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Research Article

A Genome-Wide Association Meta-Analysis of Circulating Sex Hormone–Binding Globulin Reveals Multiple Loci Implicated in Sex Steroid Hormone Regulation

  • Andrea D. Coviello equal contributor,

    equal contributor Contributed equally to this work with: Andrea D. Coviello, Robin Haring, Melissa Wellons, Dhananjay Vaidya, Terho Lehtimäki, Sarah Keildson

    Affiliations: Section of Preventive Medicine and Epidemiology, Boston University School of Medicine, Boston, Massachusetts, United States of America, Section of Endocrinology, Diabetes, and Nutrition, Boston University School of Medicine, Boston, Massachusetts, United States of America, National Heart, Lung, and Blood Institute's The Framingham Heart Study, Framingham, Massachusetts, United States of America

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  • Robin Haring equal contributor,

    equal contributor Contributed equally to this work with: Andrea D. Coviello, Robin Haring, Melissa Wellons, Dhananjay Vaidya, Terho Lehtimäki, Sarah Keildson

    Affiliation: Institute for Clinical Chemistry and Laboratory Medicine, University Medicine, Ernst-Moritz-Arndt University of Greifswald, Greifswald, Germany

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  • Melissa Wellons equal contributor,

    equal contributor Contributed equally to this work with: Andrea D. Coviello, Robin Haring, Melissa Wellons, Dhananjay Vaidya, Terho Lehtimäki, Sarah Keildson

    Affiliation: Department of Medicine and Department of Obstetrics and Gynecology, The University of Alabama at Birmingham, Birmingham, Alabama, United States of America

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  • Dhananjay Vaidya equal contributor,

    equal contributor Contributed equally to this work with: Andrea D. Coviello, Robin Haring, Melissa Wellons, Dhananjay Vaidya, Terho Lehtimäki, Sarah Keildson

    Affiliation: Department of Medicine, Johns Hopkins University, Baltimore, Maryland, United States of America

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  • Terho Lehtimäki equal contributor,

    equal contributor Contributed equally to this work with: Andrea D. Coviello, Robin Haring, Melissa Wellons, Dhananjay Vaidya, Terho Lehtimäki, Sarah Keildson

    Affiliation: Department of Clinical Chemistry, Fimlab Laboratories, Tampere University Hospital and University of Tampere School of Medicine, Tampere, Finland

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  • Sarah Keildson equal contributor,

    equal contributor Contributed equally to this work with: Andrea D. Coviello, Robin Haring, Melissa Wellons, Dhananjay Vaidya, Terho Lehtimäki, Sarah Keildson

    Affiliation: Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford, United Kingdom

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  • Kathryn L. Lunetta,

    Affiliation: Department of Biostatistics, Boston University School of Public Health, Boston, Massachusetts, United States of America

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  • Chunyan He,

    Affiliations: Department of Public Health, Indiana University School of Medicine, Indianapolis, Indiana, United States of America, Melvin and Bren Simon Cancer Center, Indiana University, Indianapolis, Indiana, United States of America

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  • Myriam Fornage,

    Affiliation: University of Texas Health Sciences Center at Houston, Houston, Texas, United States of America

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  • Vasiliki Lagou,

    Affiliations: Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford, United Kingdom, Oxford Centre for Diabetes, Endocrinology, and Metabolism, University of Oxford, Oxford, United Kingdom

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  • Massimo Mangino,

    Affiliation: Department of Twin Research and Genetic Epidemiology, King's College London, London, United Kingdom

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  • N. Charlotte Onland-Moret,

    Affiliation: Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht, The Netherlands

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  • Brian Chen,

    Affiliation: Program on Genomics and Nutrition and the Center for Metabolic Disease Prevention, School of Public Health, University of California Los Angeles, Los Angeles, California, United States of America

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  • Joel Eriksson,

    Affiliation: Center for Bone and Arthritis Research, Institute of Medicine, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden

