Breast Cancer Research (Aug 2021)
Association of germline genetic variants with breast cancer-specific survival in patient subgroups defined by clinic-pathological variables related to tumor biology and type of systemic treatment
- Anna Morra,
- Maria Escala-Garcia,
- Jonathan Beesley,
- Renske Keeman,
- Sander Canisius,
- Thomas U. Ahearn,
- Irene L. Andrulis,
- Hoda Anton-Culver,
- Volker Arndt,
- Paul L. Auer,
- Annelie Augustinsson,
- Laura E. Beane Freeman,
- Heiko Becher,
- Matthias W. Beckmann,
- Sabine Behrens,
- Stig E. Bojesen,
- Manjeet K. Bolla,
- Hermann Brenner,
- Thomas Brüning,
- Saundra S. Buys,
- Bette Caan,
- Daniele Campa,
- Federico Canzian,
- Jose E. Castelao,
- Jenny Chang-Claude,
- Stephen J. Chanock,
- Ting-Yuan David Cheng,
- Christine L. Clarke,
- NBCS Collaborators,
- Sarah V. Colonna,
- Fergus J. Couch,
- Angela Cox,
- Simon S. Cross,
- Kamila Czene,
- Mary B. Daly,
- Joe Dennis,
- Thilo Dörk,
- Laure Dossus,
- Alison M. Dunning,
- Miriam Dwek,
- Diana M. Eccles,
- Arif B. Ekici,
- A. Heather Eliassen,
- Mikael Eriksson,
- D. Gareth Evans,
- Peter A. Fasching,
- Henrik Flyger,
- Lin Fritschi,
- Manuela Gago-Dominguez,
- José A. García-Sáenz,
- Graham G. Giles,
- Mervi Grip,
- Pascal Guénel,
- Melanie Gündert,
- Eric Hahnen,
- Christopher A. Haiman,
- Niclas Håkansson,
- Per Hall,
- Ute Hamann,
- Steven N. Hart,
- Jaana M. Hartikainen,
- Arndt Hartmann,
- Wei He,
- Maartje J. Hooning,
- Reiner Hoppe,
- John L. Hopper,
- Anthony Howell,
- David J. Hunter,
- ABCTB Investigators,
- kConFab Investigators,
- Agnes Jager,
- Anna Jakubowska,
- Wolfgang Janni,
- Esther M. John,
- Audrey Y. Jung,
- Rudolf Kaaks,
- Machteld Keupers,
- Cari M. Kitahara,
- Stella Koutros,
- Peter Kraft,
- Vessela N. Kristensen,
- Allison W. Kurian,
- James V. Lacey,
- Diether Lambrechts,
- Loic Le Marchand,
- Annika Lindblom,
- Martha Linet,
- Robert N. Luben,
- Jan Lubiński,
- Michael Lush,
- Arto Mannermaa,
- Mehdi Manoochehri,
- Sara Margolin,
- John W. M. Martens,
- Maria Elena Martinez,
- Dimitrios Mavroudis,
- Kyriaki Michailidou,
- Roger L. Milne,
- Anna Marie Mulligan,
- Taru A. Muranen,
- Heli Nevanlinna,
- William G. Newman,
- Sune F. Nielsen,
- Børge G. Nordestgaard,
- Andrew F. Olshan,
- Håkan Olsson,
- Nick Orr,
- Tjoung-Won Park-Simon,
- Alpa V. Patel,
- Bernard Peissel,
- Paolo Peterlongo,
- Dijana Plaseska-Karanfilska,
- Karolina Prajzendanc,
- Ross Prentice,
- Nadege Presneau,
- Brigitte Rack,
- Gad Rennert,
- Hedy S. Rennert,
- Valerie Rhenius,
- Atocha Romero,
- Rebecca Roylance,
- Matthias Ruebner,
- Emmanouil Saloustros,
- Elinor J. Sawyer,
- Rita K. Schmutzler,
- Andreas Schneeweiss,
- Christopher Scott,
- Mitul Shah,
- Snezhana Smichkoska,
- Melissa C. Southey,
- Jennifer Stone,
- Harald Surowy,
- Anthony J. Swerdlow,
- Rulla M. Tamimi,
- William J. Tapper,
- Lauren R. Teras,
- Mary Beth Terry,
- Rob A. E. M. Tollenaar,
- Ian Tomlinson,
- Melissa A. Troester,
- Thérèse Truong,
- Celine M. Vachon,
- Qin Wang,
- Amber N. Hurson,
- Robert Winqvist,
- Alicja Wolk,
- Argyrios Ziogas,
- Hiltrud Brauch,
- Montserrat García-Closas,
- Paul D. P. Pharoah,
- Douglas F. Easton,
- Georgia Chenevix-Trench,
- Marjanka K. Schmidt
Affiliations
- Anna Morra
- Division of Molecular Pathology, The Netherlands Cancer Institute - Antoni van Leeuwenhoek Hospital
- Maria Escala-Garcia
- Division of Molecular Pathology, The Netherlands Cancer Institute - Antoni van Leeuwenhoek Hospital
- Jonathan Beesley
- Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute
- Renske Keeman
