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Hundreds of variants clustered in genomic loci and biological pathways affect human height

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Lango Allen, Hana, Estrada, Karol, Lettre, Guillaume, Berndt, Sonja I., Weedon, Michael N., Rivadeneira, Fernando, Willer, Cristen J., Jackson, Anne U., Vedantam, Sailaja, Raychaudhuri, Soumya, Ferreira, Teresa, Wood, Andrew R., Weyant, Robert J., Segrè, Ayellet V., Speliotes, Elizabeth K., Wheeler, Eleanor, Soranzo, Nicole, Park, Ju-Hyun, Yang, Jian, Gudbjartsson, Daniel, Heard-Costa, Nancy L., Randall, Joshua C., Qi, Lu, Vernon Smith, Albert, Mägi, Reedik, Pastinen, Tomi, Liang, Liming, Heid, Iris M., Luan, Jian’an, Thorleifsson, Gudmar, Winkler, Thomas W., Goddard, Michael E., Sin Lo, Ken, Palmer, Cameron, Workalemahu, Tsegaselassie, Aulchenko, Yurii S., Johansson, Åsa, Carola Zillikens, M., Feitosa, Mary F., Esko, Tõnu, Johnson, Toby, Ketkar, Shamika, Kraft, Peter, Mangino, Massimo, Prokopenko, Inga, Absher, Devin, Albrecht, Eva, Ernst, Florian, Glazer, Nicole L., Hayward, Caroline, Hottenga, Jouke-Jan, Jacobs, Kevin B., Knowles, Joshua W., Kutalik, Zoltán, Monda, Keri L., Polasek, Ozren, Preuss, Michael, Rayner, Nigel W., Robertson, Neil R., Steinthorsdottir, Valgerdur, Tyrer, Jonathan P., Voight, Benjamin F., Wiklund, Fredrik, Xu, Jianfeng, Hua Zhao, Jing, Nyholt, Dale R., Pellikka, Niina, Perola, Markus, Perry, John R. B., Surakka, Ida, Tammesoo, Mari-Liis, Altmaier, Elizabeth L., Amin, Najaf, Aspelund, Thor, Bhangale, Tushar, Boucher, Gabrielle, Chasman, Daniel I., Chen, Constance, Coin, Lachlan, Cooper, Matthew N., Dixon, Anna L., Gibson, Quince, Grundberg, Elin, Hao, Ke, Juhani Junttila, M., Kaplan, Lee M., Kettunen, Johannes, König, Inke R., Kwan, Tony, Lawrence, Robert W., Levinson, Douglas F., Lorentzon, Mattias, McKnight, Barbara, Morris, Andrew P., Müller, Martina, Suh Ngwa, Julius, Purcell, Shaun, Rafelt, Suzanne, Salem, Rany M., Salvi, Erika, Sanna, Serena, Shi, Jianxin, Sovio, Ulla, Thompson, John R., Turchin, Michael C., Vandenput, Liesbeth, Verlaan, Dominique J., Vitart, Veronique, White, Charles C., Ziegler, Andreas, Almgren, Peter, Balmforth, Anthony J., Campbell, Harry, Citterio, Lorena, De Grandi, Alessandro, Dominiczak, Anna, Duan, Jubao, Elliott, Paul, Elosua, Roberto, Eriksson, Johan G., Freimer, Nelson B., Geus, Eco J. C., Glorioso, Nicola, Haiqing, Shen, Hartikainen, Anna-Liisa, Havulinna, Aki S., Hicks, Andrew A., Hui, Jennie, Igl, Wilmar, Illig, Thomas, Jula, Antti, Kajantie, Eero, Kilpeläinen, Tuomas O., Koiranen, Markku, Kolcic, Ivana, Koskinen, Seppo, Kovacs, Peter, Laitinen, Jaana, Liu, Jianjun, Lokki, Marja-Liisa, Marusic, Ana, Maschio, Andrea, Meitinger, Thomas, Mulas, Antonella, Paré, Guillaume, Parker, Alex N., Peden, John F., Petersmann, Astrid, Pichler, Irene, Pietiläinen, Kirsi H., Pouta, Anneli, Ridderstråle, Martin, Rotter, Jerome I., Sambrook, Jennifer G., Sanders, Alan R., Oliver Schmidt, Carsten, Sinisalo, Juha, Smit, Jan