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  • Melissa Garcia,

    Affiliation: Laboratory of Epidemiology, Demography, and Biometry, National Institute on Aging, Bethesda, Maryland, United States of America

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  • Yong Mei Liu,

    Affiliations: Wake Forest University School of Medicine, Winston-Salem, North Carolina, United States of America, Department of Epidemiology and Prevention, Division of Public Health Sciences, Wake Forest University Health Sciences, Winston-Salem, North Carolina, United States of America

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  • Annemarie Koster,

    Affiliation: Laboratory of Epidemiology, Demography, and Biometry, National Institute on Aging, Bethesda, Maryland, United States of America

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  • Kurt Lohman,

    Affiliation: Wake Forest University School of Medicine, Winston-Salem, North Carolina, United States of America

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  • Leo-Pekka Lyytikäinen,

    Affiliation: Department of Clinical Chemistry, Fimlab Laboratories, Tampere University Hospital and University of Tampere School of Medicine, Tampere, Finland

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  • Ann-Kristin Petersen,

    Affiliation: Institute of Genetic Epidemiology, Helmholtz Zentrum München, Neuherberg, Germany

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  • Jennifer Prescott,

    Affiliations: Program in Molecular and Genetic Epidemiology, Department of Epidemiology, Harvard School of Public Health, Boston, Massachusetts, United States of America, Channing Laboratory, Department of Medicine, Brigham and Women's Hospital, and Harvard Medical School, Boston, Massachusetts, United States of America

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  • Lisette Stolk,

    Affiliations: Department of Internal Medicine, Erasmus MC, Rotterdam, The Netherlands, Netherlands Consortium of Healthy Aging, Rotterdam, The Netherlands

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  • Liesbeth Vandenput,

    Affiliation: Center for Bone and Arthritis Research, Institute of Medicine, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden

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  • Andrew R. Wood,

    Affiliation: Genetics of Complex Traits, Peninsula Medical School, University of Exeter, Exeter, United Kingdom

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  • Wei Vivian Zhuang,

    Affiliation: Department of Biostatistics, Boston University School of Public Health, Boston, Massachusetts, United States of America

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  • Aimo Ruokonen,

    Affiliation: Institute of Diagnostics, University of Oulu, Oulu, Finland

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  • Anna-Liisa Hartikainen,

    Affiliation: Department of Obstetrics and Gynecology, University Hospital of Oulu, Oulu, Finland

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  • Anneli Pouta,

    Affiliation: National Institute for Health and Welfare and Institute of Health Sciences, University of Oulu, Oulu, Finland

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  • Stefania Bandinelli,

    Affiliation: Geriatric Unit, Azienda Sanitaria di Firenze, Florence, Italy

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  • Reiner Biffar,

    Affiliation: Department of Prosthetic Dentistry, Gerostomatology, and Dental Materials, University of Greifswald, Greifswald, Germany

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  • Georg Brabant,

    Affiliation: Experimental and Clinical Endocrinology, University of Lübeck, Lübeck, Germany

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  • David G. Cox,

    Affiliations: Cancer Research Center of Lyon, INSERM U1052, Lyon, France, Department of Epidemiology and Biostatistics, School of Public Health, Imperial College, London, United Kingdom

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  • Yuhui Chen,

    Affiliation: Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford, United Kingdom

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  • Steven Cummings,

    Affiliation: California Pacific Medical Center, San Francisco, California, United States of America

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  • Luigi Ferrucci,

    Affiliation: Longitudinal Studies Section, Clinical Research Branch, National Institute on Aging, Baltimore, Maryland, United States of America

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  • Marc J. Gunter,

    Affiliation: Department of Epidemiology and Biostatistics, School of Public Health, Imperial College, London, United Kingdom

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  • Susan E. Hankinson,

    Affiliations: Channing Laboratory, Department of Medicine, Brigham and Women's Hospital, and Harvard Medical School, Boston, Massachusetts, United States of America, Division of Biostatistics and Epidemiology, University of Massachusetts, Amherst, Massachusetts, United States of America, Department of Epidemiology, Harvard School of Public Health, Boston, Massachusetts, United States of America

