Meta-Analysis

. 2019 Jul 23;16(7):e1002853.

doi: 10.1371/journal.pmed.1002853. eCollection 2019 Jul.

Determinants of cognitive performance and decline in 20 diverse ethno-regional groups: A COSMIC collaboration cohort study

Darren M Lipnicki¹, Steve R Makkar¹, John D Crawford¹, Anbupalam Thalamuthu¹, Nicole A Kochan¹, Maria Fernanda Lima-Costa², Erico Castro-Costa², Cleusa Pinheiro Ferri³, Carol Brayne⁴, Blossom Stephan⁵, Juan J Llibre-Rodriguez⁶, Jorge J Llibre-Guerra^{7

8}, Adolfo J Valhuerdi-Cepero⁹, Richard B Lipton^{10

11

12}, Mindy J Katz¹⁰, Carol A Derby^{10

11}, Karen Ritchie^{13

14

15}, Marie-Laure Ancelin^{13

14}, Isabelle Carrière^{13

14}, Nikolaos Scarmeas^{16

17}, Mary Yannakoulia¹⁸, Georgios M Hadjigeorgiou^{19

20}, Linda Lam²¹, Wai-Chi Chan²², Ada Fung²³, Antonio Guaita²⁴, Roberta Vaccaro²⁴, Annalisa Davin²⁴, Ki Woong Kim^{25

26

27}, Ji Won Han²⁵, Seung Wan Suh²⁵, Steffi G Riedel-Heller²⁸, Susanne Roehr²⁸, Alexander Pabst²⁸, Martin van Boxtel²⁹, Sebastian Köhler²⁹, Kay Deckers²⁹, Mary Ganguli^{30

31

32}, Erin P Jacobsen³⁰, Tiffany F Hughes³³, Kaarin J Anstey^{34

35

36}, Nicolas Cherbuin³⁶, Mary N Haan³⁷, Allison E Aiello^{38

39}, Kristina Dang³⁷, Shuzo Kumagai⁴⁰, Tao Chen⁴⁰, Kenji Narazaki⁴¹, Tze Pin Ng⁴², Qi Gao⁴², Ma Shwe Zin Nyunt⁴³, Marcia Scazufca⁴⁴, Henry Brodaty^{1

45}, Katya Numbers¹, Julian N Trollor^{1

46}, Kenichi Meguro⁴⁷, Satoshi Yamaguchi⁴⁷, Hiroshi Ishii⁴⁷, Antonio Lobo^{48

49

50}, Raul Lopez-Anton^{49

50

51}, Javier Santabárbara^{49

50

52}, Yvonne Leung¹, Jessica W Lo¹, Gordana Popovic^{1

53}, Perminder S Sachdev^{1

45}; for Cohort Studies of Memory in an International Consortium (COSMIC)