H., Stringham, Heather M., Bragi Walters, G., Widen, Elisabeth, Wild, Sarah H., Willemsen, Gonneke, Zagato, Laura, Zgaga, Lina, Zitting, Paavo, Alavere, Helene, Farrall, Martin, McArdle, Wendy L., Nelis, Mari, Peters, Marjolein J., Ripatti, Samuli, van Meurs, Joyce B. J., Aben, Katja K., Ardlie, Kristin G., Beckmann, Jacques S., Beilby, John P., Bergman, Richard N., Bergmann, Sven, Collins, Francis S., Cusi, Daniele, den Heijer, Martin, Eiriksdottir, Gudny, Gejman, Pablo V., Hall, Alistair S., Hamsten, Anders, Huikuri, Heikki V., Iribarren, Carlos, Kähönen, Mika, Kaprio, Jaakko, Kathiresan, Sekar, Kiemeney, Lambertus, Kocher, Thomas, Launer, Lenore J., Lehtimäki, Terho, Melander, Olle, Mosley Jr, Tom H., Musk, Arthur W., Nieminen, Markku S., O’Donnell, Christopher J., Ohlsson, Claes, Oostra, Ben, Palmer, Lyle J., Raitakari, Olli, Ridker, Paul M., Rioux, John D., Rissanen, Aila, Rivolta, Carlo, Schunkert, Heribert, Shuldiner, Alan R., Siscovick, David S., Stumvoll, Michael, Tönjes, Anke, Tuomilehto, Jaakko, van Ommen, Gert-Jan, Viikari, Jorma, Heath, Andrew C., Martin, Nicholas G., Montgomery, Grant W., Province, Michael A., Kayser, Manfred, Arnold, Alice M., Atwood, Larry D., Boerwinkle, Eric, Chanock, Stephen J., Deloukas, Panos, Gieger, Christian, Grönberg, Henrik, Hall, Per, Hattersley, Andrew T., Hengstenberg, Christian, Hoffman, Wolfgang, Mark Lathrop, G., Salomaa, Veikko, Schreiber, Stefan, Uda, Manuela, Waterworth, Dawn, Wright, Alan F., Assimes, Themistocles L., Barroso, Inês, Hofman, Albert, Mohlke, Karen L., Boomsma, Dorret I., Caulfield, Mark J., Adrienne Cupples, L., Erdmann, Jeanette, Fox, Caroline S., Gudnason, Vilmundur, Gyllensten, Ulf, Harris, Tamara B., Hayes, Richard B., Jarvelin, Marjo-Riitta, Mooser, Vincent, Munroe, Patricia B., Ouwehand, Willem H., Penninx, Brenda W., Pramstaller, Peter P., Quertermous, Thomas, Rudan, Igor, Samani, Nilesh J., Spector, Timothy D., Völzke, Henry, Watkins, Hugh, Wilson, James F., Groop, Leif C., Haritunians, Talin, Hu, Frank B., Kaplan, Robert C., Metspalu, Andres, North, Kari E., Schlessinger, David, Wareham, Nicholas J., Hunter, David J., O’Connell, Jeffrey R., Strachan, David P., Wichmann, H.-Erich, Borecki, Ingrid B., van Duijn, Cornelia M., Schadt, Eric E., Thorsteinsdottir, Unnur, Peltonen, Leena, Uitterlinden, André G., Visscher, Peter M., Chatterjee, Nilanjan, Loos, Ruth J. F., Boehnke, Michael, McCarthy, Mark I., Ingelsson, Erik, Lindgren, Cecilia M., Abecasis, Gonçalo R., Stefansson, Kari, Frayling, Timothy M., Hirschhorn, Joel N.·2010·Nature
DOI 10.1038/nature09410PMC PMC2955183
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Abstract

