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Cited by 972Genetic Associations and EpidemiologyLipoproteins and Cardiovascular HealthGenetic Mapping and Diversity in Plants and Animals

The power of genetic diversity in genome-wide association studies of lipids

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Graham, Sarah E., Clarke, Shoa L., Wu, Kuan-Han H., Kanoni, Stavroula, Zajac, Greg J. M., Ramdas, Shweta, Surakka, Ida, Ntalla, Ioanna +520 more·2021·Nature
DOI 10.1038/s41586-021-04064-3PMC PMC8730582
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Abstract

Increased blood lipid levels are heritable risk factors of cardiovascular disease with varied prevalence worldwide owing to different dietary patterns and medication use 1. Despite advances in prevention and treatment, in particular through reducing low-density lipoprotein cholesterol levels 2, heart disease remains the leading cause of death worldwide 3. Genome-wideassociation studies (GWAS) of blood lipid levels have led to important biological and clinical insights, as well as new drug targets, for cardiovascular disease. However, most previous GWAS 4-23 have been conducted in European ancestry populations and may have missed genetic variants that contribute to lipid-level variation in other ancestry groups. These include differences in allele frequencies, effect sizes and linkage-disequilibrium patterns 24. Here we conduct a multi-ancestry, genome-wide genetic discovery meta-analysis of lipid levels in approximately 1.65 million individuals, including 350,000 of non-European ancestries. We quantify the gain in studying non-European ancestries and provide evidence to support the expansion of recruitment of additional ancestries, even with relatively small sample sizes. We find that increasing diversity rather than studying additional individuals of European ancestry results in substantial improvements in fine-mapping functional variants and portability of polygenic prediction (evaluated in approximately 295,000 individuals from 7 ancestry groupings). Modest gains in the number of discovered loci and ancestry-specific variants were also achieved. As GWAS expand emphasis beyond the identification of genes and fundamental biology towards the use of genetic variants for preventive and precision medicine 25, we anticipate that increased diversity of participants will lead to more accurate and equitable 26 application of polygenic scores in clinical practice.

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  • The result that cross-population PGS outperformed ancestry-matched PGSs replicated previous studies showing that multi-ancestry PGS demonstrated improved prediction performance relative to ancestry-matched PGSs.

    “This result replicated previous studies showing that multi-ancestry PGS demonstrated an improved prediction performance relative to ancestry-matched PGSs41,42.”

    From Shared genetic architectures of educational attainment in East Asian and European populations (2024) · cites this paper as [41]

    The ‘Trans-ancestry PRS are most predictive’ section reports that trans-ancestry scores had the best or near-best performance across the groups tested. It describes prediction relative to ancestry-matched scores as ‘improved or comparable,’ so the claim overstates the finding by presenting improvement without that qualification. (LLM, conf=0.84)

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  1. [34]Lehmann BCL, Mackintosh M, McVean G & Holmes CC High trait variability in optimal polygenic prediction strategy within multiple-ancestry cohorts. bioRxiv, 2021.2001.2015.426781, doi: 10.1101/2021.01.15.426781 (2021). · DOI

