A Likelihood Ratio Approach for Utilizing Case-Control Data in the Clinical Classification of Rare Sequence Variants: Application to BRCA1 and BRCA2
Human Mutation, vol. 2023, pp. 1–17
Abstract
A large number of variants identified through clinical genetic testing in disease susceptibility genes are of uncertain significance (VUS). Following the recommendations of the American College of Medical Genetics and Genomics (ACMG) and Association for Molecular Pathology (AMP), the frequency in case-control datasets (PS4 criterion) can inform their interpretation. We present a novel case-control likelihood ratio-based method that incorporates gene-specific age-related penetrance. We demonstrate the utility of this method in the analysis of simulated and real datasets. In the analysis of simulated data, the likelihood ratio method was more powerful compared to other methods. Likelihood ratios were calculated for a case-control dataset of BRCA1 and BRCA2 variants from the Breast Cancer Association Consortium (BCAC) and compared with logistic regression results. A larger number of variants reached evidence in favor of pathogenicity, and a substantial number of variants had evidence against pathogenicity—findings that would not have been reached using other case-control analysis methods. Our novel method provides greater power to classify rare variants compared with classical case-control methods. As an initiative from the ENIGMA Analytical Working Group, we provide user-friendly scripts and preformatted Excel calculators for implementation of the method for rare variants in BRCA1, BRCA2, and other high-risk genes with known penetrance.
Authors 99
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Cyprus Institute of Neurology and Genetics
Affiliation as printed
Biostatistics Unit, The Cyprus Institute of Neurology and Genetics, Nicosia, Cyprus
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Cyprus Institute of Neurology and Genetics
Affiliation as printed
Biostatistics Unit, The Cyprus Institute of Neurology and Genetics, Nicosia, Cyprus
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QIMR Berghofer Medical Research Institute
Affiliation as printed
Population Health Program, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia
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University of Utah · Huntsman Cancer Institute
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Cancer Control and Population Science, Huntsman Cancer Institute, University of Utah, Salt Lake City, UT, USA
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Affiliation as printed
Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK
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University of Helsinki · Helsinki University Hospital
Affiliation as printed
Department of Clinical Genetics, Helsinki University Hospital, University of Helsinki, Helsinki, Finland
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Mount Sinai Hospital · University of Toronto · Lunenfeld-Tanenbaum Research Institute
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Department of Molecular Genetics, University of Toronto, Toronto, Ontario, Canada
Fred A. Litwin Center for Cancer Genetics, Lunenfeld-Tanenbaum Research Institute of Mount Sinai Hospital, Toronto, Ontario, Canada
Department of Molecular Genetics, University of Toronto, Toronto, Ontario, Canada; Fred A. Litwin Center for Cancer Genetics, Lunenfeld-Tanenbaum Research Institute of Mount Sinai Hospital, Toronto, Ontario, Canada
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University of California, Irvine
Affiliation as printed
Department of Medicine, Genetic Epidemiology Research Institute, University of California Irvine, Irvine, CA, USA
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Affiliation as printed
Department of Public Health Sciences, and Cancer Research Institute, Queen’s University, Kingston, ON, Canada
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Affiliation as printed
Oncology, Department of Clinical Sciences in Lund, Lund University, Lund, Sweden
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University Medical Center Hamburg-Eppendorf
Affiliation as printed
Institute for Medical Biometry and Epidemiology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
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University of Copenhagen · Herlev Hospital · Copenhagen University Hospital · Gentofte Hospital
Affiliation as printed
Copenhagen General Population Study, Herlev and Gentofte Hospital, Copenhagen University Hospital, Herlev, Denmark
Department of Clinical Biochemistry, Herlev and Gentofte Hospital, Copenhagen University Hospital, Herlev, Denmark
Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark
Copenhagen General Population Study, Herlev and Gentofte Hospital, Copenhagen University Hospital, Herlev, Denmark; Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark
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Affiliation as printed
Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK
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German Cancer Research Center · National Center for Tumor Diseases · Deutsches Konsortium für Translationale Krebsforschung
Affiliation as printed
Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany
Division of Preventive Oncology, German Cancer Research Center (DKFZ) and National Center for Tumor Diseases (NCT), Heidelberg, Germany
German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany
Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany; Division of Preventive Oncology, German Cancer Research Center (DKFZ) and National Center for Tumor Diseases (NCT), Heidelberg, Germany
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Affiliation as printed
School of Chemistry and Molecular Biosciences, University of Queensland, Brisbane, Queensland, Australia
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University of Utah · Huntsman Cancer Institute
Affiliation as printed
Department of Internal Medicine and Huntsman Cancer Institute, University of Utah, Salt Lake City, UT, USA
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Affiliation as printed
Genomic Epidemiology Group, German Cancer Research Center (DKFZ), Heidelberg, Germany
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Université Paris Sciences et Lettres · Institut Curie
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Paris Sciences Lettres Research University, Paris, France
Service de Génétique, Institut Curie, Paris, France
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Affiliation as printed
Oncology and Genetics Unit, Instituto de Investigación Sanitaria Galicia Sur (IISGS), Xerencia de Xestion Integrada de Vigo-SERGAS, Vigo, Spain
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German Cancer Research Center · University Medical Center Hamburg-Eppendorf · University Cancer Center Hamburg
Affiliation as printed
Cancer Epidemiology Group, University Cancer Center Hamburg (UCCH), University Medical Center Hamburg-Eppendorf, Hamburg, Germany
Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany
Cancer Epidemiology Group, University Cancer Center Hamburg (UCCH), University Medical Center Hamburg-Eppendorf, Hamburg, Germany; Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany
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University of Cologne · University Hospital Cologne
Affiliation as printed
Center for Familial Breast and Ovarian Cancer, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany
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Affiliation as printed
Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden
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Affiliation as printed
Department of Clinical Genetics, Fox Chase Cancer Center, Philadelphia, PA, USA
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Affiliation as printed
Center for Omics Sciences, IRCCS San Raffaele Scientific Institute, Milan, Italy
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Peter Devilee Aachen Department of Human Genetics Department of Pathology, Leiden University Medical Center
Leiden University Medical Center
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Department of Human Genetics, Leiden University Medical Center, Leiden, Netherlands
Department of Pathology, Leiden University Medical Center, Leiden, Netherlands
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Medizinische Hochschule Hannover
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Gynaecology Research Unit, Hannover Medical School, Hannover, Germany
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Affiliation as printed
Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, UK
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Affiliation as printed
School of Life Sciences, University of Westminster, London, UK
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Affiliation as printed
Faculty of Medicine, University of Southampton, Southampton, UK
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Affiliation as printed
Institute for Medical Informatics, Statistics and Epidemiology, University of Leipzig, Leipzig, Germany
LIFE-Leipzig Research Centre for Civilization Diseases, University of Leipzig, Leipzig, Germany
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Manchester Academic Health Science Centre · University of Manchester · St Mary's Hospital · Manchester University NHS Foundation Trust
Affiliation as printed
Division of Evolution and Genomic Sciences, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester Academic Health Science Centre, Manchester, UK
North West Genomics Laboratory Hub, Manchester Centre for Genomic Medicine, St Mary’s Hospital, Manchester University NHS Foundation Trust, Manchester Academic Health Science Centre, Manchester, UK
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Friedrich-Alexander-Universität Erlangen-Nürnberg · Universitätsklinikum Erlangen · Comprehensive Cancer Center Erlangen
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Department of Gynecology and Obstetrics, Comprehensive Cancer Center Erlangen-EMN, Friedrich-Alexander University Erlangen-Nuremberg, University Hospital Erlangen, Erlangen, Germany
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Complejo Hospitalario Universitario de Santiago · Fundación Pública Galega de Medicina Xenómica · Instituto de Investigación Sanitaria de Santiago · Servicio Gallego de Salud