Most common human traits and diseases have a polygenic pattern of inheritance: DNA sequence variants at many genetic loci influence the phenotype. Genome-wide association (GWA) studies have identified more than 600 variants associated with human traits, but these typically explain small fractions of phenotypic variation, raising questions about the use of further studies. Here, using 183,727 individuals, we show that hundreds of genetic variants, in at least 180 loci, influence adult height, a highly heritable and classic polygenic trait. The large number of loci reveals patterns with important implications for genetic studies of common human diseases and traits. First, the 180 loci are not random, but instead are enriched for genes that are connected in biological pathways (P = 0.016) and that underlie skeletal growth defects (P < 0.001). Second, the likely causal gene is often located near the most strongly associated variant: in 13 of 21 loci containing a known skeletal growth gene, that gene was closest to the associated variant. Third, at least 19 loci have multiple independently associated variants, suggesting that allelic heterogeneity is a frequent feature of polygenic traits, that comprehensive explorations of already-discovered loci should discover additional variants and that an appreciable fraction of associated loci may have been identified. Fourth, associated variants are enriched for likely functional effects on genes, being over-represented among variants that alter amino-acid structure of proteins and expression levels of nearby genes. Our data explain approximately 10% of the phenotypic variation in height, and we estimate that unidentified common variants of similar effect sizes would increase this figure to approximately 16% of phenotypic variation (approximately 20% of heritable variation). Although additional approaches are needed to dissect the genetic architecture of polygenic human traits fully, our findings indicate that GWA studies can identify large numbers of loci that implicate biologically relevant genes and pathways.

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Authors
Lango Allen, H., Estrada, K., Lettre, G., Berndt, S. I., Weedon, M. N., Rivadeneira, F., Willer, C. J., Jackson, A. U., Vedantam, S., Raychaudhuri, S., Ferreira, T., Wood, A. R., Weyant, R. J., Segrè, A. V., Speliotes, E. K., Wheeler, E., Soranzo, N., Park, J.-H., Yang, J., Gudbjartsson, D., Heard-Costa, N. L., Randall, J. C., Qi, L., Vernon Smith, A., Mägi, R., Pastinen, T., Liang, L., Heid, I. M., Luan, J., Thorleifsson, G., Winkler, T. W., Goddard, M. E., Sin Lo, K., Palmer, C., Workalemahu, T., Aulchenko, Y. S., Johansson, Å., Carola Zillikens, M., Feitosa, M. F., Esko, T., Johnson, T., Ketkar, S., Kraft, P., Mangino, M., Prokopenko, I., Absher, D., Albrecht, E., Ernst, F., Glazer, N. L., Hayward, C., Hottenga, J.-J., Jacobs, K. B., Knowles, J. W., Kutalik, Z., Monda, K. L., Polasek, O., Preuss, M., Rayner, N. W., Robertson, N. R., Steinthorsdottir, V., Tyrer, J. P., Voight, B. F., Wiklund, F., Xu, J., Hua Zhao, J., Nyholt, D. R., Pellikka, N., Perola, M., Perry, J. R. B., Surakka, I., Tammesoo, M.