The Influence of Age and Sex on Genetic Associations with Adult Body Size and Shape: A Large-Scale Genome-Wide Interaction Study
Winkler, Thomas W.; Justice, Anne E.; Graff, Mariaelisa; Barata, Llilda; Feitosa, Mary F.; Chu, Su; Czajkowski, Jacek; Esko, Tõnu; Fall, Tove; Kilpeläinen, Tuomas O.; Lu, Yingchang; Mägi, Reedik; Mihailov, Evelin; Pers, Tune H.; Rüeger, Sina; Teumer, Alexander; Ehret, Georg B.; Duan, Jubao; Gejman, Pablo V.; Sanders, Alan R.
2015
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Abstract
Genome-wide association studies (GWAS) have identified more than 100 genetic variants contributing to BMI, a measure of body size, or waist-to-hip ratio (adjusted for BMI, WHRadjBMI), a measure of body shape. Body size and shape change as people grow older and these changes differ substantially between men and women. To systematically screen for age- and/or sex-specific effects of genetic variants on BMI and WHRadjBMI, we performed meta-analyses of 114 studies (up to 320,485 individuals of European descent) with genome-wide chip and/or Metabochip data by the Genetic Investigation of Anthropometric Traits (GIANT) Consortium. Each study tested the association of up to ~2.8M SNPs with BMI and WHRadjBMI in four strata (men ≤50y, men >50y, women ≤50y, women >50y) and summary statistics were combined in stratum-specific meta-analyses. We then screened for variants that showed age-specific effects (G x AGE), sex-specific effects (G x SEX) or age-specific effects that differed between men and women (G x AGE x SEX). For BMI, we identified 15 loci (11 previously established for main effects, four novel) that showed significant (FDR<5%) age-specific effects, of which 11 had larger effects in younger (<50y) than in older adults (≥50y). No sex-dependent effects were identified for BMI. For WHRadjBMI, we identified 44 loci (27 previously established for main effects, 17 novel) with sex-specific effects, of which 28 showed larger effects in women than in men, five showed larger effects in men than in women, and 11 showed opposite effects between sexes. No age-dependent effects were identified for WHRadjBMI. This is the first genome-wide interaction meta-analysis to report convincing evidence of age-dependent genetic effects on BMI. In addition, we confirm the sex-specificity of genetic effects on WHRadjBMI. These results may provide further insights into the biology that underlies weight change with age or the sexually dimorphism of body shape.
Details
Title
The Influence of Age and Sex on Genetic Associations with Adult Body Size and Shape: A Large-Scale Genome-Wide Interaction Study
Author
Winkler, Thomas W. : University Regensburg
Justice, Anne E. : University of North Carolina at Chapel Hill
Graff, Mariaelisa : University of North Carolina at Chapel Hill
Barata, Llilda : Washington University in St. Louis
Feitosa, Mary F. : Washington University in St. Louis
Chu, Su : University of Michigan
Czajkowski, Jacek : Washington University in St. Louis
Esko, Tõnu : Harvard University
Fall, Tove : Uppsala University
Kilpeläinen, Tuomas O. : University of Copenhagen
Lu, Yingchang : Icahn School of Medicine at Mount Sinai
Mägi, Reedik : University of Oxford
Mihailov, Evelin : University of Tartu
Pers, Tune H. : Harvard University
Rüeger, Sina : University Hospital Lausanne
Teumer, Alexander : University Medicine Greifswald
Ehret, Georg B. : Geneva University Hospital
Duan, Jubao : University of Chicago
Gejman, Pablo V. : University of Chicago
Sanders, Alan R. : University of Chicago
Justice, Anne E. : University of North Carolina at Chapel Hill
Graff, Mariaelisa : University of North Carolina at Chapel Hill
Barata, Llilda : Washington University in St. Louis
Feitosa, Mary F. : Washington University in St. Louis
Chu, Su : University of Michigan
Czajkowski, Jacek : Washington University in St. Louis
Esko, Tõnu : Harvard University
Fall, Tove : Uppsala University
Kilpeläinen, Tuomas O. : University of Copenhagen
Lu, Yingchang : Icahn School of Medicine at Mount Sinai
