Ovarian and Breast Cancer Risks Associated With Pathogenic Variants in RAD51C and RAD51D

doi:10.1093/jnci/djaa030

. 2020 Dec 14;112(12):1242-1250.

doi: 10.1093/jnci/djaa030.

Ovarian and Breast Cancer Risks Associated With Pathogenic Variants in RAD51C and RAD51D

Xin Yang¹, Honglin Song^{1

2}, Goska Leslie¹, Christoph Engel³, Eric Hahnen^{4

5}, Bernd Auber⁶, Judit Horváth⁷, Karin Kast^{8

9

10}, Dieter Niederacher¹¹, Clare Turnbull¹², Richard Houlston¹², Helen Hanson¹², Chey Loveday¹², Jill S Dolinsky¹³, Holly LaDuca¹³, Susan J Ramus^{14

15

16}, Usha Menon¹⁷, Adam N Rosenthal¹⁸, Ian Jacobs^{18

19

20}, Simon A Gayther²¹, Ed Dicks², Heli Nevanlinna²², Kristiina Aittomäki²³, Liisa M Pelttari²², Hans Ehrencrona^{24

25}, Åke Borg²⁶, Anders Kvist²⁶, Barbara Rivera^{27

28}, Thomas V O Hansen^{29

30}, Malene Djursby³⁰, Andrew Lee¹, Joe Dennis¹, David D Bowtell^{31

32}, Nadia Traficante^{31

32}, Orland Diez^{33

34}, Judith Balmaña^{35

36}, Stephen B Gruber³⁷, Georgia Chenevix-Trench³⁸, kConFab Investigators³⁹, Allan Jensen⁴⁰, Susanne K Kjær^{40

41}, Estrid Høgdall^{40

42}, Laurent Castéra⁴³, Judy Garber⁴⁴, Ramunas Janavicius^{45

46}, Ana Osorio^{47

48}, Lisa Golmard⁴⁹, Ana Vega^{47

50

51}, Fergus J Couch⁵², Mark Robson⁵³, Jacek Gronwald⁵⁴, Susan M Domchek⁵⁵, Julie O Culver⁵⁶, Miguel de la Hoya⁵⁷, Douglas F Easton^{1