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  • Hannu Martikainen,

    Affiliation: Department of Obstetrics and Gynecology, University Hospital of Oulu, Oulu, Finland

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  • Albert Hofman,

    Affiliations: Netherlands Consortium of Healthy Aging, Rotterdam, The Netherlands, Department of Epidemiology, Erasmus MC, Rotterdam, The Netherlands

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  • Georg Homuth,

    Affiliation: Interfaculty Institute for Genetics and Functional Genomics, University of Greifswald, Greifswald, Germany

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  • Thomas Illig,

    Affiliations: Research Unit of Molecular Epidemiology, Helmholtz Zentrum München, Neuherberg, Germany, Hannover Unified Biobank, Hannover Medical School, Hannover, Germany

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  • John-Olov Jansson,

    Affiliation: Center for Bone and Arthritis Research, Institute of Medicine, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden

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  • Andrew D. Johnson,

    Affiliation: National Heart, Lung, and Blood Institute's The Framingham Heart Study, Framingham, Massachusetts, United States of America

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  • David Karasik,

    Affiliation: Hebrew SeniorLife Institute for Aging Research and Harvard Medical School, Boston, Massachusetts, United States of America

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  • Magnus Karlsson,

    Affiliation: Clinical and Molecular Osteoporosis Research Unit, Department of Clinical Sciences and Department of Orthopaedics, Lund University, Malmö, Sweden

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  • Johannes Kettunen,

    Affiliations: Institute for Molecular Medicine Finland (FIMM), University of Helsinki, Helsinki, Finland, Department of Chronic Disease Prevention, National Institute for Health and Welfare, Helsinki, Finland

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  • Douglas P. Kiel,

    Affiliation: Hebrew SeniorLife Institute for Aging Research and Harvard Medical School, Boston, Massachusetts, United States of America

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  • Peter Kraft,

    Affiliation: Program in Molecular and Genetic Epidemiology, Department of Epidemiology, Harvard School of Public Health, Boston, Massachusetts, United States of America

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  • Jingmin Liu,

    Affiliation: Women's Health Initiative Clinical Coordinating Center, Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, Washington, United States of America

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  • Östen Ljunggren,

    Affiliation: Department of Medical Sciences, University of Uppsala, Uppsala, Sweden

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  • Mattias Lorentzon,

    Affiliation: Center for Bone and Arthritis Research, Institute of Medicine, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden

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  • Marcello Maggio,

    Affiliation: Department of Internal Medicine and Biomedical Sciences, Section of Geriatrics, University of Parma, Parma, Italy

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  • Marcello R. P. Markus,

    Affiliation: Institute for Community Medicine, University of Greifswald, Greifswald, Germany

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  • Dan Mellström,

    Affiliation: Center for Bone and Arthritis Research, Institute of Medicine, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden

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  • Iva Miljkovic,

    Affiliation: University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America

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  • Daniel Mirel,

    Affiliation: Gene Environment Initiative, Program in Medical and Population Genetics, Broad Institute of Harvard and MIT, Boston, Massachusetts, United States of America

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  • Sarah Nelson,

    Affiliation: Department of Biostatistics, University of Washington, Seattle, Washington, United States of America

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  • Laure Morin Papunen,

    Affiliation: Department of Obstetrics and Gynecology, University Hospital of Oulu, Oulu, Finland

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  • Petra H. M. Peeters,

    Affiliation: Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht, The Netherlands

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  • Inga Prokopenko,

    Affiliations: Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford, United Kingdom, Oxford Centre for Diabetes, Endocrinology, and Metabolism, University of Oxford, Oxford, United Kingdom

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  • Leslie Raffel,

    Affiliation: Medical Genetics Institute, Cedars-Sinai Medical Center, Los Angeles, California, United States of America

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  • Martin Reincke,

    Affiliation: Medizinische Klinik and Poliklinik IV, Ludwig-Maximilians University, Munich, Germany