Mägi, Reedik : University of Oxford
Mihailov, Evelin : University of Tartu
Pers, Tune H. : Harvard University
Rüeger, Sina : University Hospital Lausanne
Teumer, Alexander : University Medicine Greifswald
Ehret, Georg B. : Geneva University Hospital
Duan, Jubao : University of Chicago
Gejman, Pablo V. : University of Chicago
Sanders, Alan R. : University of Chicago
Content Type
Article
Published in
PLOS Genetics
Identifier(s)
Data availability statement
The stratified genome-wide association meta-analysis results for BMI and waist-hip ratio are available from the GIANT Consortium website www.broadinstitute.org/collaboration/giant
Funding Information
Aarne Koskelo Foundation
Aase and Ejner Danielsens Foundation
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Academy of Finland, 41071
Academy of Finland, 77299
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Academy of Finland, 41071
Academy of Finland, 77299
Academy of Finland, 102318
Academy of Finland, 104781
Academy of Finland, 117787
Academy of Finland, 117844
Academy of Finland, 118590
Academy of Finland, 120315
Academy of Finland, 121584
Academy of Finland, 123885
Academy of Finland, 124243
Academy of Finland, 124282
Academy of Finland, 126925
Academy of Finland, 129269
Academy of Finland, 129293
Academy of Finland, 129378
Academy of Finland, 130326
Academy of Finland, 134309
Academy of Finland, 134791
Academy of Finland, 136895
Academy of Finland, 139635
Academy of Finland, 211497
Academy of Finland, 263836
Academy of Finland, 263924
Academy of Finland, 1114194
Academy of Finland, 24300796
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Timber Merchant Vilhelm Bangs Foundation
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Althingi
American Heart Association, 13POST16500011
Agence Nationale de la 359 Recherche
Ark
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Arthritis Research UK, 18030
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Augustinus Foundation
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Australian National Health and Medical Research Council, 389891
Australian National Health and Medical Research Council, 389892
Australian National Health and Medical Research Council, 389938
Australian National Health and Medical Research Council, 442915
Australian National Health and Medical Research Council, 442981
Australian National Health and Medical Research Council, 496739
Australian National Health and Medical Research Council, 496688
Australian National Health and Medical Research Council, 552485
Australian National Health and Medical Research Council, 613672
Australian National Health and Medical Research Council, 613601
Australian National Health and Medical Research Council, 1011506
Australian Research Council, DP0770096
Australian Research Council, DP1093502
Becket Foundation
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Biobanking and Biomolecular Resources Research Infrastructure, CP 32
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Dr. Robert Pfleger-Stiftung
Dresden University of Technology, Funding Grant, Med Drive
Dutch Brain Foundation
Dutch Diabetes Research Foundation
Dutch Economic Structure Enhancing Fund
Dutch Kidney Foundation
Dutch Ministry for Health, Welfare and Sports
Dutch Ministry of Economic Affairs
Dutch Ministry of Education, Culture and Science
Egmont Foundation
Else Kröner-Fresenius Stiftung, 2012_A147
Else Kröner-Fresenius Stiftung, P48/08//A11/08
Emil Aaltonen Foundation
Erasmus Medical Center
Erasmus University
Estonian Ministry of Science and Education, SF0180142s08
European Commission, 223004
European Commission, 2004310
European Commission, DGXII
European Commission, FP6-EUROSPAN
European Commission, FP6-EXGENESIS
European Commission, FP6-LSHG-CT- 2006-018947
European Commission, FP6-LSHG-CT- 2006-01947
European Commission, FP6-LSHM-CT-2004-503485
European Commission, FP6-LSHM-CT- 2006-037593
European Commission, FP6-LSHM-CT-2007-037273
European Commission, FP7-201379
European Commission, FP7-201668
