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,Breast Cancer Research

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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
Breast Cancer Research ( IF 7.4 ) Pub Date : 2021-08-18 , DOI: 10.1186/s13058-021-01450-7
Anna Morra ₁ , Maria Escala-Garcia ₁ , Jonathan Beesley ₂ , Renske Keeman ₁ , Sander Canisius _{1,

3} , Thomas U Ahearn ₄ , Irene L Andrulis _{5,

6} , Hoda Anton-Culver ₇ , Volker Arndt ₈ , Paul L Auer _{9,

10} , Annelie Augustinsson ₁₁ , Laura E Beane Freeman ₄ , Heiko Becher ₁₂ , Matthias W Beckmann ₁₃ , Sabine Behrens ₁₄ , Stig E Bojesen _{15,

16,

17} , Manjeet K Bolla ₁₈ , Hermann Brenner _{8,

19,

20} , Thomas Brüning ₂₁ , Saundra S Buys ₂₂ , Bette Caan ₂₃ , Daniele Campa _{14,

24} , Federico Canzian ₂₅ , Jose E Castelao ₂₆ , Jenny Chang-Claude _{14,

27} , Stephen J Chanock ₄ , Ting-Yuan David Cheng ₂₈ , Christine L Clarke ₂₉ , , Sarah V Colonna ₂₂ , Fergus J Couch ₃₀ , Angela Cox ₃₁ , Simon S Cross ₃₂ , Kamila Czene ₃₃ , Mary B Daly ₃₄ , Joe Dennis ₁₈ , Thilo Dörk ₃₅ , Laure Dossus ₃₆ , Alison M Dunning ₃₇ , Miriam Dwek ₃₈ , Diana M Eccles ₃₉ , Arif B Ekici ₄₀ , A Heather Eliassen _{41,

42} , Mikael Eriksson ₃₃ , D Gareth Evans _{43,

44} , Peter A Fasching _{13,

45} , Henrik Flyger ₄₆ , Lin Fritschi ₄₇ , Manuela Gago-Dominguez _{48,

49} , José A García-Sáenz ₅₀ , Graham G Giles _{51,

52,

53} , Mervi Grip ₅₄ , Pascal Guénel ₅₅ , Melanie Gündert _{56,

57,

58} , Eric Hahnen _{59,

60} , Christopher A Haiman ₆₁ , Niclas Håkansson ₆₂ , Per Hall _{33,

63} , Ute Hamann ₆₄ , Steven N Hart ₆₅ , Jaana M Hartikainen _{66,

67} , Arndt Hartmann ₆₈ , Wei He ₃₃ , Maartje J Hooning ₆₉ , Reiner Hoppe _{70,

71} , John L Hopper ₅₂ , Anthony Howell ₇₂ , David J Hunter _{42,

73} , , , Agnes Jager ₆₉ , Anna Jakubowska _{74,

75} , Wolfgang Janni ₇₆ , Esther M John _{77,

78} , Audrey Y Jung ₁₄ , Rudolf Kaaks ₁₄ , Machteld Keupers ₇₉ , Cari M Kitahara ₈₀ , Stella Koutros ₄ , Peter Kraft _{42,

81} , Vessela N Kristensen _{82,

83} , Allison W Kurian _{77,

78} , James V Lacey _{84,

85} , Diether Lambrechts _{86,

87} , Loic Le Marchand ₈₈ , Annika Lindblom _{89,

90} , Martha Linet ₈₀ , Robert N Luben ₉₁ , Jan Lubiński ₇₄ , Michael Lush ₁₈ , Arto Mannermaa _{66,

67,

92} , Mehdi Manoochehri ₆₄ , Sara Margolin _{63,

93} , John W M Martens ₆₉ , Maria Elena Martinez _{49,

94} , Dimitrios Mavroudis ₉₅ , Kyriaki Michailidou _{18,

96,

97} , Roger L Milne _{51,

52,

53} , Anna Marie Mulligan _{98,

99} , Taru A Muranen ₁₀₀ , Heli Nevanlinna ₁₀₀ , William G Newman _{43,

44} , Sune F Nielsen _{15,

16} , Børge G Nordestgaard _{15,

16,

17} , Andrew F Olshan ₁₀₁ , Håkan Olsson ₁₁ , Nick Orr ₁₀₂ , Tjoung-Won Park-Simon ₃₅ , Alpa V Patel ₁₀₃ , Bernard Peissel ₁₀₄ , Paolo Peterlongo ₁₀₅ , Dijana Plaseska-Karanfilska ₁₀₆ , Karolina Prajzendanc ₇₄ , Ross Prentice ₉ , Nadege Presneau ₃₈ , Brigitte Rack ₇₆ , Gad Rennert ₁₀₇ , Hedy S Rennert ₁₀₇ , Valerie Rhenius ₃₇ , Atocha Romero ₁₀₈ , Rebecca Roylance ₁₀₉ , Matthias Ruebner ₁₃ , Emmanouil Saloustros ₁₁₀ , Elinor J Sawyer ₁₁₁ , Rita K Schmutzler _{59,