2}, William D Foulkes^{5

8}, Marc Tischkowitz^{5

9}, Alfons Meindl⁵⁸, Rita K Schmutzler^{4

5

59}, Paul D P Pharoah^{1

2}, Antonis C Antoniou¹

Affiliations

¹ Department of Public Health and Primary Care, Centre for Cancer Genetic Epidemiology, University of Cambridge, Cambridge, UK.
² Department of Oncology, Centre for Cancer Genetic Epidemiology, University of Cambridge, Cambridge, UK.
³ Institute for Medical Informatics, Statistics and Epidemiology, University of Leipzig, Leipzig, Germany.
⁴ Faculty of Medicine and University Hospital Cologne, Center for Familial Breast and Ovarian Cancer, University of Cologne, Cologne, Germany.
⁵ Faculty of Medicine and University Hospital Cologne, Center for Integrated Oncology, University of Cologne, Cologne, Germany.
⁶ Institute of Human Genetics, Hannover Medical School, Hannover, Germany.
⁷ Institute of Human Genetics, University of Münster, Münster, Germany.
⁸ Department of Gynecology and Obstetrics, Medical Faculty and University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany.
⁹ National Center for Tumor Diseases (NCT), Dresden, Germany: German Cancer Research Center (DKFZ), Heidelberg, Germany; Faculty of Medicine and University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany; Helmholtz-Zentrum Dresden-Rossendorf (HZDR), Dresden, Germany.
¹⁰ German Cancer Consortium (DKTK), Dresden and German Cancer Research Center (DKFZ), Heidelberg, Germany.
¹¹ Department of Gynecology and Obstetrics, Heinrich-Heine University Düsseldorf, University Hospital Düsseldorf, Düsseldorf, Germany.
¹² Division of Genetics and Epidemiology, The Institute of Cancer Research, London, UK.
¹³ Ambry Genetics, Aliso Viejo, Canada.
¹⁴ School of Women's and Children's Health, Faculty of Medicine, University of NSW Sydney, Sydney, New South Wales, Australia.
¹⁵ Garvan Institute of Medical Research, The Kinghorn Cancer Centre, Sydney, New South Wales, Australia.
¹⁶ Adult Cancer Program, Lowy Cancer Research Centre, University of NSW Sydney, Sydney, New South Wales, Australia.
¹⁷ MRC Clinical Trials Unit at UCL, Institute of Clinical Trials and Methodology, University College London, London, UK.
¹⁸ Women's Cancer, Institute for Women's Health, University College London, London, UK.
¹⁹ University of New South Wales, Sydney, New South Wales, Australia.
²⁰ University of Manchester, Manchester, UK.
²¹ Center for Bioinformatics and Functional Genomics and the Cedars Sinai Genomics Core, Cedars-Sinai Medical Center, Los Angeles, CA, USA.
²² Department of Obstetrics and Gynecology, Helsinki University Hospital, University of Helsinki, Helsinki, Finland.
²³ Department of Clinical Genetics, Helsinki University Hospital, University of Helsinki, Helsinki, Finland.
²⁴ Department of Clinical Genetics and Pathology, Laboratory Medicine, Office for Medical Services, Region Skåne, Lund, Sweden.
²⁵ Division of Clinical Genetics, Department of Laboratory Medicine, Lund University, Lund, Sweden.
²⁶ Division of Oncology and Pathology, Department of Clinical Sciences Lund, Lund University, Lund, Sweden.
²⁷ Gerald Bronfman Dept Oncology, Jewish General Hospital, McGill University and Lady Davis Institute, Montréal, QC, Canada.
²⁸ Program in Molecular Mechanisms and Experimental Therapy in Oncology (Oncobell), IDIBELL, Hospitalet de Llobregat, Barcelona, Spain.
²⁹ Center for Genomic Medicine, Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark.
³⁰ Department of Clinical Genetics Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark.
³¹ Peter MacCallum Cancer Center, Melbourne, Victoria, Australia.
³² Sir Peter MacCallum, Department of Oncology, The University of Melbourne, Parkville, Victoria, Australia.
³³ Oncogenetics Group, Vall dHebron Institute of Oncology, Barcelona, Spain.
³⁴ Clinical and Molecular Genetics Area, University Hospital Vall dHebron, Barcelona, Spain.
³⁵ Hereditary Cancer Genetics Group, Vall d'Hebron Institute of Oncology, Barcelona, Spain.
³⁶ Department of Medical Oncology, University Hospital of Vall d'Hebron, Barcelona, Spain.
³⁷ Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
³⁸ Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.
³⁹ Kathleen Cuningham Foundation Consortium for research into Familial Breast cancer.
⁴⁰ Department of Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Copenhagen, Denmark.
⁴¹ Department of Gynaecology, University of Copenhagen, Rigshospitalet, Copenhagen, Denmark.
⁴² Department of Pathology, Molecular Unit, Herlev Hospital, University of Copenhagen, Copenhagen, Denmark.
⁴³ Department of Cancer Biology and Genetics, Normandy Centre for Genomic and Personalized Medicine, François Baclesse Center, Inserm U1245, Caen, France.
⁴⁴ Cancer Risk and Prevention Clinic, Dana-Farber Cancer Institute, Boston, MA, USA.
⁴⁵ Department of Molecular and Regenerative Medicine, Hematology, Oncology and Transfusion Medicine Center, Vilnius University Hospital Santariskiu Clinics, Vilnius, Lithuania.
⁴⁶ State Research Institute Centre for Innovative Medicine, Vilnius, Lithuania.
⁴⁷ Centro de Investigación en Red de Enfermedades Raras, Madrid, Spain.
⁴⁸ Human Cancer Genetics Programme, Spanish National Cancer Research Centre, Madrid, Spain.
⁴⁹ Institut Curie, Paris Sciences Lettres Research University, Service de Génétique, Paris, France.
⁵⁰ Fundación Pública Galega de Medicina Xenómica, Santiago de Compostela, Spain.
⁵¹ Instituto de Investigación Sanitaria de Santiago de Compostela, Complejo Hospitalario Universitario de Santiago, SERGAS, Santiago de Compostela, Spain.
⁵² Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN, USA.
⁵³ Department of Medicine, Memorial Sloan Kettering Cancer Center, Clinical Genetics Service, New York, NY, USA.
⁵⁴ Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland.
⁵⁵ Basser Center for BRCA, Abramson Cancer Center, University of Pennsylvania, Philadelphia, PA, USA.
⁵⁶ Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
⁵⁷ Molecular Oncology Laboratory CIBERONC, Hospital Clinico San Carlos, IdISSC (Instituto de Investigación Sanitaria del Hospital Clínico San Carlos), Madrid, Spain.
⁵⁸ Department of Gynecology and Obstetrics, University of Munich, Campus Großhadern, Munich, Germany.
⁵⁹ Faculty of Medicine and University Hospital Cologne, Center for Molecular Medicine Cologne, University of Cologne, Cologne, Germany.