European Commission, FP7-279143
European Commission, FP7-305739
European Commission, FP7-313010
European Commission, FP7-ENGAGE-HEALTH-F4-2007-201413
European Commission, FP7-EurHEALTHAgeing-277849
European Commission, FP7-HEALTH-F4-2007-201550
European Commission, HEALTH-2011.2.4.2-2-EU-MASCARA
European Commission, HEALTH-F2-2008-201865-GEFOS
European Commission, HEALTH-F7-305507 HOMAGE
European Commission, LSHM-CT-2006-037593
European Commission, QLG1-CT- 2001-01252
European Commission, QLG1-CT-2002-00896
European Commission, QLG2-CT-2002-01254
European Regional Development Fund
European Regional Development Fund, 3.2.0304.11-0312
European Research Council, 2011-StG-280559-SEPI
European Research Council, 2011-294713-EPLORE
European Research Council, 230374
European Science Foundation, EU/QLRT-2001-01254
European Science Foundation, EuroSTRESS project, FP-006
Finlands Slottery Machine Association
Finnish Centre for Pensions
Finnish Cultural Foundation
Finnish Diabetes Association
Finnish Diabetes Research Foundation
Finnish Foundation for Cardiovascular Research
Finnish Foundation for Pediatric Research
Finnish Funding Agency for Technology and Innovation, 40058/07
Finnish Medical Society
Finnish Ministry of Education and Culture, 627;2004–2011
Finnish Ministry of Health and Social Affairs, 5254
Finnish National Public Health Institute
Finnish Special Governmental Subsidy for Health Sciences
Finska Läkaresällskapet, Signe and Ane Gyllenberg Foundation
Flemish League against Cancer, project Care4Me, ITEA2
Folkhälsan Research Foundation
Fonds voor Wetenschappelijk Onderzoek Vlaanderen
Foundation for Life and Health in Finland
Foundation for Strategic Research and the Stockholm County Council, 560283
G. Ph. Verhagen Foundation
Gene-diet Interactions in Obesity' project
Genetic Association Information Network
GENEVA Coordinating Center, U01 HG 004446
GenomEUtwin, QLRT- 2001-01254
GenomEUtwin, QLG2-CT-2002-01254
German Bundesministerium fuer Forschung und Technology, 01 AK 803 A-H
German Bundesministerium fuer Forschung und Technology, 01 IG 07015 G
German Diabetes Association
German Ministry of Cultural Affairs; the German Federal Ministry of Education and Research, 03IS2061A
German Ministry of Cultural Affairs; the German Federal Ministry of Education and Research, 03ZIK012
German Ministry of Cultural Affairs; the German Federal Ministry of Education and Research, 01ZZ9603
German Ministry of Cultural Affairs; the German Federal Ministry of Education and Research, 01ZZ0103
German Ministry of Cultural Affairs; the German Federal Ministry of Education and Research, 01ZZ0403
German National Genome Research Network
German Research Council, Obesity mechanisms, SFB- 1052
Great Wine Estates of the Margaret River region of Western Australia
Greek General Secretary of Research and Technology, PENED 2003
Gyllenberg Foundation
Health Care Centers in Vasa, Närpes and Korsholm
Health Fund of the Danish Health Insurance Societies
Helmholtz Zentrum München - German Research Center for Environmental Health
Helsinki University Central Hospital, special government funds, TYH7215
Helsinki University Central Hospital, special government funds, TKK2012005
Helsinki University Central Hospital, special government funds, TYH2012209
Hjartavernd
Ib Henriksen Foundation
Illinois Department of Public Health
Translational Genomics Research Institute
INTERREG IV Oberrhein Program, Project A28
Interuniversity Cardiology Institute of the Netherlands, 09.001
Italian Ministry of Health, targeted project, ICS110.1/RF97.71
Italian National Centre of Research InterOmics, PB05_SP3
John D and Catherine T MacArthur Foundation Research Networks on Successful Midlife Development and Socio-economic Status and Health
Johns Hopkins University, Center for Inherited Disease Research
Siemens Healthcare, Erlangen, Germany and the Federal State of Mecklenburg- West Pomerania
Juho Vainio Foundation
Juselius FouJuvenile Diabetes Research Foundation Internationalndation
KfH Stiftung Präventivmedizin e.V.