- Division of Molecular Pathology, The Netherlands Cancer Institute - Antoni van Leeuwenhoek Hospital
- Sander Canisius
- Division of Molecular Pathology, The Netherlands Cancer Institute - Antoni van Leeuwenhoek Hospital
- Thomas U. Ahearn
- Department of Health and Human Services, Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health
- Irene L. Andrulis
- Lunenfeld-Tanenbaum Research Institute of Mount Sinai Hospital, Fred A. Litwin Center for Cancer Genetics
- Hoda Anton-Culver
- Department of Medicine, Genetic Epidemiology Research Institute, University of California Irvine
- Volker Arndt
- Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ)
- Paul L. Auer
- Cancer Prevention Program, Fred Hutchinson Cancer Research Center
- Annelie Augustinsson
- Department of Cancer Epidemiology, Clinical Sciences, Lund University
- Laura E. Beane Freeman
- Department of Health and Human Services, Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health
- Heiko Becher
- Institute of Medical Biometry and Epidemiology, University Medical Center Hamburg-Eppendorf
- Matthias W. Beckmann
- Department of Gynecology and Obstetrics, Comprehensive Cancer Center Erlangen-EMN, University Hospital Erlangen, Friedrich-Alexander University Erlangen-Nuremberg (FAU)
- Sabine Behrens
- Division of Cancer Epidemiology, German Cancer Research Center (DKFZ)
- Stig E. Bojesen
- Copenhagen University Hospital, Copenhagen General Population Study, Herlev and Gentofte Hospital
- Manjeet K. Bolla
- Department of Public Health and Primary Care, University of Cambridge, Centre for Cancer Genetic Epidemiology
- Hermann Brenner
- Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ)
- Thomas Brüning
- Institute of the Ruhr University Bochum (IPA), Institute for Prevention and Occupational Medicine of the German Social Accident Insurance
- Saundra S. Buys
- Department of Medicine, Huntsman Cancer Institute
- Bette Caan
- Division of Research, Kaiser Permanente
- Daniele Campa
- Division of Cancer Epidemiology, German Cancer Research Center (DKFZ)
- Federico Canzian
- German Cancer Research Center (DKFZ), Genomic Epidemiology Group
- Jose E. Castelao
- Instituto de Investigacion Sanitaria Galicia Sur (IISGS), Xerencia de Xestion Integrada de Vigo-SERGAS, Oncology and Genetics Unit
- Jenny Chang-Claude
- Division of Cancer Epidemiology, German Cancer Research Center (DKFZ)
- Stephen J. Chanock
- Department of Health and Human Services, Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health
- Ting-Yuan David Cheng
- Division of Cancer Prevention and Control, Roswell Park Cancer Institute
- Christine L. Clarke
- Westmead Institute for Medical Research, University of Sydney
- NBCS Collaborators
- Department of Cancer Genetics, Institute for Cancer Research, Oslo University Hospital-Radiumhospitalet
- Sarah V. Colonna
- Department of Medicine, Huntsman Cancer Institute
- Fergus J. Couch
- Department of Laboratory Medicine and Pathology, Mayo Clinic
- Angela Cox
- Department of Oncology and Metabolism, University of Sheffield, Sheffield Institute for Nucleic Acids (SInFoNiA)
- Simon S. Cross
- Academic Unit of Pathology, Department of Neuroscience, University of Sheffield
- Kamila Czene
- Department of Medical Epidemiology and Biostatistics, Karolinska Institutet
- Mary B. Daly
- Department of Clinical Genetics, Fox Chase Cancer Center
- Joe Dennis
- Department of Public Health and Primary Care, University of Cambridge, Centre for Cancer Genetic Epidemiology
- Thilo Dörk
- Gynaecology Research Unit, Hannover Medical School
- Laure Dossus
- Nutrition and Metabolism Section, International Agency for Research on Cancer (IARC-WHO)
