Pernix, Pfizer, Supernus, Teva, Trigemina, Vector, Vedanta; and receives royalties from Wolff’s Headache, 8th Edition, Oxford Press University, 2009, Wiley and Informa. MJK is funded by NIH/NIA and the following private foundations: Czap Foundation, Sylvia and Leonard Marx Foundation and also receives consultation fees from Eli Lilly and Company. HB has received departmental grants for drug trials from Lilly, Merck, Sanofi, Servier and Tau Therapeutics; is on the advisory board for Nutricia and has been asked to be an advisor to Lundbeck, Otuska and Eli Lilly; and is on clinical advisory committees for Montefiore Homes and Cranbrook Care, both of which operate residential/ long-term care homes. AL has received honoraria or travel fees from Lundbeck and Sanofi. PSS would like to acknowledge financial support from the National Health & Medical Research Council (APP1093083), the Vincent Fairfax Foundation and the Yulgilbar Foundation for COSMIC. All other authors declare no competing interests.

                • Conceptualization: PSS DML JDC NAK SK CB FEM BCMS CHYW LCWL MFLC ECC KJA AL NS ED MY RBL MJK GA KWK MS.

                • Data curation: DML JDC RD AT AWTF NC SK SC KN TPN QG CHYW LCWL JSc CB FEM BCMS THK MFLC ECC KJA RLA JSa MJK JWH KWK PB MS.

                • Formal analysis: RD AT SC NAK CHYW LCWL MFLC ECC RLA JSa NS MY JWH KWK MS FEM BCMS.

                • Funding acquisition: PSS.

                • Investigation: AWTF NC SK SC KN TPN QG CHYW LCWL AG RV AD MLA HB THK NAK MFLC ECC KJA AL RLA JSa NS ED MY KR RBL MJK SR JWH GA KWK PB MS CB FEM BCMS.

                • Methodology: JDC AT SK SC KN TPN QG CB FEM LCWL KJA NS ED MY KWK MS.

                • Project administration: DML.

                • Software: JSa MJK KWK MS FEM BCMS.

                • Supervision: PSS.

                • Validation: CB FEM BCMS LCWL JSc MLA MFLC ECC KJA AL RLA JSa RBL MJK JWH KWK MS.

                • Visualization: AT.

                • Writing – original draft: DML JDC PSS.

                • Writing – review & editing: DML PSS JDC RD AT NAK GA MFLC ECC CB FEM BCMS RBL MJK KR JSc MLA NS MY ED LCWL CHYW AWTF AG RV AD KWK JWH THK KJA NC PB MS KS CS KN TPN QG SR HB AL RLA JSa.

                ¶ Membership of the Cohort Studies of Memory in an International Consortium (COSMIC) is provided in the Acknowledgments.

                Author information
                http://orcid.org/0000-0002-2267-4458
                http://orcid.org/0000-0002-8630-6398
                http://orcid.org/0000-0002-4315-2173
                http://orcid.org/0000-0002-3474-2980
                http://orcid.org/0000-0001-5307-663X
                http://orcid.org/0000-0002-1728-2388
                http://orcid.org/0000-0002-5083-7496
                http://orcid.org/0000-0003-3954-5932
                http://orcid.org/0000-0002-9706-9316
                http://orcid.org/0000-0001-9585-855X
                http://orcid.org/0000-0002-1965-7411
                http://orcid.org/0000-0003-4785-0224
                http://orcid.org/0000-0001-9487-6617
                Article
                PMEDICINE-D-16-03371
                10.1371/journal.pmed.1002261
                5360220
                28323832
                fc51f9d4-1496-40fd-a2dd-a8623c3464f4
                © 2017 Lipnicki et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 16 October 2016
                : 10 February 2017
                Page count
                Figures: 3, Tables: 2, Pages: 21
                Funding
                Funding for COSMIC comes from a National Health and Medical Research Council of Australia Program Grant (ID 1093083) and philanthropic contributions to The Dementia Momentum Fund (PSS). Funding for each of the contributing studies is as follows: The Brazilian Ministry of Health and Ministry of Science and Technology (MFLC, ECC); Major awards from the UK Medical Research Council and the Department of Health (CB, FEM, BCMS); National Institute on Health/National Institute on Aging grants (5P01 AG003949, 1R03 AG045474; RBL, MJK); Novartis (KR, JS, MLA); Alzheimer’s Association (IIRG-09-133014), ESPA-EU program Excellence Grant (ARISTEIA), which is co-funded by the European Social Fund and Greek National resources (189 10276/8/9/2011), and Ministry for Health and Social Solidarity, Greece (ΔΥ2β/οικ.51657/14.4.2009; NS, MY, ED); Mr. Lai Seung Hung & Mrs. Lai Chan Pui Ngong Dementia in Hong Kong Research Fund, and an educational fund from Eisai (LCWL, CHYW, AWTF); Fondazione Golgi Cenci and Federazione Alzheimer Italia (AG, RV, AD); Korean Health Technology R&D Project, Ministry of Health and Welfare, Republic of Korea [Grant No. HI09C1379 (A092077); KWK, JWH, THK]; National Health and Medical Research Council of Australia (Grants 973302, 179805, 157125 and 1002160; KJA, NC, PB); Wellcome Trust (grant code GR066133MA) and FAPESP-Brazil (grant code 2004/12694-8; MS); Health and Labour Sciences Research Grant from the Ministry of Health, Labour and Welfare of Japan (H25-Ninchisho-Ippan-004) and a research grant from Sasaguri town, Fukuoka, Japan (SK, SC, KN); Research grants (No. 03/ 121/17/214 and No. 08/1/21/19/567) from the Biomedical Research Council, Agency for Science, Technology and Research (A_STAR) in Singapore (TPN, QG); National Health & Medical Research Council of Australia Program Grant (ID 350833; PSS, DML, NAK, JDC, AT, GA, SR, HB); Fondo de Investigación Sanitaria, Instituto de Salud Carlos III, Spanish Ministry of Health, Madrid, Spain (Grants 94/ 1562, 97/1321E, 98/0103, 01/0255, 03/0815, 06/0617, and G03/128) and Pfizer Foundation, Madrid (AL, RLA, JS). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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                Data cannot be shared openly based on the terms of each study, however researchers may apply to the COSMIC Scientific Steering Committee by contacting Dr Kristan Kang ( k.kang@ 123456unsw.edu.au ).

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