Knut and Alice Wallenberg Foundation
Kuopio University Hospital
Leenaards Foundation
Leiden University Medical Center
Liv och Hälsa
Local Government Pensions Institution
Lokaal Gezondheids Overleg Leuven and Hageland
Ludwig-Maximilians-Universität, LMUinnovativ
Lundberg Foundation
March of Dimes Birth Defects Foundation
Medical Research Council, G0601966
Medical Research Council, G0700931
Medical Research Council, G0000934
Medical Research Council, G0500539
Medical Research Council, G0600705
Medical Research Council, G1002319
Medical Research Council, G0701863
Medical Research Council, PrevMetSyn/SALVE
Medical Research Council, MC_U106179471
Medical Research Council, MC_UU_12019/1
MRC centre for Causal Analyses in Translational Epidemiology
MRC Centre for Obesity and Related Metabolic Diseases
MRC Human Genetics Unit
Medical Research Council of Canada
Mid-Atlantic Nutrition and Obesity Research Center, P30 DK072488
Ministry of the Flemish Community, Brussels, Belgium, G.0881.13
Ministry of the Flemish Community, Brussels, Belgium, G.0880.13
MIUR - CNR, Italian Flagship Project
Montreal Heart Institute Foundation
Munich Center of Health Sciences
Municipal Health Care Center and Hospital in Jakobstad
Närpes Health Care Foundation
National Alliance for Research on Schizophrenia and Depression
National Cancer Institute, CA047988
National Center for Advancing Translational Sciences, UL1TR000124
National Center for Research Resources, U54RR020278
National Heart, Lung and Blood Institute, 1RL1MH083268-01
National Heart, Lung and Blood Institute, 5R01HL087679-02
National Heart, Lung and Blood Institute, HHSN268200800007C
National Heart, Lung and Blood Institute, HHSN268201200036C
National Heart, Lung and Blood Institute, HL043851
National Heart, Lung and Blood Institute, HL080467
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National Heart, Lung and Blood Institute, HL45670
National Heart, Lung and Blood Institute, N01HC25195
National Heart, Lung and Blood Institute, N01HC55015
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National Heart, Lung and Blood Institute, N01HC55018
National Heart, Lung and Blood Institute, N01HC55019
National Heart, Lung and Blood Institute, N01HC55020
National Heart, Lung and Blood Institute, N01HC55021
National Heart, Lung and Blood Institute, N01HC55022
National Heart, Lung and Blood Institute, N01HC55222
National Heart, Lung and Blood Institute, N01HC85079
National Heart, Lung and Blood Institute, N01HC85080
National Heart, Lung and Blood Institute, N01HC85081
National Heart, Lung and Blood Institute, N01HC85082
National Heart, Lung and Blood Institute, N01HC85083
National Heart, Lung and Blood Institute, N01HC85086
National Heart, Lung and Blood Institute, N02HL64278
National Heart, Lung and Blood Institute, R01HL086694
National Heart, Lung and Blood Institute, R01HL087641
National Heart, Lung and Blood Institute, R01HL087652
National Heart, Lung and Blood Institute, R01HL087676
National Heart, Lung and Blood Institute, R01HL59367
National Heart, Lung and Blood Institute, R01HL103612
National Heart, Lung and Blood Institute, R01HL105756
National Heart, Lung and Blood Institute, R01HL120393
National Heart, Lung and Blood Institute, U01HL080295
National Human Genome Research Institute, U01HG004402
National Institute for Health and Welfare
National Institute for Health Research, RP-PG-0407-10371
National Institute of Allergy and Infectious Diseases
National Institute of Child Health and Human Development
National Institute of Diabetes and Digestive and Kidney Disease, 1R01DK8925601
National Institute of Diabetes and Digestive and Kidney Disease, DK063491
National Institute of Diabetes and Digestive and Kidney Disease, R01DK089256
National Institute of Diabetes and Digestive and Kidney Disease, P30 DK072488
National Institute of Food and Agriculture, 2007-35205-17883