Affiliations

¹ Centre for Healthy Brain Ageing, University of New South Wales, Sydney, New South Wales, Australia.
² Instituto René Rachou, Fundação Oswaldo Cruz, Rio de Janeiro, Brazil.
³ Departamento de Psiquiatria, Universidade Federal de São Paulo, São Paulo, Brazil.
⁴ Department of Public Health and Primary Care, Cambridge University, Cambridge, United Kingdom.
⁵ Institute of Health and Society, Newcastle University, Newcastle upon Tyne, United Kingdom.
⁶ Finlay-Albarrán Faculty of Medical Sciences, Medical University of Havana, Havana, Cuba.
⁷ Institute of Neurology and Neurosurgery, Havana, Cuba.
⁸ Memory and Aging Center, University of California, San Francisco, San Francisco, California, United States of America.
⁹ Medical University of Matanzas, Matanzas, Cuba.
¹⁰ Saul R. Korey Department of Neurology, Albert Einstein College of Medicine, Yeshiva University, New York, New York, United States of America.
¹¹ Department of Epidemiology and Population Health, Albert Einstein College of Medicine, Yeshiva University, New York, New York, United States of America.
¹² Department of Psychiatry and Behavioral Medicine, Albert Einstein College of Medicine, Yeshiva University, New York, New York, United States of America.
¹³ Inserm, U1061 Neuropsychiatry: Epidemiological and Clinical Research, La Colombière Hospital, Montpellier, France.
¹⁴ Université de Montpellier, Montpellier, France.
¹⁵ Centre for Clinical Brain Sciences, University of Edinburgh, Edinburgh, United Kingdom.
¹⁶ 1st Department of Neurology, Aiginition Hospital, Medical School, National and Kapodistrian University of Athens, Athens, Greece.
¹⁷ Taub Institute for Research on Alzheimer's Disease and the Aging Brain, Gertrude H. Sergievsky Center, Department of Neurology, Columbia University, New York, New York, United States of America.
¹⁸ Department of Nutrition and Dietetics, Harokopio University, Athens, Greece.
¹⁹ University of Thessaly, Larissa, Greece.
²⁰ Department of Neurology, Medical School, University of Cyprus, Nicosia, Cyprus.
²¹ Department of Psychiatry, Chinese University of Hong Kong, Hong Kong SAR, China.
²² Department of Psychiatry, University of Hong Kong, Hong Kong SAR, China.
²³ Department of Applied Social Sciences, Hong Kong Polytechnic University, Hong Kong SAR, China.
²⁴ Golgi Cenci Foundation, Milan, Italy.
²⁵ Department of Neuropsychiatry, Seoul National University Bundang Hospital, Seongnam, Korea.
²⁶ Department of Psychiatry, College of Medicine, Seoul National University, Seoul, Korea.
²⁷ Department of Brain and Cognitive Science, College of Natural Sciences, Seoul National University, Seoul, Korea.
²⁸ Institute of Social Medicine, Occupational Health and Public Health, Medical Faculty, University of Leipzig, Leipzig, Germany.
²⁹ Department of Psychiatry and Neuropsychology, School for Mental Health and Neuroscience, Maastricht University Medical Center, Maastricht, The Netherlands.
³⁰ Department of Psychiatry, School of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.
³¹ Department of Neurology, School of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.
³² Department of Epidemiology, Graduate School of Public Health, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.
³³ Department of Sociology, Anthropology, and Gerontology, Youngstown State University, Youngstown, Ohio, United States of America.
³⁴ School of Psychology, University of New South Wales, Sydney, New South Wales, Australia.
³⁵ Neuroscience Research Australia, Sydney, New South Wales, Australia.
³⁶ Centre for Research on Ageing, Health and Wellbeing, Australian National University, Canberra, Australian Capital Territory, Australia.
³⁷ Department of Epidemiology and Biostatistics, School of Medicine, University of California, San Francisco, San Francisco, California, United States of America.
³⁸ Department of Epidemiology, Gillings School of Global Public Health, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.
³⁹ Carolina Population Center, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.
⁴⁰ Center for Health Science and Counseling, Kyushu University, Kasuga, Japan.
⁴¹ Faculty of Socio-Environmental Studies, Fukuoka Institute of Technology, Fukuoka, Japan.
⁴² Gerontology Research Programme, Department of Psychological Medicine, Yong Loo Lin School of Medicine, National University of Singapore, Singapore.
⁴³ Department of Psychological Medicine, Yong Loo Lin School of Medicine, National University of Singapore, Singapore.
⁴⁴ Instituto de Psiquiatria e LIM-23, Hospital da Clínicas, Faculdade de Medicina, Universidade de São Paulo, São Paulo, Brazil.
⁴⁵ Dementia Collaborative Research Centre, University of New South Wales, Sydney, New South Wales, Australia.
⁴⁶ Department of Developmental Disability Neuropsychiatry, School of Psychiatry, University of New South Wales, Sydney, New South Wales, Australia.
⁴⁷ Geriatric Behavioral Neurology, Tohoku University, Sendai, Japan.
⁴⁸ Department of Medicine and Psychiatry, Universidad de Zaragoza, Zaragoza, Spain.
⁴⁹ Instituto de Investigación Sanitaria Aragón, Zaragoza, Spain.
⁵⁰ Centro de Investigación Biomédica en Red de Salud Mental, Ministry of Science and Innovation, Madrid, Spain.
⁵¹ Department of Psychology and Sociology, Universidad de Zaragoza, Zaragoza, Spain.
⁵² Department of Microbiology, Preventive Medicine and Public Health, Universidad de Zaragoza, Zaragoza, Spain.
⁵³ School of Mathematics and Statistics, University of New South Wales, Sydney, New South Wales, Australia.