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  • Alex P. Reiner,

    Affiliation: Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, Washington, United States of America

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  • Kathryn Rexrode,

    Affiliation: Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, United States of America

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  • Fernando Rivadeneira,

    Affiliations: Department of Internal Medicine, Erasmus MC, Rotterdam, The Netherlands, Netherlands Consortium of Healthy Aging, Rotterdam, The Netherlands

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  • Stephen M. Schwartz,

    Affiliation: Cardiovascular Health Research Unit, Department of Epidemiology, University of Washington, Seattle, Washington, United States of America

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  • David Siscovick,

    Affiliation: Cardiovascular Health Research Unit, Department of Epidemiology, University of Washington, Seattle, Washington, United States of America

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  • Nicole Soranzo,

    Affiliations: Department of Twin Research and Genetic Epidemiology, King's College London, London, United Kingdom, Human Genetics, Wellcome Trust Sanger Institute, Hinxton, United Kingdom

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  • Doris Stöckl,

    Affiliations: Institute of Epidemiology II, Helmholtz Zentrum München, Neuherberg, Germany, Department of Obstetrics and Gynaecology, Ludwig-Maximilians-University, Munich, Germany

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  • Shelley Tworoger,

    Affiliations: Channing Laboratory, Department of Medicine, Brigham and Women's Hospital, and Harvard Medical School, Boston, Massachusetts, United States of America, Department of Epidemiology, Harvard School of Public Health, Boston, Massachusetts, United States of America

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  • André G. Uitterlinden,

    Affiliations: Department of Internal Medicine, Erasmus MC, Rotterdam, The Netherlands, Netherlands Consortium of Healthy Aging, Rotterdam, The Netherlands, Department of Epidemiology, Erasmus MC, Rotterdam, The Netherlands

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  • Carla H. van Gils,

    Affiliation: Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht, The Netherlands

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  • Ramachandran S. Vasan,

    Affiliations: Section of Preventive Medicine and Epidemiology, Boston University School of Medicine, Boston, Massachusetts, United States of America, National Heart, Lung, and Blood Institute's The Framingham Heart Study, Framingham, Massachusetts, United States of America

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  • H.-Erich Wichmann,

    Affiliations: Institute of Epidemiology I, Helmholtz Zentrum München, Neuherberg, Germany, Institute of Medical Informatics, Biometry, and Epidemiology, Ludwig-Maximilians-Universität, Munich, Germany, Klinikum Großhadern, Munich, Germany

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  • Guangju Zhai,

    Affiliations: Department of Twin Research and Genetic Epidemiology, King's College London, London, United Kingdom, Discipline of Genetics, Faculty of Medicine, Memorial University of Newfoundland, St. John's, Newfoundland, Canada

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  • Shalender Bhasin,

    Affiliation: Section of Endocrinology, Diabetes, and Nutrition, Boston University School of Medicine, Boston, Massachusetts, United States of America

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  • Martin Bidlingmaier,

    Affiliation: Medizinische Klinik and Poliklinik IV, Ludwig-Maximilians University, Munich, Germany

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  • Stephen J. Chanock,

    Affiliation: Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, Maryland, United States of America

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  • Immaculata De Vivo,

    Affiliations: Program in Molecular and Genetic Epidemiology, Department of Epidemiology, Harvard School of Public Health, Boston, Massachusetts, United States of America, Channing Laboratory, Department of Medicine, Brigham and Women's Hospital, and Harvard Medical School, Boston, Massachusetts, United States of America

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  • Tamara B. Harris,

    Affiliation: Laboratory of Epidemiology, Demography, and Biometry, National Institute on Aging, Bethesda, Maryland, United States of America

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  • David J. Hunter,

    Affiliations: Program in Molecular and Genetic Epidemiology, Department of Epidemiology, Harvard School of Public Health, Boston, Massachusetts, United States of America, Channing Laboratory, Department of Medicine, Brigham and Women's Hospital, and Harvard Medical School, Boston, Massachusetts, United States of America