Affiliation as printed
Genomic Medicine Group, International Cancer Genetics and Epidemiology Group, Fundación Pública Galega de Medicina Xenómica, Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), Complejo Hospitalario Universitario de Santiago, SERGAS, Santiago de Compostela, Spain
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National Institutes of Health · Division of Cancer Epidemiology and Genetics
Affiliation as printed
Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
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Hospital Clínico San Carlos · Instituto de Investigación Sanitaria del Hospital Clínico San Carlos · Centro de Investigación Biomédica en Red de Cáncer
Affiliation as printed
Medical Oncology Department, Hospital Clínico San Carlos, Instituto de Investigación Sanitaria San Carlos (IdISSC), Centro Investigación Biomédica en Red de Cáncer (CIBERONC), Madrid, Spain
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MRC Clinical Trials Unit at UCL · University College London
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MRC Clinical Trials Unit, Institute of Clinical Trials & Methodology, University College London, London, UK
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Affiliation as printed
Department of Clinical Genetics, Erasmus University Medical Center, Rotterdam, Netherlands
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The University of Melbourne · Cancer Council Victoria · Monash Health · Monash University
Affiliation as printed
Cancer Epidemiology Division, Cancer Council Victoria, Melbourne, Victoria, Australia
Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Melbourne, Victoria, Australia
Precision Medicine, School of Clinical Sciences at Monash Health, Monash University, Clayton, Victoria, Australia
Cancer Epidemiology Division, Cancer Council Victoria, Melbourne, Victoria, Australia; Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Melbourne, Victoria, Australia; Precision Medicine, School of Clinical Sciences at Monash Health, Monash University, Clayton, Victoria, Australia
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Mount Sinai Hospital · Lunenfeld-Tanenbaum Research Institute
Affiliation as printed
Fred A. Litwin Center for Cancer Genetics, Lunenfeld-Tanenbaum Research Institute of Mount Sinai Hospital, Toronto, Ontario, Canada
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Royal Victoria Hospital · McGill University
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Department of Medicine, McGill University, Montréal, QC, Canada
Division of Clinical Epidemiology, Royal Victoria Hospital, McGill University, Montréal, QC, Canada
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Maastricht University Medical Centre · Maastricht University
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Department of Clinical Genetics, Maastricht University Medical Center, Maastricht, Netherlands
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German Cancer Research Center · Heidelberg University · Helmholtz Munich · Institute of Diabetes Research
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Institute of Diabetes Research, Helmholtz Zentrum München, German Research Center for Environmental Health, Neuherberg, Germany
Molecular Biology of Breast Cancer, University Womens Clinic Heidelberg, University of Heidelberg, Heidelberg, Germany
Molecular Epidemiology Group, C080, German Cancer Research Center (DKFZ), Heidelberg, Germany
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Inserm · Université de Versailles Saint-Quentin-en-Yvelines · Université Paris-Saclay · Centre de recherche en Epidémiologie et Santé des Populations
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Team 'Exposome and Heredity', CESP, Gustave Roussy, INSERM, University Paris-Saclay, UVSQ, Villejuif, France
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University of Cologne · University Hospital Cologne
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Center for Familial Breast and Ovarian Cancer, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany
Center for Integrated Oncology (CIO), Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany
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University of Southern California
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Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
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Karolinska Institutet · Stockholm South General Hospital
Affiliation as printed
Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden
Department of Oncology, Södersjukhuset, Stockholm, Sweden
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Affiliation as printed
Molecular Genetics of Breast Cancer, German Cancer Research Center (DKFZ), Heidelberg, Germany
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Manchester Academic Health Science Centre · University of Manchester · Manchester University NHS Foundation Trust · Wythenshawe Hospital · NIHR Manchester Biomedical Research Centre
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Division of Informatics, Imaging and Data Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester Academic Health Science Centre, Manchester, UK