PMID: 31335910
PMCID: PMC6650056
DOI: 10.1371/journal.pmed.1002853

Meta-Analysis

Determinants of cognitive performance and decline in 20 diverse ethno-regional groups: A COSMIC collaboration cohort study

Darren M Lipnicki et al. PLoS Med. 2019.

. 2019 Jul 23;16(7):e1002853.

doi: 10.1371/journal.pmed.1002853. eCollection 2019 Jul.

Authors

Affiliations

¹ Centre for Healthy Brain Ageing, University of New South Wales, Sydney, New South Wales, Australia.
² Instituto René Rachou, Fundação Oswaldo Cruz, Rio de Janeiro, Brazil.
³ Departamento de Psiquiatria, Universidade Federal de São Paulo, São Paulo, Brazil.
⁴ Department of Public Health and Primary Care, Cambridge University, Cambridge, United Kingdom.
⁵ Institute of Health and Society, Newcastle University, Newcastle upon Tyne, United Kingdom.
⁶ Finlay-Albarrán Faculty of Medical Sciences, Medical University of Havana, Havana, Cuba.
⁷ Institute of Neurology and Neurosurgery, Havana, Cuba.
⁸ Memory and Aging Center, University of California, San Francisco, San Francisco, California, United States of America.
⁹ Medical University of Matanzas, Matanzas, Cuba.
¹⁰ Saul R. Korey Department of Neurology, Albert Einstein College of Medicine, Yeshiva University, New York, New York, United States of America.
¹¹ Department of Epidemiology and Population Health, Albert Einstein College of Medicine, Yeshiva University, New York, New York, United States of America.
¹² Department of Psychiatry and Behavioral Medicine, Albert Einstein College of Medicine, Yeshiva University, New York, New York, United States of America.
¹³ Inserm, U1061 Neuropsychiatry: Epidemiological and Clinical Research, La Colombière Hospital, Montpellier, France.
¹⁴ Université de Montpellier, Montpellier, France.
¹⁵ Centre for Clinical Brain Sciences, University of Edinburgh, Edinburgh, United Kingdom.
¹⁶ 1st Department of Neurology, Aiginition Hospital, Medical School, National and Kapodistrian University of Athens, Athens, Greece.
¹⁷ Taub Institute for Research on Alzheimer's Disease and the Aging Brain, Gertrude H. Sergievsky Center, Department of Neurology, Columbia University, New York, New York, United States of America.
¹⁸ Department of Nutrition and Dietetics, Harokopio University, Athens, Greece.
¹⁹ University of Thessaly, Larissa, Greece.
²⁰ Department of Neurology, Medical School, University of Cyprus, Nicosia, Cyprus.
²¹ Department of Psychiatry, Chinese University of Hong Kong, Hong Kong SAR, China.
²² Department of Psychiatry, University of Hong Kong, Hong Kong SAR, China.
²³ Department of Applied Social Sciences, Hong Kong Polytechnic University, Hong Kong SAR, China.
²⁴ Golgi Cenci Foundation, Milan, Italy.
²⁵ Department of Neuropsychiatry, Seoul National University Bundang Hospital, Seongnam, Korea.
²⁶ Department of Psychiatry, College of Medicine, Seoul National University, Seoul, Korea.
²⁷ Department of Brain and Cognitive Science, College of Natural Sciences, Seoul National University, Seoul, Korea.
²⁸ Institute of Social Medicine, Occupational Health and Public Health, Medical Faculty, University of Leipzig, Leipzig, Germany.
²⁹ Department of Psychiatry and Neuropsychology, School for Mental Health and Neuroscience, Maastricht University Medical Center, Maastricht, The Netherlands.
³⁰ Department of Psychiatry, School of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.
³¹ Department of Neurology, School of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.
³² Department of Epidemiology, Graduate School of Public Health, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.
³³ Department of Sociology, Anthropology, and Gerontology, Youngstown State University, Youngstown, Ohio, United States of America.
³⁴ School of Psychology, University of New South Wales, Sydney, New South Wales, Australia.
³⁵ Neuroscience Research Australia, Sydney, New South Wales, Australia.
³⁶ Centre for Research on Ageing, Health and Wellbeing, Australian National University, Canberra, Australian Capital Territory, Australia.
³⁷ Department of Epidemiology and Biostatistics, School of Medicine, University of California, San Francisco, San Francisco, California, United States of America.
³⁸ Department of Epidemiology, Gillings School of Global Public Health, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.
³⁹ Carolina Population Center, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.
⁴⁰ Center for Health Science and Counseling, Kyushu University, Kasuga, Japan.
⁴¹ Faculty of Socio-Environmental Studies, Fukuoka Institute of Technology, Fukuoka, Japan.
⁴² Gerontology Research Programme, Department of Psychological Medicine, Yong Loo Lin School of Medicine, National University of Singapore, Singapore.
⁴³ Department of Psychological Medicine, Yong Loo Lin School of Medicine, National University of Singapore, Singapore.
⁴⁴ Instituto de Psiquiatria e LIM-23, Hospital da Clínicas, Faculdade de Medicina, Universidade de São Paulo, São Paulo, Brazil.
⁴⁵ Dementia Collaborative Research Centre, University of New South Wales, Sydney, New South Wales, Australia.
⁴⁶ Department of Developmental Disability Neuropsychiatry, School of Psychiatry, University of New South Wales, Sydney, New South Wales, Australia.
⁴⁷ Geriatric Behavioral Neurology, Tohoku University, Sendai, Japan.
⁴⁸ Department of Medicine and Psychiatry, Universidad de Zaragoza, Zaragoza, Spain.
⁴⁹ Instituto de Investigación Sanitaria Aragón, Zaragoza, Spain.
⁵⁰ Centro de Investigación Biomédica en Red de Salud Mental, Ministry of Science and Innovation, Madrid, Spain.
⁵¹ Department of Psychology and Sociology, Universidad de Zaragoza, Zaragoza, Spain.
⁵² Department of Microbiology, Preventive Medicine and Public Health, Universidad de Zaragoza, Zaragoza, Spain.
⁵³ School of Mathematics and Statistics, University of New South Wales, Sydney, New South Wales, Australia.