60,

112} , Andreas Schneeweiss _{57,

113} , Christopher Scott ₆₅ , Mitul Shah ₃₇ , Snezhana Smichkoska ₁₁₄ , Melissa C Southey _{51,

53,

115} , Jennifer Stone _{52,

116} , Harald Surowy _{56,

57} , Anthony J Swerdlow _{117,

118} , Rulla M Tamimi _{42,

119} , William J Tapper ₃₉ , Lauren R Teras ₁₀₃ , Mary Beth Terry ₁₂₀ , Rob A E M Tollenaar ₁₂₁ , Ian Tomlinson _{122,

123} , Melissa A Troester ₁₀₁ , Thérèse Truong ₅₅ , Celine M Vachon ₁₂₄ , Qin Wang ₁₈ , Amber N Hurson ₄ , Robert Winqvist _{125,

126} , Alicja Wolk _{62,

127} , Argyrios Ziogas ₇ , Hiltrud Brauch _{70,

128,

129} , Montserrat García-Closas ₄ , Paul D P Pharoah _{18,

37} , Douglas F Easton _{18,

37} , Georgia Chenevix-Trench ₂ , Marjanka K Schmidt _{1,

130}

Affiliation

Division of Molecular Pathology, The Netherlands Cancer Institute - Antoni van Leeuwenhoek Hospital, Amsterdam, 1066 CX, The Netherlands.
Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.
Division of Molecular Carcinogenesis, The Netherlands Cancer Institute - Antoni van Leeuwenhoek Hospital, Amsterdam, The Netherlands.
Department of Health and Human Services, Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.
Lunenfeld-Tanenbaum Research Institute of Mount Sinai Hospital, Fred A. Litwin Center for Cancer Genetics, Toronto, ON, Canada.
Department of Molecular Genetics, University of Toronto, Toronto, ON, Canada.
Department of Medicine, Genetic Epidemiology Research Institute, University of California Irvine, Irvine, CA, USA.
Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany.
Cancer Prevention Program, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
Zilber School of Public Health, University of Wisconsin-Milwaukee, Milwaukee, WI, USA.
Department of Cancer Epidemiology, Clinical Sciences, Lund University, Lund, Sweden.
Institute of Medical Biometry and Epidemiology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
Department of Gynecology and Obstetrics, Comprehensive Cancer Center Erlangen-EMN, University Hospital Erlangen, Friedrich-Alexander University Erlangen-Nuremberg (FAU), Erlangen, Germany.
Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany.
Copenhagen University Hospital, Copenhagen General Population Study, Herlev and Gentofte 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.
Department of Public Health and Primary Care, University of Cambridge, Centre for Cancer Genetic Epidemiology, Cambridge, UK.
Division of Preventive Oncology, German Cancer Research Center (DKFZ) and National Center for Tumor Diseases (NCT), Heidelberg, Germany.
German Cancer Research Center (DKFZ), German Cancer Consortium (DKTK), Heidelberg, Germany.
Institute of the Ruhr University Bochum (IPA), Institute for Prevention and Occupational Medicine of the German Social Accident Insurance, Bochum, Germany.
Department of Medicine, Huntsman Cancer Institute, Salt Lake City, UT, USA.
Division of Research, Kaiser Permanente, Oakland, CA, USA.
Department of Biology, University of Pisa, Pisa, Italy.
German Cancer Research Center (DKFZ), Genomic Epidemiology Group, Heidelberg, Germany.
Instituto de Investigacion Sanitaria Galicia Sur (IISGS), Xerencia de Xestion Integrada de Vigo-SERGAS, Oncology and Genetics Unit, Vigo, Spain.
Cancer Epidemiology Group, University Cancer Center Hamburg (UCCH), University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
Division of Cancer Prevention and Control, Roswell Park Cancer Institute, Buffalo, NY, USA.
Westmead Institute for Medical Research, University of Sydney, Sydney, New South Wales, Australia.
Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN, USA.
Department of Oncology and Metabolism, University of Sheffield, Sheffield Institute for Nucleic Acids (SInFoNiA), Sheffield, UK.
Academic Unit of Pathology, Department of Neuroscience, University of Sheffield, Sheffield, UK.
Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.
Department of Clinical Genetics, Fox Chase Cancer Center, Philadelphia, PA, USA.
Gynaecology Research Unit, Hannover Medical School, Hannover, Germany.
Nutrition and Metabolism Section, International Agency for Research on Cancer (IARC-WHO), Lyon, France.
Department of Oncology, University of Cambridge, Centre for Cancer Genetic Epidemiology, Cambridge, UK.
School of Life Sciences, University of Westminster, London, UK.
Faculty of Medicine, University of Southampton, Southampton, UK.
Institute of Human Genetics, Comprehensive Cancer Center Erlangen-EMN, University Hospital Erlangen, Friedrich-Alexander University Erlangen-Nuremberg (FAU), Erlangen, Germany.
Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Channing Division of Network Medicine, Boston, MA, USA.
Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA.
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.
St Mary's Hospital, Manchester University NHS Foundation Trust, Manchester Academic Health Science Centre, North West Genomics Laboratory Hub, Manchester Centre for Genomic Medicine, Manchester, UK.
Department of Medicine Division of Hematology and Oncology, University of California at Los Angeles, David Geffen School of Medicine, Los Angeles, CA, USA.
Department of Breast Surgery, Herlev and Gentofte Hospital, Copenhagen University Hospital, Herlev, Denmark.
School of Public Health, Curtin University, Perth, Western Australia, Australia.
Galician Public Foundation of Genomic Medicine (FPGMX), Genomic Medicine Group, International Cancer Genetics and Epidemiology Group, Health Research Institute of Santiago (IDIS), Santiago de Compostela, Spain.
University of California San Diego, Moores Cancer Center, La Jolla, CA, USA.
Instituto de Investigación Sanitaria San Carlos (IdISSC), Centro Investigación Biomédica en Red de Cáncer (CIBERONC), Medical Oncology Department, Hospital Clínico San Carlos, Madrid, Spain.
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.
Department of Surgery, Oulu University Hospital, University of Oulu, Oulu, Finland.
Team Exposome and Heredity, INSERM, University Paris-Saclay, Center for Research in Epidemiology and Population Health (CESP), Villejuif, France.
Molecular Epidemiology Group, C080, German Cancer Research Center (DKFZ), Heidelberg, Germany.
Molecular Biology of Breast Cancer, University Womens Clinic Heidelberg, University of Heidelberg, Heidelberg, Germany.
German Research Center for Environmental Health, Institute of Diabetes Research, Helmholtz Zentrum München, Neuherberg, Germany.
Faculty of Medicine and University Hospital Cologne, Center for Familial Breast and Ovarian Cancer, University of Cologne, Cologne, Germany.
Faculty of Medicine and University Hospital Cologne, Center for Integrated Oncology (CIO), University of Cologne, Cologne, Germany.
Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden.
Department of Oncology, Södersjukhuset, Stockholm, Sweden.
Molecular Genetics of Breast Cancer, German Cancer Research Center (DKFZ), Heidelberg, Germany.
Department of Health Sciences Research, Mayo Clinic, Rochester, MN, USA.
Translational Cancer Research Area, University of Eastern Finland, Kuopio, Finland.
Institute of Clinical Medicine, Pathology and Forensic Medicine, University of Eastern Finland, Kuopio, Finland.
Institute of Pathology, Comprehensive Cancer Center Erlangen Nuremberg, University Hospital Erlangen, Friedrich-Alexander-University Erlangen-Nuremberg, Erlangen, Germany.
Department of Medical Oncology, Erasmus MC Cancer Institute, Rotterdam, The Netherlands.
Dr. Margarete Fischer-Bosch-Institute of Clinical Pharmacology, Stuttgart, Germany.
University of Tübingen, Tübingen, Germany.
Division of Cancer Sciences, University of Manchester, Manchester, UK.
Nuffield Department of Population Health, University of Oxford, Oxford, UK.
Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland.
Independent Laboratory of Molecular Biology and Genetic Diagnostics, Pomeranian Medical University, Szczecin, Poland.
Department of Gynaecology and Obstetrics, University Hospital Ulm, Ulm, Germany.
Department of Epidemiology & 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.
Department of Radiation Oncology, University Hospitals Leuven, , University of Leuven, Leuven, Belgium.
Division of Cancer Epidemiology and Genetics, Radiation Epidemiology Branch, National Cancer Institute, Bethesda, MD, USA.
Program in Genetic Epidemiology and Statistical Genetics, Harvard T.H. Chan School of Public Health, Boston, MA, USA.
Faculty of Medicine, Institute of Clinical Medicine, University of Oslo, Oslo, Norway.
Department of Medical Genetics, Oslo University Hospital and University of Oslo, Oslo, Norway.
Department of Computational and Quantitative Medicine, City of Hope, Duarte, CA, USA.
City of Hope Comprehensive Cancer Center, City of Hope, Duarte, CA, USA.
VIB Center for Cancer Biology, Leuven, Belgium.
Laboratory for Translational Genetics, Department of Human Genetics, University of Leuven, Leuven, Belgium.
Epidemiology Program, University of Hawaii Cancer Center, Honolulu, HI, USA.