NIHR Manchester Biomedical Research Unit, Manchester University NHS Foundation Trust, Manchester Academic Health Science Centre, Manchester, UK
Nightingale & Genesis Prevention Centre, Wythenshawe Hospital, Manchester University NHS Foundation Trust, Manchester, UK
Division of Informatics, Imaging and Data Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester Academic Health Science Centre, Manchester, UK; Nightingale & Genesis Prevention Centre, Wythenshawe Hospital, Manchester University NHS Foundation Trust, Manchester, UK
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The Netherlands Cancer Institute
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Family Cancer Clinic, The Netherlands Cancer Institute-Antoni van Leeuwenhoek hospital, Amsterdam, Netherlands
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Affiliation as printed
Department of Medical Oncology, Erasmus MC Cancer Institute, Rotterdam, Netherlands
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Dr. Margarete Fischer-Bosch-Institute of Clinical Pharmacology · University of Tübingen
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Dr. Margarete Fischer-Bosch-Institute of Clinical Pharmacology, Stuttgart, Germany
University of Tübingen, Tübingen, Germany
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Affiliation as printed
Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Melbourne, Victoria, Australia
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Inserm · Centre Hospitalier Universitaire de Rouen
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Department of Genetics, F76000 and Normandy University, UNIROUEN, Inserm U1245, Normandy Centre for Genomic and Personalized Medicine, Rouen University Hospital, Rouen, France
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Affiliation as printed
Division of Genetics and Epidemiology, The Institute of Cancer Research, London, UK
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Affiliation as printed
Division of Cancer Sciences, University of Manchester, Manchester, UK
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The University of Sydney · Westmead Institute for Medical Research
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Australian Breast Cancer Tissue Bank, Westmead Institute for Medical Research, University of Sydney, Sydney, New South Wales, Australia
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Affiliation as printed
Research Centre for Genetic Engineering and Biotechnology 'Georgi D. Efremov', MASA, Skopje, North Macedonia
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Affiliation as printed
Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland
Independent Laboratory of Molecular Biology and Genetic Diagnostics, Pomeranian Medical University, Szczecin, Poland
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Affiliation as printed
Oncology, Department of Clinical Sciences in Lund, Lund University, Lund, Sweden
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Stanford Medicine · Stanford Cancer Institute · Stanford University
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Department of Epidemiology and Population Health, Stanford University School of Medicine, Stanford, CA, USA
Department of Medicine, Division of Oncology, Stanford Cancer Institute, Stanford University School of Medicine, Stanford, CA, USA
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Affiliation as printed
Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany
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National Cancer Institute · Division of Cancer Epidemiology and Genetics
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Radiation Epidemiology Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, USA
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National Institutes of Health · Division of Cancer Epidemiology and Genetics
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Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
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Affiliation as printed
Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA
Program in Genetic Epidemiology and Statistical Genetics, Harvard T.H. Chan School of Public Health, Boston, MA, USA
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Oslo University Hospital · University of Oslo
Affiliation as printed
Department of Medical Genetics, Oslo University Hospital and University of Oslo, Oslo, Norway
Institute of Clinical Medicine, Faculty of Medicine, University of Oslo, Oslo, Norway
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City Of Hope National Medical Center · City of Hope
Affiliation as printed
City of Hope Comprehensive Cancer Center, City of Hope, Duarte, CA, USA
Department of Computational and Quantitative Medicine, City of Hope, Duarte, CA, USA
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VIB-KU Leuven Center for Cancer Biology · KU Leuven
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Laboratory for Translational Genetics, Department of Human Genetics, KU Leuven, Leuven, Belgium
VIB Center for Cancer Biology, VIB, Leuven, Belgium
Laboratory for Translational Genetics, Department of Human Genetics, KU Leuven, Leuven, Belgium; VIB Center for Cancer Biology, VIB, Leuven, Belgium