PMID: 32107557
PMCID: PMC7735771
DOI: 10.1093/jnci/djaa030

Ovarian and Breast Cancer Risks Associated With Pathogenic Variants in RAD51C and RAD51D

Xin Yang et al. J Natl Cancer Inst. 2020.

. 2020 Dec 14;112(12):1242-1250.

doi: 10.1093/jnci/djaa030.

Authors

Affiliations

¹ Department of Public Health and Primary Care, Centre for Cancer Genetic Epidemiology, University of Cambridge, Cambridge, UK.
² Department of Oncology, Centre for Cancer Genetic Epidemiology, University of Cambridge, Cambridge, UK.
³ Institute for Medical Informatics, Statistics and Epidemiology, University of Leipzig, Leipzig, Germany.
⁴ Faculty of Medicine and University Hospital Cologne, Center for Familial Breast and Ovarian Cancer, University of Cologne, Cologne, Germany.
⁵ Faculty of Medicine and University Hospital Cologne, Center for Integrated Oncology, University of Cologne, Cologne, Germany.
⁶ Institute of Human Genetics, Hannover Medical School, Hannover, Germany.
⁷ Institute of Human Genetics, University of Münster, Münster, Germany.
⁸ Department of Gynecology and Obstetrics, Medical Faculty and University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany.
⁹ National Center for Tumor Diseases (NCT), Dresden, Germany: German Cancer Research Center (DKFZ), Heidelberg, Germany; Faculty of Medicine and University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany; Helmholtz-Zentrum Dresden-Rossendorf (HZDR), Dresden, Germany.
¹⁰ German Cancer Consortium (DKTK), Dresden and German Cancer Research Center (DKFZ), Heidelberg, Germany.
¹¹ Department of Gynecology and Obstetrics, Heinrich-Heine University Düsseldorf, University Hospital Düsseldorf, Düsseldorf, Germany.
¹² Division of Genetics and Epidemiology, The Institute of Cancer Research, London, UK.
¹³ Ambry Genetics, Aliso Viejo, Canada.
¹⁴ School of Women's and Children's Health, Faculty of Medicine, University of NSW Sydney, Sydney, New South Wales, Australia.
¹⁵ Garvan Institute of Medical Research, The Kinghorn Cancer Centre, Sydney, New South Wales, Australia.
¹⁶ Adult Cancer Program, Lowy Cancer Research Centre, University of NSW Sydney, Sydney, New South Wales, Australia.
¹⁷ MRC Clinical Trials Unit at UCL, Institute of Clinical Trials and Methodology, University College London, London, UK.
¹⁸ Women's Cancer, Institute for Women's Health, University College London, London, UK.
¹⁹ University of New South Wales, Sydney, New South Wales, Australia.
²⁰ University of Manchester, Manchester, UK.
²¹ Center for Bioinformatics and Functional Genomics and the Cedars Sinai Genomics Core, Cedars-Sinai Medical Center, Los Angeles, CA, USA.
²² Department of Obstetrics and Gynecology, Helsinki University Hospital, University of Helsinki, Helsinki, Finland.
²³ Department of Clinical Genetics, Helsinki University Hospital, University of Helsinki, Helsinki, Finland.
²⁴ Department of Clinical Genetics and Pathology, Laboratory Medicine, Office for Medical Services, Region Skåne, Lund, Sweden.
²⁵ Division of Clinical Genetics, Department of Laboratory Medicine, Lund University, Lund, Sweden.
²⁶ Division of Oncology and Pathology, Department of Clinical Sciences Lund, Lund University, Lund, Sweden.
²⁷ Gerald Bronfman Dept Oncology, Jewish General Hospital, McGill University and Lady Davis Institute, Montréal, QC, Canada.
²⁸ Program in Molecular Mechanisms and Experimental Therapy in Oncology (Oncobell), IDIBELL, Hospitalet de Llobregat, Barcelona, Spain.
²⁹ Center for Genomic Medicine, Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark.
³⁰ Department of Clinical Genetics Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark.
³¹ Peter MacCallum Cancer Center, Melbourne, Victoria, Australia.
³² Sir Peter MacCallum, Department of Oncology, The University of Melbourne, Parkville, Victoria, Australia.
³³ Oncogenetics Group, Vall dHebron Institute of Oncology, Barcelona, Spain.
³⁴ Clinical and Molecular Genetics Area, University Hospital Vall dHebron, Barcelona, Spain.
³⁵ Hereditary Cancer Genetics Group, Vall d'Hebron Institute of Oncology, Barcelona, Spain.
³⁶ Department of Medical Oncology, University Hospital of Vall d'Hebron, Barcelona, Spain.
³⁷ Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
³⁸ Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.
³⁹ Kathleen Cuningham Foundation Consortium for research into Familial Breast cancer.
⁴⁰ Department of Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Copenhagen, Denmark.
⁴¹ Department of Gynaecology, University of Copenhagen, Rigshospitalet, Copenhagen, Denmark.
⁴² Department of Pathology, Molecular Unit, Herlev Hospital, University of Copenhagen, Copenhagen, Denmark.
⁴³ Department of Cancer Biology and Genetics, Normandy Centre for Genomic and Personalized Medicine, François Baclesse Center, Inserm U1245, Caen, France.
⁴⁴ Cancer Risk and Prevention Clinic, Dana-Farber Cancer Institute, Boston, MA, USA.
⁴⁵ Department of Molecular and Regenerative Medicine, Hematology, Oncology and Transfusion Medicine Center, Vilnius University Hospital Santariskiu Clinics, Vilnius, Lithuania.
⁴⁶ State Research Institute Centre for Innovative Medicine, Vilnius, Lithuania.
⁴⁷ Centro de Investigación en Red de Enfermedades Raras, Madrid, Spain.
⁴⁸ Human Cancer Genetics Programme, Spanish National Cancer Research Centre, Madrid, Spain.
⁴⁹ Institut Curie, Paris Sciences Lettres Research University, Service de Génétique, Paris, France.
⁵⁰ Fundación Pública Galega de Medicina Xenómica, Santiago de Compostela, Spain.
⁵¹ Instituto de Investigación Sanitaria de Santiago de Compostela, Complejo Hospitalario Universitario de Santiago, SERGAS, Santiago de Compostela, Spain.
⁵² Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN, USA.
⁵³ Department of Medicine, Memorial Sloan Kettering Cancer Center, Clinical Genetics Service, New York, NY, USA.
⁵⁴ Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland.
⁵⁵ Basser Center for BRCA, Abramson Cancer Center, University of Pennsylvania, Philadelphia, PA, USA.
⁵⁶ Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
⁵⁷ Molecular Oncology Laboratory CIBERONC, Hospital Clinico San Carlos, IdISSC (Instituto de Investigación Sanitaria del Hospital Clínico San Carlos), Madrid, Spain.
⁵⁸ Department of Gynecology and Obstetrics, University of Munich, Campus Großhadern, Munich, Germany.
⁵⁹ Faculty of Medicine and University Hospital Cologne, Center for Molecular Medicine Cologne, University of Cologne, Cologne, Germany.