- Alison M. Dunning
- Department of Oncology, University of Cambridge, Centre for Cancer Genetic Epidemiology
- Miriam Dwek
- School of Life Sciences, University of Westminster
- Diana M. Eccles
- Faculty of Medicine, University of Southampton
- Arif B. Ekici
- Institute of Human Genetics, Comprehensive Cancer Center Erlangen-EMN, University Hospital Erlangen, Friedrich-Alexander University Erlangen-Nuremberg (FAU)
- A. Heather Eliassen
- Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, Channing Division of Network Medicine
- Mikael Eriksson
- Department of Medical Epidemiology and Biostatistics, Karolinska Institutet
- D. Gareth Evans
- Division of Evolution and Genomic Sciences, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester Academic Health Science Centre
- Peter A. Fasching
- Department of Gynecology and Obstetrics, Comprehensive Cancer Center Erlangen-EMN, University Hospital Erlangen, Friedrich-Alexander University Erlangen-Nuremberg (FAU)
- Henrik Flyger
- Department of Breast Surgery, Herlev and Gentofte Hospital, Copenhagen University Hospital
- Lin Fritschi
- School of Public Health, Curtin University
- Manuela Gago-Dominguez
- Galician Public Foundation of Genomic Medicine (FPGMX), Genomic Medicine Group, International Cancer Genetics and Epidemiology Group, Health Research Institute of Santiago (IDIS)
- José A. García-Sáenz
- Instituto de Investigación Sanitaria San Carlos (IdISSC), Centro Investigación Biomédica en Red de Cáncer (CIBERONC), Medical Oncology Department, Hospital Clínico San Carlos
- Graham G. Giles
- Cancer Epidemiology Division, Cancer Council Victoria
- Mervi Grip
- Department of Surgery, Oulu University Hospital, University of Oulu
- Pascal Guénel
- Team Exposome and Heredity, INSERM, University Paris-Saclay, Center for Research in Epidemiology and Population Health (CESP)
- Melanie Gündert
- Molecular Epidemiology Group, C080, German Cancer Research Center (DKFZ)
- Eric Hahnen
- Faculty of Medicine and University Hospital Cologne, Center for Familial Breast and Ovarian Cancer, University of Cologne
- Christopher A. Haiman
- Department of Preventive Medicine, Keck School of Medicine, University of Southern California
- Niclas Håkansson
- Institute of Environmental Medicine, Karolinska Institutet
- Per Hall
- Department of Medical Epidemiology and Biostatistics, Karolinska Institutet
- Ute Hamann
- Molecular Genetics of Breast Cancer, German Cancer Research Center (DKFZ)
- Steven N. Hart
- Department of Health Sciences Research, Mayo Clinic
- Jaana M. Hartikainen
- Translational Cancer Research Area, University of Eastern Finland
- Arndt Hartmann
- Institute of Pathology, Comprehensive Cancer Center Erlangen Nuremberg, University Hospital Erlangen, Friedrich-Alexander-University Erlangen-Nuremberg
- Wei He
- Department of Medical Epidemiology and Biostatistics, Karolinska Institutet
- Maartje J. Hooning
- Department of Medical Oncology, Erasmus MC Cancer Institute
- Reiner Hoppe
- Dr. Margarete Fischer-Bosch-Institute of Clinical Pharmacology
- John L. Hopper
- Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne
- Anthony Howell
- Division of Cancer Sciences, University of Manchester
- David J. Hunter
- Department of Epidemiology, Harvard T.H. Chan School of Public Health
- ABCTB Investigators
- Westmead Institute for Medical Research, Australian Breast Cancer Tissue Bank, University of Sydney
- kConFab Investigators
- Research Department, Peter MacCallum Cancer Center
- Agnes Jager
- Department of Medical Oncology, Erasmus MC Cancer Institute