-L., Altmaier, E. L., Amin, N., Aspelund, T., Bhangale, T., Boucher, G., Chasman, D. I., Chen, C., Coin, L., Cooper, M. N., Dixon, A. L., Gibson, Q., Grundberg, E., Hao, K., Juhani Junttila, M., Kaplan, L. M., Kettunen, J., König, I. R., Kwan, T., Lawrence, R. W., Levinson, D. F., Lorentzon, M., McKnight, B., Morris, A. P., Müller, M., Suh Ngwa, J., Purcell, S., Rafelt, S., Salem, R. M., Salvi, E., Sanna, S., Shi, J., Sovio, U., Thompson, J. R., Turchin, M. C., Vandenput, L., Verlaan, D. J., Vitart, V., White, C. C., Ziegler, A., Almgren, P., Balmforth, A. J., Campbell, H., Citterio, L., De Grandi, A., Dominiczak, A., Duan, J., Elliott, P., Elosua, R., Eriksson, J. G., Freimer, N. B., Geus, E. J. C., Glorioso, N., Haiqing, S., Hartikainen, A.-L., Havulinna, A. S., Hicks, A. A., Hui, J., Igl, W., Illig, T., Jula, A., Kajantie, E., Kilpeläinen, T. O., Koiranen, M., Kolcic, I., Koskinen, S., Kovacs, P., Laitinen, J., Liu, J., Lokki, M.-L., Marusic, A., Maschio, A., Meitinger, T., Mulas, A., Paré, G., Parker, A. N., Peden, J. F., Petersmann, A., Pichler, I., Pietiläinen, K. H., Pouta, A., Ridderstråle, M., Rotter, J. I., Sambrook, J. G., Sanders, A. R., Oliver Schmidt, C., Sinisalo, J., Smit, J. H., Stringham, H. M., Bragi Walters, G., Widen, E., Wild, S. H., Willemsen, G., Zagato, L., Zgaga, L., Zitting, P., Alavere, H., Farrall, M., McArdle, W. L., Nelis, M., Peters, M. J., Ripatti, S., van Meurs, J. B. J., Aben, K. K., Ardlie, K. G., Beckmann, J. S., Beilby, J. P., Bergman, R. N., Bergmann, S., Collins, F. S., Cusi, D., den Heijer, M., Eiriksdottir, G., Gejman, P. V., Hall, A. S., Hamsten, A., Huikuri, H. V., Iribarren, C., Kähönen, M., Kaprio, J., Kathiresan, S., Kiemeney, L., Kocher, T., Launer, L. J., Lehtimäki, T., Melander, O., Mosley Jr, T. H., Musk, A. W., Nieminen, M. S., O’Donnell, C. J., Ohlsson, C., Oostra, B., Palmer, L. J., Raitakari, O., Ridker, P. M., Rioux, J. D., Rissanen, A., Rivolta, C., Schunkert, H., Shuldiner, A. R., Siscovick, D. S., Stumvoll, M., Tönjes, A., Tuomilehto, J., van Ommen, G.-J., Viikari, J., Heath, A. C., Martin, N. G., Montgomery, G. W., Province, M. A., Kayser, M., Arnold, A. M., Atwood, L. D., Boerwinkle, E., Chanock, S. J., Deloukas, P., Gieger, C., Grönberg, H., Hall, P., Hattersley, A. T., Hengstenberg, C., Hoffman, W., Mark Lathrop, G., Salomaa, V., Schreiber, S., Uda, M., Waterworth, D., Wright, A. F., Assimes, T. L., Barroso, I., Hofman, A., Mohlke, K. L., Boomsma, D. I., Caulfield, M. J., Adrienne Cupples, L., Erdmann, J., Fox, C. S., Gudnason, V., Gyllensten, U., Harris, T. B., Hayes, R. B., Jarvelin, M.-R., Mooser, V., Munroe, P. B., Ouwehand, W. H., Penninx, B. W., Pramstaller, P. P., Quertermous, T., Rudan, I., Samani, N. J., Spector, T. D., Völzke, H., Watkins, H., Wilson, J. F., Groop, L. C., Haritunians, T., Hu, F. B., Kaplan, R. C., Metspalu, A., North, K. E., Schlessinger, D., Wareham, N. J., Hunter, D. J., O’Connell, J. R., Strachan, D. P., Wichmann, H.-E., Borecki, I. B., van Duijn, C. M., Schadt, E. E., Thorsteinsdottir, U., Peltonen, L., Uitterlinden, A. G., Visscher, P. M., Chatterjee, N., Loos, R. J. F., Boehnke, M., McCarthy, M. I., Ingelsson, E., Lindgren, C. M., Abecasis, G. R., Stefansson, K., Frayling, T. M., & Hirschhorn, J. N.