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Hospices Civils de Lyon · Centre Léon Bérard
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Genetic and Cancer Medical Laboratory HCL-CLB, Hospices Civils de Lyon, Bron, France
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Karolinska University Hospital · Karolinska Institutet
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Department of Clinical Genetics, Karolinska University Hospital, Stockholm, Sweden
Department of Molecular Medicine and Surgery, Karolinska Institutet, Stockholm, Sweden
Department of Clinical Genetics, Karolinska University Hospital, Stockholm, Sweden; Department of Molecular Medicine and Surgery, Karolinska Institutet, Stockholm, Sweden
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Affiliation as printed
Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland
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Affiliation as printed
Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK
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Affiliation as printed
Molecular Genetics of Breast Cancer, German Cancer Research Center (DKFZ), Heidelberg, Germany
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Fondazione IRCCS Istituto Nazionale dei Tumori
Affiliation as printed
Unit of Medical Genetics, Department of Medical Oncology and Hematology, Fondazione IRCCS Istituto Nazionale dei Tumori di Milano, Milan, Italy
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Karolinska Institutet · Stockholm South General Hospital
Affiliation as printed
Department of Clinical Science and Education, Södersjukhuset, Karolinska Institutet, Stockholm, Sweden
Department of Oncology, Södersjukhuset, Stockholm, Sweden
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University of California San Diego · Moores Cancer Center
Affiliation as printed
Herbert Wertheim School of Public Health and Human Longevity Science, University of California San Diego, La Jolla, CA, USA
Moores Cancer Center, University of California San Diego, La Jolla, CA, USA
Herbert Wertheim School of Public Health and Human Longevity Science, University of California San Diego, La Jolla, CA, USA; Moores Cancer Center, University of California San Diego, La Jolla, CA, USA
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MRC Clinical Trials Unit at UCL · University College London
Affiliation as printed
MRC Clinical Trials Unit, Institute of Clinical Trials & Methodology, University College London, London, UK
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The University of Melbourne · Cancer Council Victoria · Monash Health · Monash University
Affiliation as printed
Cancer Epidemiology Division, Cancer Council Victoria, Melbourne, Victoria, Australia
Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Melbourne, Victoria, Australia
Precision Medicine, School of Clinical Sciences at Monash Health, Monash University, Clayton, Victoria, Australia
Cancer Epidemiology Division, Cancer Council Victoria, Melbourne, Victoria, Australia; Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Melbourne, Victoria, Australia; Precision Medicine, School of Clinical Sciences at Monash Health, Monash University, Clayton, Victoria, Australia
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Affiliation as printed
Department of Cancer Epidemiology, Moffitt Cancer Center, Tampa, FL, USA
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BC Cancer Agency · University of British Columbia
Affiliation as printed
Cancer Control Research, BC Cancer, Vancouver, BC, Canada
School of Population and Public Health, University of British Columbia, Vancouver, BC, Canada
Cancer Control Research, BC Cancer, Vancouver, BC, Canada; School of Population and Public Health, University of British Columbia, Vancouver, BC, Canada
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City of Hope · Beckman Research Institute
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Department of Population Sciences, Beckman Research Institute of City of Hope, Duarte, CA, USA
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University of Helsinki · Helsinki University Hospital
Affiliation as printed
Department of Obstetrics and Gynecology, Helsinki University Hospital, University of Helsinki, Helsinki, Finland
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Manchester Academic Health Science Centre · University of Manchester · St Mary's Hospital · Manchester University NHS Foundation Trust
Affiliation as printed
Division of Evolution and Genomic Sciences, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester Academic Health Science Centre, Manchester, UK
North West Genomics Laboratory Hub, Manchester Centre for Genomic Medicine, St Mary’s Hospital, Manchester University NHS Foundation Trust, Manchester Academic Health Science Centre, Manchester, UK
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Memorial Sloan Kettering Cancer Center
Affiliation as printed
Clinical Genetics Research Lab, Department of Cancer Biology and Genetics, Memorial Sloan Kettering Cancer Center, New York, NY, USA
Clinical Genetics Service, Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA
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Affiliation as printed
Cancer Research Institute, Seoul National University, Seoul, Republic of Korea
Department of Preventive Medicine, Seoul National University College of Medicine, Seoul, Republic of Korea
Integrated Major in Innovative Medical Science, Seoul National University College of Medicine, Seoul, Republic of Korea
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The Royal Melbourne Hospital · The University of Melbourne · Peter MacCallum Cancer Centre
Affiliation as printed
Parkville Familial Cancer Centre, Peter MacCallum Cancer Centre and Royal Melbourne Hospital, Melbourne, Victoria, Australia
Sir Peter MacCallum Department of Oncology, The University of Melbourne, Melbourne, Victoria, Australia
Parkville Familial Cancer Centre, Peter MacCallum Cancer Centre and Royal Melbourne Hospital, Melbourne, Victoria, Australia; Sir Peter MacCallum Department of Oncology, The University of Melbourne, Melbourne, Victoria, Australia
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Affiliation as printed
Genome Diagnostics Program, IFOM-ETS the AIRC Institute of Molecular Oncology, Milan, Italy
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London School of Hygiene & Tropical Medicine
Affiliation as printed
Department of Non-Communicable Disease Epidemiology, London School of Hygiene and Tropical Medicine, London, UK
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Affiliation as printed
Research Centre for Genetic Engineering and Biotechnology 'Georgi D. Efremov', MASA, Skopje, North Macedonia
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Universitair Ziekenhuis Leuven · KU Leuven
Affiliation as printed
Department of General Medical Oncology and Multidisciplinary Breast Centre, Leuven Cancer Institute and University Hospitals Leuven, Leuven, Belgium
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Fondazione IRCCS Istituto Nazionale dei Tumori
Affiliation as printed
Unit of Molecular Bases of Genetic Risk and Genetic Testing, Department of Research, Fondazione IRCCS Istituto Nazionale dei Tumori (INT), Milan, Italy
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German Cancer Research Center · Shaukat Khanum Memorial Cancer Hospital and Research Center
Affiliation as printed
Department of Basic Sciences, Shaukat Khanum Memorial Cancer Hospital and Research Centre (SKMCH & RC), Lahore, Pakistan
Molecular Genetics of Breast Cancer, German Cancer Research Center (DKFZ), Heidelberg, Germany
Department of Basic Sciences, Shaukat Khanum Memorial Cancer Hospital and Research Centre (SKMCH & RC), Lahore, Pakistan; Molecular Genetics of Breast Cancer, German Cancer Research Center (DKFZ), Heidelberg, Germany
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Technion – Israel Institute of Technology · Carmel Medical Center
Affiliation as printed
Clalit National Cancer Control Center, Carmel Medical Center and Technion Faculty of Medicine, Haifa, Israel
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Hospital Universitario Puerta de Hierro Majadahonda
Affiliation as printed
Medical Oncology Department, Hospital Universitario Puerta de Hierro, Madrid, Spain
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The Netherlands Cancer Institute
Affiliation as printed
Department of Pathology, The Netherlands Cancer Institute-Antoni van Leeuwenhoek hospital, Amsterdam, Netherlands
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University Hospital of Larissa
Affiliation as printed
Department of Oncology, University Hospital of Larissa, Larissa, Greece
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National Institute of Environmental Health Sciences
Affiliation as printed
Epidemiology Branch, National Institute of Environmental Health Sciences, NIH, Research Triangle Park, NC, USA
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Leiden University Medical Center · The Netherlands Cancer Institute
Affiliation as printed
Department of Clinical Genetics, Leiden University Medical Center, Leiden, Netherlands
Division of Molecular Pathology, The Netherlands Cancer Institute, Amsterdam, Netherlands
Division of Psychosocial Research and Epidemiology, The Netherlands Cancer Institute-Antoni van Leeuwenhoek hospital, Amsterdam, Netherlands
Department of Clinical Genetics, Leiden University Medical Center, Leiden, Netherlands; Division of Molecular Pathology, The Netherlands Cancer Institute, Amsterdam, Netherlands
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University of Cologne · University Hospital Cologne
Affiliation as printed
Center for Familial Breast and Ovarian Cancer, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany
Center for Integrated Oncology (CIO), Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany
Center for Molecular Medicine Cologne (CMMC), Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany
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Vanderbilt University · Vanderbilt-Ingram Cancer Center
Affiliation as printed
Division of Epidemiology, Department of Medicine, Vanderbilt Epidemiology Center, Vanderbilt-Ingram Cancer Center, Vanderbilt University School of Medicine, Nashville, TN, USA
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