- Anna Jakubowska
- Department of Genetics and Pathology, Pomeranian Medical University
- Wolfgang Janni
- Department of Gynaecology and Obstetrics, University Hospital Ulm
- Esther M. John
- Department of Epidemiology & Population Health, Stanford University School of Medicine
- Audrey Y. Jung
- Division of Cancer Epidemiology, German Cancer Research Center (DKFZ)
- Rudolf Kaaks
- Division of Cancer Epidemiology, German Cancer Research Center (DKFZ)
- Machteld Keupers
- Department of Radiation Oncology, University Hospitals Leuven, , University of Leuven
- Cari M. Kitahara
- Division of Cancer Epidemiology and Genetics, Radiation Epidemiology Branch, National Cancer Institute
- Stella Koutros
- Department of Health and Human Services, Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health
- Peter Kraft
- Department of Epidemiology, Harvard T.H. Chan School of Public Health
- Vessela N. Kristensen
- Faculty of Medicine, Institute of Clinical Medicine, University of Oslo
- Allison W. Kurian
- Department of Epidemiology & Population Health, Stanford University School of Medicine
- James V. Lacey
- Department of Computational and Quantitative Medicine, City of Hope
- Diether Lambrechts
- VIB Center for Cancer Biology
- Loic Le Marchand
- Epidemiology Program, University of Hawaii Cancer Center
- Annika Lindblom
- Department of Molecular Medicine and Surgery, Karolinska Institutet
- Martha Linet
- Division of Cancer Epidemiology and Genetics, Radiation Epidemiology Branch, National Cancer Institute
- Robert N. Luben
- Clinical Gerontology, Department of Public Health and Primary Care, University of Cambridge
- Jan Lubiński
- Department of Genetics and Pathology, Pomeranian Medical University
- Michael Lush
- Department of Public Health and Primary Care, University of Cambridge, Centre for Cancer Genetic Epidemiology
- Arto Mannermaa
- Translational Cancer Research Area, University of Eastern Finland
- Mehdi Manoochehri
- Molecular Genetics of Breast Cancer, German Cancer Research Center (DKFZ)
- Sara Margolin
- Department of Oncology, Södersjukhuset
- John W. M. Martens
- Department of Medical Oncology, Erasmus MC Cancer Institute
- Maria Elena Martinez
- University of California San Diego, Moores Cancer Center
- Dimitrios Mavroudis
- Department of Medical Oncology, University Hospital of Heraklion
- Kyriaki Michailidou
- Department of Public Health and Primary Care, University of Cambridge, Centre for Cancer Genetic Epidemiology
- Roger L. Milne
- Cancer Epidemiology Division, Cancer Council Victoria
- Anna Marie Mulligan
- Department of Laboratory Medicine and Pathobiology, University of Toronto
- Taru A. Muranen
- Department of Obstetrics and Gynecology, Helsinki University Hospital, University of Helsinki
- Heli Nevanlinna
- Department of Obstetrics and Gynecology, Helsinki University Hospital, University of Helsinki
- William G. Newman
- Division of Evolution and Genomic Sciences, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester Academic Health Science Centre
- Sune F. Nielsen
- Copenhagen University Hospital, Copenhagen General Population Study, Herlev and Gentofte Hospital
- Børge G. Nordestgaard
- Copenhagen University Hospital, Copenhagen General Population Study, Herlev and Gentofte Hospital
- Andrew F. Olshan
- Department of Epidemiology, Gillings School of Global Public Health and UNC Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill
- Håkan Olsson
- Department of Cancer Epidemiology, Clinical Sciences, Lund University
- Nick Orr
- Centre for Cancer Research and Cell Biology, Queen’s University Belfast