PMID: 32107557
PMCID: PMC7735771
DOI: 10.1093/jnci/djaa030

Abstract

Background: The purpose of this study was to estimate precise age-specific tubo-ovarian carcinoma (TOC) and breast cancer (BC) risks for carriers of pathogenic variants in RAD51C and RAD51D.

Methods: We analyzed data from 6178 families, 125 with pathogenic variants in RAD51C, and 6690 families, 60 with pathogenic variants in RAD51D. TOC and BC relative and cumulative risks were estimated using complex segregation analysis to model the cancer inheritance patterns in families while adjusting for the mode of ascertainment of each family. All statistical tests were two-sided.

Results: Pathogenic variants in both RAD51C and RAD51D were associated with TOC (RAD51C: relative risk [RR] = 7.55, 95% confidence interval [CI] = 5.60 to 10.19; P = 5 × 10-40; RAD51D: RR = 7.60, 95% CI = 5.61 to 10.30; P = 5 × 10-39) and BC (RAD51C: RR = 1.99, 95% CI = 1.39 to 2.85; P = 1.55 × 10-4; RAD51D: RR = 1.83, 95% CI = 1.24 to 2.72; P = .002). For both RAD51C and RAD51D, there was a suggestion that the TOC relative risks increased with age until around age 60 years and decreased thereafter. The estimated cumulative risks of developing TOC to age 80 years were 11% (95% CI = 6% to 21%) for RAD51C and 13% (95% CI = 7% to 23%) for RAD51D pathogenic variant carriers. The estimated cumulative risks of developing BC to 80 years were 21% (95% CI = 15% to 29%) for RAD51C and 20% (95% CI = 14% to 28%) for RAD51D pathogenic variant carriers. Both TOC and BC risks for RAD51C and RAD51D pathogenic variant carriers varied by cancer family history and could be as high as 32-36% for TOC, for carriers with two first-degree relatives diagnosed with TOC, or 44-46% for BC, for carriers with two first-degree relatives diagnosed with BC.