Affiliations
  • Erasmus MC (NL)
  • Montreal Heart Institute (CA)
  • National Institutes of Health (US)
  • University of Exeter (GB)
  • University of Michigan (US)
  • Broad Institute (US)
  • Centre for Human Genetics (GB)
  • Wellcome Sanger Institute (GB)
  • King's College London (GB)
  • QIMR Berghofer Medical Research Institute (AU)
  • deCODE Genetics (Iceland) (IS)
  • Brigham and Women's Hospital (US)
  • McGill University Health Centre (CA)
  • Harvard University (US)
  • Helmholtz Munich (DE)
  • Addenbrooke's Hospital (GB)
  • University Hospital Regensburg (DE)
  • The University of Melbourne (AU)
  • Uppsala University (SE)
  • Washington University in St. Louis (US)
  • Estonian Biocentre (EE)
  • University of London (GB)
  • HudsonAlpha Institute for Biotechnology (US)
  • Universität Greifswald (DE)
  • University of Washington (US)
  • Western General Hospital (GB)
  • Vrije Universiteit Amsterdam (NL)
  • National Cancer Institute (US)
  • Stanford Medicine (US)
  • SIB Swiss Institute of Bioinformatics (CH)
  • University of North Carolina at Chapel Hill (US)
  • University of Lübeck (DE)
  • University of Cambridge (GB)
  • Karolinska Institutet (SE)
  • Wake Forest University (US)
  • University of Helsinki (FI)
  • University of Tartu (EE)
  • University of Iceland (IS)
  • Imperial College London (GB)
  • The University of Western Australia (AU)
  • Royal National Hospital for Rheumatic Diseases (GB)
  • University of Maryland, Baltimore (US)
  • Merck & Co., Inc., Rahway, NJ, USA (United States) (US)
  • University of Gothenburg (SE)
  • University of Leicester (GB)
  • University of Milan (IT)
  • Institute of Genetic and Biomedical Research (IT)
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  • British Heart Foundation (GB)
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  • Genome Institute of Singapore (SG)
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  • McMaster University (CA)
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  • National Health Service (GB)
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  • University of Zagreb (HR)
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  • Karolinska University Hospital (SE)
  • Kaiser Permanente (US)
  • Tampere University Hospital (FI)
  • Radboud University Medical Center (NL)
  • Universitätsmedizin Greifswald (DE)
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  • GlaxoSmithKline (United States) (US)
  • National Heart, Lung, and Blood Institute (US)
  • NYU Langone Health (US)
  • University Medical Center Groningen (NL)
  • Albert Einstein College of Medicine (US)
  • National Institute on Aging (US)
  • Sage Bionetworks (US)
Corresponding author
  • Weedon, Michael N.
  • Abecasis, Gonçalo R.
  • Frayling, Timothy M.
  • Hirschhorn, Joel N.