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Graham, S. E., Clarke, S. L., Wu, K.-H. H., Kanoni, S., Zajac, G. J. M., Ramdas, S., Surakka, I., Ntalla, I., Vedantam, S., Winkler, T. W., Locke, A. E., Marouli, E., Hwang, M. Y., Han, S., Narita, A., Choudhury, A., Bentley, A. R., Ekoru, K., Verma, A., Trivedi, B., Martin, H. C., Hunt, K. A., Hui, Q., Klarin, D., Zhu, X., Thorleifsson, G., Helgadottir, A., Gudbjartsson, D. F., Holm, H., Olafsson, I., Akiyama, M., Sakaue, S., Terao, C., Kanai, M., Zhou, W., Brumpton, B. M., Rasheed, H., Ruotsalainen, S. E., Havulinna, A. S., Veturi, Y., Feng, Q., Rosenthal, E. A., Lingren, T., Pacheco, J. A., Pendergrass, S. A., Haessler, J., Giulianini, F., Bradford, Y., Miller, J. E., Campbell, A., Lin, K., Millwood, I. Y., Hindy, G., Rasheed, A., Faul, J. D., Zhao, W., Weir, D. R., Turman, C., Huang, H., Graff, M., Mahajan, A., Brown, M. R., Zhang, W., Yu, K., Schmidt, E. M., Pandit, A., Gustafsson, S., Yin, X., Luan, J., Zhao, J.-H., Matsuda, F., Jang, H.-M., Yoon, K., Medina-Gomez, C., Pitsillides, A., Hottenga, J. J., Willemsen, G., Wood, A. R., Ji, Y., Gao, Z., Haworth, S., Mitchell, R. E., Chai, J. F., Aadahl, M., Yao, J., Manichaikul, A., Warren, H. R., Ramirez, J., Bork-Jensen, J., Kårhus, L. L., Goel, A., Sabater-Lleal, M., Noordam, R., Sidore, C., Fiorillo, E., McDaid, A. F., Marques-Vidal, P., Wielscher, M., Trompet, S., Sattar, N., Møllehave, L. T., Thuesen, B. H., Munz, M., Zeng, L., Huang, J., Yang, B., Poveda, A., Kurbasic, A., Lamina, C., Forer, L., Scholz, M., Galesloot, T. E., Bradfield, J. P., Daw, E. W., Zmuda, J. M., Mitchell, J. S., Fuchsberger, C., Christensen, H., Brody, J. A., Feitosa, M. F., Wojczynski, M. K., Preuss, M., Mangino, M., Christofidou, P., Verweij, N., Benjamins, J. W., Engmann, J., Kember, R. L., Slieker, R. C., Lo, K. S., Zilhao, N. R., Le, P., Kleber, M. E., Delgado, G. E., Huo, S., Ikeda, D. D., Iha, H., Yang, J., Liu, J., Leonard, H. L., Marten, J., Schmidt, B., Arendt, M., Smyth, L. J., Cañadas-Garre, M., Wang, C., Nakatochi, M., Wong, A., Hutri-Kähönen, N., Sim, X., Xia, R., Huerta-Chagoya, A., Fernandez-Lopez, J. C., Lyssenko, V., Ahmed, M., Jackson, A. U., Yousri, N. A., Irvin, M. R., Oldmeadow, C., Kim, H.-N., Ryu, S., Timmers, P. R. H. J., Arbeeva, L., Dorajoo, R., Lange, L. A., Chai, X., Prasad, G., Lorés-Motta, L., Pauper, M., Long, J., Li, X., Theusch, E., Takeuchi, F., Spracklen, C. N., Loukola, A., Bollepalli, S., Warner, S. C., Wang, Y. X., Wei, W. B., Nutile, T., Ruggiero, D., Sung, Y. J., Hung, Y.-J., Chen, S., Liu, F., Yang, J., Kentistou, K. A., Gorski, M., Brumat, M., Meidtner, K., Bielak, L. F., Smith, J. A., Hebbar, P., Farmaki, A.-E., Hofer, E., Lin, M., Xue, C., Zhang, J., Concas, M. P., Vaccargiu, S., van der Most, P. J., Pitkänen, N., Cade, B. E., Lee, J., van der Laan, S. W., Chitrala, K. N., Weiss, S., Zimmermann, M. E., Lee, J. Y., Choi, H. S., Nethander, M., Freitag-Wolf, S., Southam, L., Rayner, N. W., Wang, C. A., Lin, S.-Y., Wang, J.-S., Couture, C., Lyytikäinen, L.-P., Nikus, K., Cuellar-Partida, G., Vestergaard, H., Hildalgo, B., Giannakopoulou, O., Cai, Q., Obura, M. O., van Setten, J., Li, X., Schwander, K., Terzikhan, N., Shin, J. H., Jackson, R. D., Reiner, A. P., Martin, L. W., Chen, Z., Li, L., Highland, H. M., Young, K. L., Kawaguchi, T., Thiery, J., Bis, J. C., Nadkarni, G. N., Launer, L. J., Li, H., Nalls, M. A., Raitakari, O. T., Ichihara, S., Wild, S. H., Nelson, C. P., Campbell, H., Jäger, S., Nabika, T., Al-Mulla, F., Niinikoski, H., Braund, P. S., Kolcic, I., Kovacs, P., Giardoglou, T., Katsuya, T., Bhatti, K. F., de Kleijn, D., de Borst, G. J., Kim, E. K., Adams, H. H. H., Ikram, M. A., Zhu, X., Asselbergs, F. W., Kraaijeveld, A. O., Beulens, J. W. J., Shu, X.