PMID: 31335910
PMCID: PMC6650056
DOI: 10.1371/journal.pmed.1002853

Abstract

Background: With no effective treatments for cognitive decline or dementia, improving the evidence base for modifiable risk factors is a research priority. This study investigated associations between risk factors and late-life cognitive decline on a global scale, including comparisons between ethno-regional groups.

Methods and findings: We harmonized longitudinal data from 20 population-based cohorts from 15 countries over 5 continents, including 48,522 individuals (58.4% women) aged 54-105 (mean = 72.7) years and without dementia at baseline. Studies had 2-15 years of follow-up. The risk factors investigated were age, sex, education, alcohol consumption, anxiety, apolipoprotein E ε4 allele (APOE*4) status, atrial fibrillation, blood pressure and pulse pressure, body mass index, cardiovascular disease, depression, diabetes, self-rated health, high cholesterol, hypertension, peripheral vascular disease, physical activity, smoking, and history of stroke. Associations with risk factors were determined for a global cognitive composite outcome (memory, language, processing speed, and executive functioning tests) and Mini-Mental State Examination score. Individual participant data meta-analyses of multivariable linear mixed model results pooled across cohorts revealed that for at least 1 cognitive outcome, age (B = -0.1, SE = 0.01), APOE*4 carriage (B = -0.31, SE = 0.11), depression (B = -0.11, SE = 0.06), diabetes (B = -0.23, SE = 0.10), current smoking (B = -0.20, SE = 0.08), and history of stroke (B = -0.22, SE = 0.09) were independently associated with poorer cognitive performance (p < 0.05 for all), and higher levels of education (B = 0.12, SE = 0.02) and vigorous physical activity (B = 0.17, SE = 0.06) were associated with better performance (p < 0.01 for both). Age (B = -0.07, SE = 0.01), APOE*4 carriage (B = -0.41, SE = 0.18), and diabetes (B = -0.18, SE = 0.10) were independently associated with faster cognitive decline (p < 0.05 for all). Different effects between Asian people and white people included stronger associations for Asian people between ever smoking and poorer cognition (group by risk factor interaction: B = -0.24, SE = 0.12), and between diabetes and cognitive decline (B = -0.66, SE = 0.27; p < 0.05 for both). Limitations of our study include a loss or distortion of risk factor data with harmonization, and not investigating factors at midlife.