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  • Mika Kähönen,

    Affiliation: Department of Clinical Physiology, Tampere University Hospital and University of Tampere School of Medicine, Tampere, Finland

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  • Simin Liu,

    Affiliation: Program on Genomics and Nutrition, Department of Epidemiology, University of California Los Angeles, Los Angeles, California, United States of America

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  • Pamela Ouyang,

    Affiliation: Division of Cardiology, Johns Hopkins Bayview Medical Center, Baltimore, Maryland, United States of America

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  • Tim D. Spector,

    Affiliation: Department of Twin Research and Genetic Epidemiology, King's College London, London, United Kingdom

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  • Yvonne T. van der Schouw,

    Affiliation: Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht, The Netherlands

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  • Jorma Viikari,

    Affiliation: Department of Medicine, Turku University Hospital and University of Turku, Turku, Finland

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  • Henri Wallaschofski,

    Affiliation: Institute for Clinical Chemistry and Laboratory Medicine, University Medicine, Ernst-Moritz-Arndt University of Greifswald, Greifswald, Germany

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  • Mark I. McCarthy,

    Affiliations: Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford, United Kingdom, Oxford Centre for Diabetes, Endocrinology, and Metabolism, University of Oxford, Churchill Hospital, Oxford, United Kingdom, Oxford NIHR Biomedical Research Centre, Churchill Hospital, Oxford, United Kingdom

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  • Timothy M. Frayling,

    Affiliation: Genetics of Complex Traits, Peninsula Medical School, University of Exeter, Exeter, United Kingdom

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  • Anna Murray,

    Affiliation: Genetics of Complex Traits, Peninsula Medical School, University of Exeter, Exeter, United Kingdom

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  • Steve Franks,

    Affiliation: Institute of Reproductive and Developmental Biology, Imperial College London, London, United Kingdom

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  • Marjo-Riitta Järvelin ,

    Affiliations: Department of Biostatistics and Epidemiology, School of Public Health, MRC-HPA Centre for Environment and Health, Faculty of Medicine, Imperial College London, London, United Kingdom, Institute of Health Sciences, University of Oulu, Oulu, Finland, Biocenter Oulu, University of Oulu, Oulu, Finland, National Institute of Health and Welfare, University of Oulu, Oulu, Finland

    These authors also contributed equally to this work.

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  • Frank H. de Jong ,

    Affiliation: Department of Internal Medicine, Erasmus MC, Rotterdam, The Netherlands

    These authors also contributed equally to this work.

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  • Olli Raitakari ,

    Affiliation: Department of Clinical Physiology and Nuclear Medicine, Turku University Hospital and Research Centre of Applied and Preventive Cardiovascular Medicine, University of Turku, Turku, Finland

    These authors also contributed equally to this work.

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  • Alexander Teumer ,

    Affiliation: Interfaculty Institute for Genetics and Functional Genomics, University of Greifswald, Greifswald, Germany

    These authors also contributed equally to this work.

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  • Claes Ohlsson ,

    Affiliation: Center for Bone and Arthritis Research, Institute of Medicine, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden

    These authors also contributed equally to this work.

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  • Joanne M. Murabito mail,

    murabito@bu.edu (JM Murabito); John.perry@pms.ac.uk (JRB Perry)

    Affiliations: National Heart, Lung, and Blood Institute's The Framingham Heart Study, Framingham, Massachusetts, United States of America, Section of General Internal Medicine, Boston University School of Medicine, Boston, Massachusetts, United States of America

    These authors also contributed equally to this work.

    X
  • John R. B. Perry mail

    murabito@bu.edu (JM Murabito); John.perry@pms.ac.uk (JRB Perry)

    Affiliations: Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford, United Kingdom, Department of Twin Research and Genetic Epidemiology, King's College London, London, United Kingdom, Genetics of Complex Traits, Peninsula Medical School, University of Exeter, Exeter, United Kingdom

    These authors also contributed equally to this work.

    X
  • Published: July 19, 2012
  • DOI: 10.1371/journal.pgen.1002805

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