ORCID
Venue
Nature
Publisher
Springer Science and Business Media LLC
Published
2010-09-29
Volume
467
Issue
7317
Pages
832-838
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
DOI
10.1038/nature09410
PMC
PMC2955183
OpenAlex
W2161998322
Cited by
1,945
References
32
Citations by year
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FWCI
115.72
Type
journal article
Language
en
Open access
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  • Wellcome Trust (068545/Z/02), 085301/Z/08/Z, 079771, 091746/Z/10/Z, 072856, 072960, 083270, 081682, 075491, 064890, 088885, 081682/Z/06/Z, 086596, 077016, 084183/Z/07/Z, 086596/Z/08/Z, 079557, 068545, 085301, 077016/Z/05/Z, 079895, 090532, 091746, ­076113/B/04/Z, 076113, 076113/C/04/Z)
  • Cancer Research UK
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  • National Institute on Aging (R01-AG-031890, N01-AG12100, N01-AG012100, Z01AG000675, N01 AG012109, Z01AG007380)
  • National Heart, Lung, and Blood Institute (N01-HC-85081, N01HC85085, N01-HC55022, N01 HC085086, N01HC-85083, U01HL72515, N01 HC055016, N01-HC-55018, HL 71981, N01HC15103, U01HL084729, R01HL071981, N01 HC 55020, N01 HC085079, R01‐HL043851, N01‐HC25195, N01 HC 55019, N01HC85082, N01HC‐75150, N01 HC85086, R01 HL-59367, R01HL087676, R01HL087652, U19HL069757, N01 HC035129, U01HL084756, N01HC85080, R01-HL087700, N02- HL-64278, N01 HC055018, N01 HC015103, N01 HC55222, R01HL087647, HL-084729, U01HL069757, N01‐HC‐45133, R01 HL087679, N01-HC-025195, ­N01-HC55016, R01HL087641, N01 HC055022, HL 69757, R01HL059367, U01HL080295, U01HL072515, N01 HC055222, R01HL088119, K99-HL094535, N01‐HC‐55015, N01-HC55021, N01 HC075150, R01HL117078, N01 HC055015, N01 HC045133, R01HL086694, N01-HC85079, ­N01-HC85084, N01HC35129)
  • National Institute of Mental Health (R01 MH61675, U01-MH79470, R01MH059160, R01 MH-59571, R01MH59588, R01-MH59566, R01-MH60879, R01-MH79469, R01-MH60870, R01-MH59586, R01MH059566, R01MH063706, R01 MH81800, R01MH59587, R01-MH59565, R01MH059571, R01MH060879, R01MH059565, RL1-MH083268, R01MH081800, R01-MH63706, R01 MH-67257, R01MH060870, U01MH079469, R01MH061675, R01MH059586, MH084698, R01MH059588, R01MH067257, U01MH079470, R01MH084698, R01MH059587, U01MH-79469)
  • National Institute on Drug Abuse (R56DA012854, DA12854, R01DA012854)
  • National Human Genome Research Institute (Z01HG000024, HG005581, HG005214, U01HG004399, U01HG004402, R01HG002651, U01HG005214, N01 HG065403, T32 HG-00040, HG002651, RC2HG005581, T32HG000040)
  • National Cancer Institute (CA-49449, R01CA065725, CA-87969, U01CA067262, CA67262, P01CA087969, R01CA104021, R01‐CA049449, CA 65725, CA50385, CA 047988, U01CA098233, R01CA050385, U01CA049449, R01CA047988, R01CA067262)
  • National Institute of General Medical Sciences (U01GM074518)
  • National Institute of Diabetes and Digestive and Kidney Diseases (R01DK073490, R01DK091718, DK063491, DK-072193, R01DK072193, R01DK089256, U01DK062370, R01DK058845, R01-DK068336, R01DK075681, P30DK046200, R56DK062370, F32DK079466, K23DK080145, U01DK062418, DK079466, P30DK072488, DK-062370, DK58845, DK080145, R01DK075787, P30DK063491, R01DK062370, DK46200.)
  • National Institute of Arthritis and Musculoskeletal and Skin Diseases (K08AR055688)
  • National Center for Research Resources (U54-RR020278, UL1RR025005, M01RR000425, M01-RR00425)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Physical Performance
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and phenotypic traits in livestock
Keywords
human height, genetic variants, genetic loci, polygenic inheritance, biological pathways, causal genes, allelic heterogeneity, heritability
MeSH terms
Body Height, Chromosomes, Human, Pair 3, Humans, Phenotype, Genome, Human, Genetic Predisposition to Disease, Multifactorial Inheritance, Polymorphism, Single Nucleotide, Metabolic Networks and Pathways, Genome-Wide Association Study, Genetic Loci

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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