Conclusions: These results suggest that education, smoking, physical activity, diabetes, and stroke are all modifiable factors associated with cognitive decline. If these factors are determined to be causal, controlling them could minimize worldwide levels of cognitive decline. However, any global prevention strategy may need to consider ethno-regional differences.

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Conflict of interest statement

I have read the journal's policy and the authors of this manuscript have the following competing interests: AEA is a consultant for Kinsa Inc. and has received an unrestricted gift from Gojo Inc. CB is a member of the Editorial Board of PLOS Medicine. HB is on the Advisory Board of Nutricia Australia. MG was on Biogen Inc’s “Patient Journey Advisory Group” in 2016 and 2017. NS reports personal fees from Merck Consumer Health and the NIH outside the submitted work. RBL is the Edwin S. Lowe Professor of Neurology at the Albert Einstein College of Medicine in New York. He receives research support from the NIH: 2PO1 AG003949 (mPI), 5U10 NS077308 (PI), RO1 NS082432 (Investigator), 1RF1 AG057531 (Site PI), RF1 AG054548 (Investigator), 1RO1 AG048642 (Investigator), R56 AG057548 (Investigator), K23 NS09610 (Mentor), K23AG049466 (Mentor), 1K01AG054700 (Mentor). He also receives support from the Migraine Research Foundation and the National Headache Foundation. He serves on the editorial board of Neurology, senior advisor to Headache, and associate editor to Cephalalgia. He has reviewed for the NIA and NINDS, holds stock options in eNeura Therapeutics and Biohaven Holdings; 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, Dr. Reddy’s, Electrocore, Eli Lilly, eNeura Therapeutics, GlaxoSmithKline, Merck, Pernix, Pfizer, Supernus, Teva, Trigemina, Vector, Vedanta. He receives royalties from Wolff’s Headache 7th and 8th Edition, Oxford Press University, 2009, Wiley and Informa. PSS received grant funding from the NIH/NIA (USA) and the NHMRC (Australia), as well as philanthropic funding through The Dementia Momentum. He is on the Australian Advisory Board of Biogen Pharmaceuticals. All other authors have declared that no competing interests exist.

Figures

**Fig 1. Risk factors for cognitive performance that differ between Asian people and white people.**
Bars show standardized scores at the mean time in study (3.1 years) for participants with and without the risk factor in both groups: Asian people and white people. Error bars indicate standard error of the mean. Mean Mini-Mental State Examination (MMSE) performance is compared for smokers and non-smokers (A), participants with poor versus very good self-rated health (B), and apolipoprotein E ε4 allele (*APOE*4*) carriers and non-carriers (C). (D) compares the mean performance for the global cognition composite (calculated from tests of 4 cognitive domains) in men and women.

**Fig 2. Risk factors for cognitive decline that differ between Asian people and white people.**
Fitted trajectories are for the first half decade since baseline, and show mean changes in standardized Mini-Mental State Examination (MMSE) scores for both groups: Asian people and white people. (A) compares participants with and without high cholesterol, and (B) compares participants with and without diabetes. (C) compares participants with high and low levels of education, determined as 1 standard deviation (4.5 years) above and below the mean of 9 years, respectively.

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Determinants of cognitive performance and decline in 20 diverse ethno-regional groups: A COSMIC collaboration cohort study

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Determinants of cognitive performance and decline in 20 diverse ethno-regional groups: A COSMIC collaboration cohort study

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