-O., Rallidis, L. S., Pedersen, O., Hansen, T., Mitchell, P., Hewitt, A. W., Kähönen, M., Pérusse, L., Bouchard, C., Tönjes, A., Chen, Y.-D. I., Pennell, C. E., Mori, T. A., Lieb, W., Franke, A., Ohlsson, C., Mellström, D., Cho, Y. S., Lee, H., Yuan, J.-M., Koh, W.-P., Rhee, S. Y., Woo, J.-T., Heid, I. M., Stark, K. J., Völzke, H., Homuth, G., Evans, M. K., Zonderman, A. B., Polasek, O., Pasterkamp, G., Hoefer, I. E., Redline, S., Pahkala, K., Oldehinkel, A. J., Snieder, H., Biino, G., Schmidt, R., Schmidt, H., Chen, Y. E., Bandinelli, S., Dedoussis, G., Thanaraj, T. A., Kardia, S. L. R., Kato, N., Schulze, M. B., Girotto, G., Jung, B., Böger, C. A., Joshi, P. K., Bennett, D. A., De Jager, P. L., Lu, X., Mamakou, V., Brown, M., Caulfield, M. J., Munroe, P. B., Guo, X., Ciullo, M., Jonas, J. B., Samani, N. J., Kaprio, J., Pajukanta, P., Adair, L. S., Bechayda, S. A., de Silva, H. J., Wickremasinghe, A. R., Krauss, R. M., Wu, J.-Y., Zheng, W., den Hollander, A. I., Bharadwaj, D., Correa, A., Wilson, J. G., Lind, L., Heng, C.-K., Nelson, A. E., Golightly, Y. M., Wilson, J. F., Penninx, B., Kim, H.-L., Attia, J., Scott, R. J., Rao, D. C., Arnett, D. K., Hunt, S. C., Walker, M., Koistinen, H. A., Chandak, G. R., Yajnik, C. S., Mercader, J. M., Tusié-Luna, T., Aguilar-Salinas, C. A., Villalpando, C. G., Orozco, L., Fornage, M., Tai, E. S., van Dam, R. M., Lehtimäki, T., Chaturvedi, N., Yokota, M., Liu, J., Reilly, D. F., McKnight, A. J., Kee, F., Jöckel, K.-H., McCarthy, M. I., Palmer, C. N. A., Vitart, V., Hayward, C., Simonsick, E., van Duijn, C. M., Lu, F., Qu, J., Hishigaki, H., Lin, X., März, W., Parra, E. J., Cruz, M., Gudnason, V., Tardif, J.-C., Lettre, G., ’t Hart, L. M., Elders, P. J. M., Damrauer, S. M., Kumari, M., Kivimaki, M., van der Harst, P., Spector, T. D., Loos, R. J. F., Province, M. A., Psaty, B. M., Brandslund, I., Pramstaller, P. P., Christensen, K., Ripatti, S., Widén, E., Hakonarson, H., Grant, S. F. A., Kiemeney, L. A. L. M., de Graaf, J., Loeffler, M., Kronenberg, F., Gu, D., Erdmann, J., Schunkert, H., Franks, P. W., Linneberg, A., Jukema, J. W., Khera, A. V., Männikkö, M., Jarvelin, M.-R., Kutalik, Z., Cucca, F., Mook-Kanamori, D. O., van Dijk, K. W., Watkins, H., Strachan, D. P., Grarup, N., Sever, P., Poulter, N., Rotter, J. I., Dantoft, T. M., Karpe, F., Neville, M. J., Timpson, N. J., Cheng, C.-Y., Wong, T.-Y., Khor, C. C., Sabanayagam, C., Peters, A., Gieger, C., Hattersley, A. T., Pedersen, N. L., Magnusson, P. K. E., Boomsma, D. I., de Geus, E. J. C., Cupples, L. A., van Meurs, J. B. J., Ghanbari, M., Gordon-Larsen, P., Huang, W., Kim, Y. J., Tabara, Y., Wareham, N. J., Langenberg, C., Zeggini, E., Kuusisto, J., Laakso, M., Ingelsson, E., Abecasis, G., Chambers, J. C., Kooner, J. S., de Vries, P. S., Morrison, A. C., North, K. E., Daviglus, M., Kraft, P., Martin, N. G., Whitfield, J. B., Abbas, S., Saleheen, D., Walters, R. G., Holmes, M. V., Black, C., Smith, B. H., Justice, A. E., Baras, A., Buring, J. E., Ridker, P. M., Chasman, D. I., Kooperberg, C., Wei, W.-Q., Jarvik, G. P., Namjou, B., Hayes, M. G., Ritchie, M. D., Jousilahti, P., Salomaa, V., Hveem, K., Åsvold, B. O., Kubo, M., Kamatani, Y., Okada, Y., Murakami, Y., Thorsteinsdottir, U., Stefansson, K., Ho, Y.-L., Lynch, J. A., Rader, D. J., Tsao, P. S., Chang, K.-M., Cho, K., O’Donnell, C. J., Gaziano, J. M., Wilson, P., Rotimi, C. N., Hazelhurst, S., Ramsay, M., Trembath, R. C., van Heel, D. A., Tamiya, G., Yamamoto, M., Kim, B.-J., Mohlke, K. L., Frayling, T. M., Hirschhorn, J. N., Kathiresan, S., Program, V. M. V., Global Lipids Genetics Consortium*, Boehnke, M., Natarajan, P., Peloso, G. M., Brown, C. D., Morris, A. P., Assimes, T. L., Deloukas, P., Sun, Y. V., & Willer, C. J.