National Institute of Neurological Disorders and Stroke
National Institute on Aging, 263-MA-410953
National Institute on Aging, 263-MD-821336
National Institute on Aging, 263-MD-9164
National Institute on Aging, AG023629
National Institute on Aging, AG13196
National Institute on Aging, NO1AG12109
National Institute on Aging, P30AG10161
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National Institute on Aging, R01AG30146
National Institute of Arthritis and Musculoskeletal and Skin Diseases, 5-P60-AR30701
National Institute of Arthritis and Musculoskeletal and Skin Diseases, 5-P60-AR49465-03
National Institutes of Health, 1R01DK8925601
National Institutes of Health, 1RC2MH089951
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National Institutes of Health, 1Z01HG000024
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National Institutes of Health, AA014041
National Institutes of Health, AA07535
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National Institutes of Health, HL084729
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National Institutes of Health, N01HG65403
National Institutes of Health, R01DK093757
National Institutes of Health, R01DK075787
National Institutes of Health, R01HL71981
National Institutes of Health, R01MH59565
National Institutes of Health, R01MH59566
National Institutes of Health, R01MH59571
National Institutes of Health, R01MH59586
National Institutes of Health, R01MH59587
National Institutes of Health, R01MH59588
National Institutes of Health, R01MH60870
National Institutes of Health, R01MH60879
National Institutes of Health, R01MH61675
National Institutes of Health, R01MH67257
National Institutes of Health, R01MH81800
National Institutes of Health, U01HG004423
National Institutes of Health, U01HG004436
National Institutes of Health, U01HG004438
National Institutes of Health, U01HL072515-06
National Institutes of Health, U01HL105198
National Institutes of Health, U01HL84756
National Institutes of Health, U01MH79469
National Institutes of Health, U01MH79470
National Institutes of Health, U01NS069208-01
National Institutes of Health, UL1RR025005
National Institute for Health and Care Research, Biomedical Research Centre
Netherlands Heart Foundation, 2001 D 032
Netherlands Organisation for Scientific Research, Geestkracht program grant, 10-000-1002
Netherlands Organisation for Scientific Research, 050-060-810
Netherlands Organisation for Scientific Research, 100-001-004
Netherlands Organisation for Scientific Research, 175.010.2003.005
Netherlands Organisation for Scientific Research, 175.010.2005.011
Netherlands Organisation for Scientific Research, 175.010.2007.006
Netherlands Organisation for Scientific Research, 261-98-710
Netherlands Organisation for Scientific Research, 40-0056-98-9032
Netherlands Organisation for Scientific Research, 400-05-717
Netherlands Organisation for Scientific Research, 452-04-314
Netherlands Organisation for Scientific Research, 452-06-004
Netherlands Organisation for Scientific Research, 480-01-006
Netherlands Organisation for Scientific Research, 480-04-004
Netherlands Organisation for Scientific Research, 480-05-003
Netherlands Organisation for Scientific Research, 480-07-001
Netherlands Organisation for Scientific Research, 481-08-013
Netherlands Organisation for Scientific Research, 60-60600-97-118
Netherlands Organisation for Scientific Research, 904-61-090
Netherlands Organisation for Scientific Research, 904-61-193
Netherlands Organisation for Scientific Research, 911-03-012
Netherlands Organisation for Scientific Research, 985-10-002
Netherlands Organisation for Scientific Research, Addiction-31160008
Netherlands Organisation for Scientific Research, GB-MW 940-38-011
Netherlands Organization for the Health Research and Development, 91111025
Nordic Center of Excellence in Disease Genetics