- Tjoung-Won Park-Simon
- Gynaecology Research Unit, Hannover Medical School
- Alpa V. Patel
- Department of Population Science, American Cancer Society
- Bernard Peissel
- Unit of Medical Genetics, Department of Medical Oncology and Hematology, Fondazione IRCCS Istituto Nazionale dei Tumori di Milano
- Paolo Peterlongo
- Genome Diagnostics Program, IFOM - the FIRC Institute of Molecular Oncology
- Dijana Plaseska-Karanfilska
- MASA, Research Centre for Genetic Engineering and Biotechnology ‘Georgi D. Efremov’
- Karolina Prajzendanc
- Department of Genetics and Pathology, Pomeranian Medical University
- Ross Prentice
- Cancer Prevention Program, Fred Hutchinson Cancer Research Center
- Nadege Presneau
- School of Life Sciences, University of Westminster
- Brigitte Rack
- Department of Gynaecology and Obstetrics, University Hospital Ulm
- Gad Rennert
- Carmel Medical Center and Technion Faculty of Medicine, Clalit National Cancer Control Center
- Hedy S. Rennert
- Carmel Medical Center and Technion Faculty of Medicine, Clalit National Cancer Control Center
- Valerie Rhenius
- Department of Oncology, University of Cambridge, Centre for Cancer Genetic Epidemiology
- Atocha Romero
- Medical Oncology Department, Hospital Universitario Puerta de Hierro
- Rebecca Roylance
- Department of Oncology, UCLH Foundation Trust
- Matthias Ruebner
- Department of Gynecology and Obstetrics, Comprehensive Cancer Center Erlangen-EMN, University Hospital Erlangen, Friedrich-Alexander University Erlangen-Nuremberg (FAU)
- Emmanouil Saloustros
- Department of Oncology, University Hospital of Larissa
- Elinor J. Sawyer
- School of Cancer & Pharmaceutical Sciences, Comprehensive Cancer Centre, Guy’s Campus, King’s College London
- Rita K. Schmutzler
- Faculty of Medicine and University Hospital Cologne, Center for Familial Breast and Ovarian Cancer, University of Cologne
- Andreas Schneeweiss
- Molecular Biology of Breast Cancer, University Womens Clinic Heidelberg, University of Heidelberg
- Christopher Scott
- Department of Health Sciences Research, Mayo Clinic
- Mitul Shah
- Department of Oncology, University of Cambridge, Centre for Cancer Genetic Epidemiology
- Snezhana Smichkoska
- Medical Faculty, University Clinic of Radiotherapy and Oncology, Ss. Cyril and Methodius University in Skopje
- Melissa C. Southey
- Cancer Epidemiology Division, Cancer Council Victoria
- Jennifer Stone
- Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne
- Harald Surowy
- Molecular Epidemiology Group, C080, German Cancer Research Center (DKFZ)
- Anthony J. Swerdlow
- Division of Genetics and Epidemiology, The Institute of Cancer Research
- Rulla M. Tamimi
- Department of Epidemiology, Harvard T.H. Chan School of Public Health
- William J. Tapper
- Faculty of Medicine, University of Southampton
- Lauren R. Teras
- Department of Population Science, American Cancer Society
- Mary Beth Terry
- Department of Epidemiology, Mailman School of Public Health, Columbia University
- Rob A. E. M. Tollenaar
- Department of Surgery, Leiden University Medical Center
- Ian Tomlinson
- Institute of Cancer and Genomic Sciences, University of Birmingham
- Melissa A. Troester
- Department of Epidemiology, Gillings School of Global Public Health and UNC Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill
- Thérèse Truong
- Team Exposome and Heredity, INSERM, University Paris-Saclay, Center for Research in Epidemiology and Population Health (CESP)
- Celine M. Vachon
- Department of Health Science Research, Division of Epidemiology, Mayo Clinic