Affiliations
  • University of Michigan (US)
  • VA Palo Alto Health Care System (US)
  • Queen Mary University of London (GB)
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  • Broad Institute (US)
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  • Korea National Institute of Health (KR)
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Corresponding author
Sun, Yan V.
ORCID
Venue
Nature
Publisher
Springer Science and Business Media LLC
Published
2021-12-09
Volume
600
Issue
7890
Pages
675-679
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
DOI
10.1038/s41586-021-04064-3
PMC
PMC8730582
OpenAlex
W3205644245
Cited by
972
References
77
Citations by year
2026: 164 · 2025: 246 · 2024: 274 · 2023: 192 · 2022: 89 · 2021: 6 · 2012: 1
FWCI
21.98
Type
journal article
Language
en
Update notices
correction (2023-05-26)
Open access
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Funders
  • U.S. Department of Veterans Affairs (IK2-CX001780, I01-BX004821, I01-BX003362)
  • McKnight Foundation
  • Office of Research and Development
  • Wellcome Trust (212946/Z/18/Z, 212945/Z/18/Z, 210561/Z/18/Z, 217065/Z/19/Z, 202802/Z/16/Z, 221854/Z/20/Z)
  • Barts Charity (MGU0284)
  • Cancer Research UK (16896)
  • National Institute for Health and Care Research (NF-SI-0611-10170, NF-SI-0512-10113, NIHR-INF-0987, 16/136/102, NF-SI-0617-10154)
  • British Heart Foundation (FS/19/62/34901D, RG/14/5/30893)
  • Public Health Agency (STL/5569/19)
  • Lundbeckfonden (R155-2013-14070)
  • Novo Nordisk Fonden (NNF14OC0010513, NNF19OC0055250, NNF18OC0033898, NNF13OC0005785)
  • National Institutes of Health (5k01hl135405-04, 24460, 85,86)
  • Medical Research Council (MR/S019669/1, MC_PC_14135, MC_UU_00017/1, MR/S011676/1, MR/R024227/1, MC_PC_15018, MC_PC_20026, MC_PC_19009, MC_UU_00007/10, MC_PC_13049)
  • Economic and Social Research Council (ES/N00812X/1, ES/L008459/1)
  • Japan Society for the Promotion of Science (21H03206, 21K10439, 19K19434, 21H04850)
  • National Institute on Aging (R01AG017917, R01AG015819, P30AG010161)
  • National Heart, Lung, and Blood Institute (R01HL133218, R01HL127564, R03HL154284, K01-HL135405, R35HL135818, R01HL149683, R35HL135824, R01HL105756, R01HL109946, R01HL153805)
  • National Human Genome Research Institute (K08HG010155, R01HG010297, T32HG000040, U01HG011723)
  • National Cancer Institute (R01CA144034, R01CA080205, UM1CA182876)
  • National Institute of Diabetes and Digestive and Kidney Diseases (R01DK072193, U01DK062370, P30DK020572, R01DK093757, P30DK020541, R01DK062370)
  • National Center for Chronic Disease Prevention and Health Promotion (U01DP006266)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD030880)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
  • Health Sciences › Medicine › Surgery › Lipoproteins and Cardiovascular Health
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Mapping and Diversity in Plants and Animals
Keywords
serum lipids, genetic diversity, non-European ancestry, polygenic risk score, fine mapping, cardiovascular risk, LDL cholesterol, triglycerides, HDL cholesterol, genetic ancestry, sample size and statistical power, linkage disequilibrium
MeSH terms
Cardiovascular Diseases, Humans, Linkage Disequilibrium, Genetic Predisposition to Disease, Multifactorial Inheritance, Polymorphism, Single Nucleotide, Population Groups, Genome-Wide Association Study

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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