Nordic Centre of Excellence on Systems, biology in controlled dietary interventions and cohort studies, SYSDIET, 070014
Northern Netherlands Collaboration of Provinces
Novo Nordisk Foundation
Department of Veterans Affairs
Ollqvist Foundation
Paavo Nurmi Foundation
Påhlssons Foundation
Päivikki and Sakari Sohlberg Foundation
Perklén Foundation
Republic of Croatia Ministry of Science, Education and Sports, 108-1080315-0302
Research Centre for Prevention and Health, the Capital Region of Denmark
Research Foundation of Copenhagen County
Research Institute for Diseases in the Elderly, 014-93-015
Reynold's Foundation
Foundation against Cancer
Royal Swedish Academy of Science
Russian Foundation for Basic Research, NWO-RFBR 047.017.043
National Institute of Mental Health, Rutgers University Cell and DNA Repository cooperative agreement, U24 MH068457-06
Samfundet Folkhälsan
Sigrid Juselius Foundation
Social Insurance Institution of Finland, Kuopio, Tampere and Turku University, Hospital Medical Funds, 9M048
Social Insurance Institution of Finland, Kuopio, Tampere and Turku University, Hospital Medical Funds, 9N035
Social Ministry of the Federal State of Mecklenburg-West Pomerania
Société Francophone du 358 Diabète
South Tyrolean Sparkasse Foundation
Stichting Nationale Computerfaciliteiten
Strategic Cardiovascular Programme of Karolinska Institutet and the Stockholm County Council, 560183
Susan G. Komen Breast Cancer Foundation
Swedish Cancer Society
Swedish Cultural Foundation in Finland
Swedish Diabetes Association
Swedish Diabetes Foundation, 2013-024
Swedish Foundation for Strategic Research, ICA08-0047
Swedish Heart-Lung Foundation, 20120197
Swedish Medical Research Council, K2007-66X-20270-01-3,
Swedish Medical Research Council, 2012-1397
Swedish Ministry for Higher Education
Swedish Research Council, 8691
Swedish Research Council, M-2005-1112
Swedish Research Council, 2009-2298
Swedish Society for Medical Research
Swiss National Science Foundation, 31003A-143914
Swiss National Science Foundation, 3200B0105993
Swiss National Science Foundation, 3200B0-118308
Swiss National Science Foundation, 33CSCO-122661
Swiss National Science Foundation, 33CS30-139468
Swiss National Science Foundation, 33CS30-148401
SystemsX.ch, 51RTP0_151019
Tampere Tuberculosis Foundation
TEKES, 70103/06
TEKES, 40058/07
The Paul Michael Donovan Charitable Foundation
Torsten and Ragnar Söderberg Foundation
Umeå Medical Research Foundation
United Kingdom NIHR Cambridge Biomedical Research Centre
Universities and Research of the Autonomous Province of Bolzano, South Tyrol
University Hospital of Regensburg, ReForM A
University Hospital of Regensburg, ReForM C
University Hospital Oulu, Biocenter, University of Oulu, Finland, 75617
University Medical Center Groningen
University of Groningen
University of Maryland General Clinical Research Center, M01RR16500
University of Maryland General Clinical Research Center, AG000219
University of Tartu, SP1GVARENG
University of Tromsø, Norwegian Research Council, 185764
Västerbottens Intervention Programme
Velux Foundation
VU University Institute for Health and Care Research, EMGO+
Neuroscience Campus Amsterdam
Wellcome Trust, 064890
Wellcome Trust, 068545/Z/02
Wellcome Trust, 076113/B/04/Z
Wellcome Trust, 077016/Z/05/Z
Wellcome Trust, 079895
Wellcome Trust, 084723/Z/08/Z
Wellcome Trust, 086596/Z/08/Z
Wellcome Trust, 088869/B/09/Z
Wellcome Trust, 089062
Wellcome Trust, 090532
Wellcome Trust, 098017
Wellcome Trust, 098051
Wellcome Trust, 098381
Western Australian DNA Bank
Yrjö Jahnsson Foundation, 56358
Zorg Onderzoek Nederland-Medische Wetenschappen, KWF Kankerbestrijding, Stichting, Centraal Fonds Reserves van voormalig Vrijwillige Ziekenfondsverzekeringen
Publication Date
2015-10-01
Language
English
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Notes
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2024-01-11