- Qin Wang
- Department of Public Health and Primary Care, University of Cambridge, Centre for Cancer Genetic Epidemiology
- Amber N. Hurson
- Department of Health and Human Services, Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health
- Robert Winqvist
- Laboratory of Cancer Genetics and Tumor Biology, Cancer and Translational Medicine Research Unit, Biocenter Oulu, University of Oulu
- Alicja Wolk
- Institute of Environmental Medicine, Karolinska Institutet
- Argyrios Ziogas
- Department of Medicine, Genetic Epidemiology Research Institute, University of California Irvine
- Hiltrud Brauch
- Dr. Margarete Fischer-Bosch-Institute of Clinical Pharmacology
- Montserrat García-Closas
- Department of Health and Human Services, Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health
- Paul D. P. Pharoah
- Department of Public Health and Primary Care, University of Cambridge, Centre for Cancer Genetic Epidemiology
- Douglas F. Easton
- Department of Public Health and Primary Care, University of Cambridge, Centre for Cancer Genetic Epidemiology
- Georgia Chenevix-Trench
- Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute
- Marjanka K. Schmidt
- Division of Molecular Pathology, The Netherlands Cancer Institute - Antoni van Leeuwenhoek Hospital
- DOI
- https://doi.org/10.1186/s13058-021-01450-7
- Journal volume & issue
-
Vol. 23,
no. 1
pp. 1 – 18
Abstract
Abstract Background Given the high heterogeneity among breast tumors, associations between common germline genetic variants and survival that may exist within specific subgroups could go undetected in an unstratified set of breast cancer patients. Methods We performed genome-wide association analyses within 15 subgroups of breast cancer patients based on prognostic factors, including hormone receptors, tumor grade, age, and type of systemic treatment. Analyses were based on 91,686 female patients of European ancestry from the Breast Cancer Association Consortium, including 7531 breast cancer-specific deaths over a median follow-up of 8.1 years. Cox regression was used to assess associations of common germline variants with 15-year and 5-year breast cancer-specific survival. We assessed the probability of these associations being true positives via the Bayesian false discovery probability (BFDP < 0.15). Results Evidence of associations with breast cancer-specific survival was observed in three patient subgroups, with variant rs5934618 in patients with grade 3 tumors (15-year-hazard ratio (HR) [95% confidence interval (CI)] 1.32 [1.20, 1.45], P = 1.4E−08, BFDP = 0.01, per G allele); variant rs4679741 in patients with ER-positive tumors treated with endocrine therapy (15-year-HR [95% CI] 1.18 [1.11, 1.26], P = 1.6E−07, BFDP = 0.09, per G allele); variants rs1106333 (15-year-HR [95% CI] 1.68 [1.39,2.03], P = 5.6E−08, BFDP = 0.12, per A allele) and rs78754389 (5-year-HR [95% CI] 1.79 [1.46,2.20], P = 1.7E−08, BFDP = 0.07, per A allele), in patients with ER-negative tumors treated with chemotherapy. Conclusions We found evidence of four loci associated with breast cancer-specific survival within three patient subgroups. There was limited evidence for the existence of associations in other patient subgroups. However, the power for many subgroups is limited due to the low number of events. Even so, our results suggest that the impact of common germline genetic variants on breast cancer-specific survival might be limited.
Keywords
- Common germline genetic variants
- Breast cancer-specific survival
- Patient subgroups
- Tumor biology
- Systemic treatment