Conclusions: These estimates will facilitate the genetic counseling of RAD51C and RAD51D pathogenic variant carriers and justify the incorporation of RAD51C and RAD51D into cancer risk prediction models.

PubMed Disclaimer

Figures

**Figure 1.**
Estimated age-specific tubo-ovarian carcinoma and breast cancer cumulative risks in *RAD51C* and *RAD51D* pathogenic variant carriers. The shaded areas correspond to the 95% confidence intervals.

**Figure 2.**
Estimated TOC and BC cumulative risks for *RAD51C* and *RAD51D* pathogenic variant carriers by cancer family history. BC = breast cancer; TOC = tubo-ovarian carcinoma.

See this image and copyright information in PMC

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References

1. Meindl A, Hellebrand H, Wiek C, et al. Germline mutations in breast and ovarian cancer pedigrees establish RAD51C as a human cancer susceptibility gene. Nat Genet. 2010;42(5):410–414. - PubMed
1. Loveday C, Turnbull C, Ramsay E. et al. Germline mutations in RAD51D confer susceptibility to ovarian cancer. Nat Genet. 2011;43(9):879–882. 10.1038/ng.893 - DOI - PMC - PubMed
1. Loveday C, Turnbull C, Ruark E. et al. Germline RAD51C mutations confer susceptibility to ovarian cancer. Nat Genet. 2012;44(5):475–476; author reply 476. 10.1038/ng.2224 22538716 - DOI - PubMed
1. Couch FJ, Hart SN, Sharma P, et al. Inherited mutations in 17 breast cancer susceptibility genes among a large triple-negative breast cancer cohort unselected for family history of breast cancer. J Clin Oncol. 2015;33(4):304–311. - PMC - PubMed
1. Li N, McInerny S, Zethoven M, et al. Combined tumor sequencing and case/control analyses of RAD51C in breast cancer. J Natl Cancer Inst. 2019;111(12):1332–1338. - PMC - PubMed

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[1] Meindl A, Hellebrand H, Wiek C, et al. Germline mutations in breast and ovarian cancer pedigrees establish RAD51C as a human cancer susceptibility gene. Nat Genet. 2010;42(5):410–414. - PubMed

[2] Meindl A, Hellebrand H, Wiek C, et al. Germline mutations in breast and ovarian cancer pedigrees establish RAD51C as a human cancer susceptibility gene. Nat Genet. 2010;42(5):410–414. - PubMed

[3] Loveday C, Turnbull C, Ramsay E. et al. Germline mutations in RAD51D confer susceptibility to ovarian cancer. Nat Genet. 2011;43(9):879–882. 10.1038/ng.893 - DOI - PMC - PubMed

[4] Loveday C, Turnbull C, Ramsay E. et al. Germline mutations in RAD51D confer susceptibility to ovarian cancer. Nat Genet. 2011;43(9):879–882. 10.1038/ng.893 - DOI - PMC - PubMed

[5] Loveday C, Turnbull C, Ruark E. et al. Germline RAD51C mutations confer susceptibility to ovarian cancer. Nat Genet. 2012;44(5):475–476; author reply 476. 10.1038/ng.2224 22538716 - DOI - PubMed

[6] Loveday C, Turnbull C, Ruark E. et al. Germline RAD51C mutations confer susceptibility to ovarian cancer. Nat Genet. 2012;44(5):475–476; author reply 476. 10.1038/ng.2224 22538716 - DOI - PubMed

[7] Couch FJ, Hart SN, Sharma P, et al. Inherited mutations in 17 breast cancer susceptibility genes among a large triple-negative breast cancer cohort unselected for family history of breast cancer. J Clin Oncol. 2015;33(4):304–311. - PMC - PubMed

[8] Couch FJ, Hart SN, Sharma P, et al. Inherited mutations in 17 breast cancer susceptibility genes among a large triple-negative breast cancer cohort unselected for family history of breast cancer. J Clin Oncol. 2015;33(4):304–311. - PMC - PubMed

[9] Li N, McInerny S, Zethoven M, et al. Combined tumor sequencing and case/control analyses of RAD51C in breast cancer. J Natl Cancer Inst. 2019;111(12):1332–1338. - PMC - PubMed

[10] Li N, McInerny S, Zethoven M, et al. Combined tumor sequencing and case/control analyses of RAD51C in breast cancer. J Natl Cancer Inst. 2019;111(12):1332–1338. - PMC - PubMed

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Ovarian and Breast Cancer Risks Associated With Pathogenic Variants in RAD51C and RAD51D

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Ovarian and Breast Cancer Risks Associated With Pathogenic Variants in RAD51C and RAD51D

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