Department of Molecular Medicine and Surgery, Karolinska Institutet, Stockholm, Sweden.
Department of Clinical Genetics, Karolinska University Hospital, Stockholm, Sweden.
Clinical Gerontology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK.
Kuopio University Hospital, Biobank of Eastern Finland, Kuopio, Finland.
Department of Clinical Science and Education, Karolinska Institutet, Södersjukhuset, Stockholm, Sweden.
Department of Family Medicine and Public Health, University of California San Diego, La Jolla, CA, USA.
Department of Medical Oncology, University Hospital of Heraklion, Heraklion, Greece.
Biostatistics Unit, The Cyprus Institute of Neurology & Genetics, Nicosia, Cyprus.
The Cyprus Institute of Neurology & Genetics, Cyprus School of Molecular Medicine, Nicosia, Cyprus.
Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, ON, Canada.
University Health Network, Laboratory Medicine Program, Toronto, ON, Canada.
Department of Obstetrics and Gynecology, Helsinki University Hospital, University of Helsinki, Helsinki, Finland.
Department of Epidemiology, Gillings School of Global Public Health and UNC Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA.
Centre for Cancer Research and Cell Biology, Queen's University Belfast, Belfast, Northern Ireland, UK.
Department of Population Science, American Cancer Society, Atlanta, GA, USA.
Unit of Medical Genetics, Department of Medical Oncology and Hematology, Fondazione IRCCS Istituto Nazionale dei Tumori di Milano, Milan, Italy.
Genome Diagnostics Program, IFOM - the FIRC Institute of Molecular Oncology, Milan, Italy.
MASA, Research Centre for Genetic Engineering and Biotechnology 'Georgi D. Efremov', Skopje, Republic of North Macedonia.
Carmel Medical Center and Technion Faculty of Medicine, Clalit National Cancer Control Center, Haifa, Israel.
Medical Oncology Department, Hospital Universitario Puerta de Hierro, Madrid, Spain.
Department of Oncology, UCLH Foundation Trust, London, UK.
Department of Oncology, University Hospital of Larissa, Larissa, Greece.
School of Cancer & Pharmaceutical Sciences, Comprehensive Cancer Centre, Guy's Campus, King's College London, London, UK.
Faculty of Medicine and University Hospital Cologne, University of Cologne, Center for Molecular Medicine Cologne (CMMC), Cologne, Germany.
University Hospital and German Cancer Research Center, National Center for Tumor Diseases, Heidelberg, Germany.
Medical Faculty, University Clinic of Radiotherapy and Oncology, Ss. Cyril and Methodius University in Skopje, Skopje, Republic of North Macedonia.
Department of Clinical Pathology, The University of Melbourne, Melbourne, Victoria, Australia.
Genetic Epidemiology Group, School of Population and Global Health, University of Western Australia, Perth, Western Australia, Australia.
Division of Genetics and Epidemiology, The Institute of Cancer Research, London, UK.
Division of Breast Cancer Research, The Institute of Cancer Research, London, UK.
Department of Population Health Sciences, Weill Cornell Medicine, New York, NY, USA.
Department of Epidemiology, Mailman School of Public Health, Columbia University, New York, NY, USA.
Department of Surgery, Leiden University Medical Center, Leiden, The Netherlands.
Institute of Cancer and Genomic Sciences, University of Birmingham, Birmingham, UK.
University of Oxford, Wellcome Trust Centre for Human Genetics and Oxford NIHR Biomedical Research Centre, Oxford, UK.
Department of Health Science Research, Division of Epidemiology, Mayo Clinic, Rochester, MN, USA.
Laboratory of Cancer Genetics and Tumor Biology, Cancer and Translational Medicine Research Unit, Biocenter Oulu, University of Oulu, Oulu, Finland.
Laboratory of Cancer Genetics and Tumor Biology, Northern Finland Laboratory Centre Oulu, Oulu, Finland.
Department of Surgical Sciences, Uppsala University, Uppsala, Sweden.
iFIT-Cluster of Excellence, University of Tübingen, Tübingen, Germany.
German Cancer Research Center (DKFZ) and German Cancer Consortium (DKTK) Partner Site Tübingen, Tübingen, Germany.
Division of Psychosocial Research and Epidemiology, The Netherlands Cancer Institute - Antoni van Leeuwenhoek Hospital, Amsterdam, The Netherlands.

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. 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). 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. 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.

中文翻译：

在由与肿瘤生物学和全身治疗类型相关的临床病理变量定义的患者亚组中，种系遗传变异与乳腺癌特异性生存的关联

鉴于乳腺肿瘤之间的高度异质性，在未分层的乳腺癌患者组中，可能无法检测到特定亚组中可能存在的常见种系遗传变异与生存之间的关联。我们根据激素受体、肿瘤分级、年龄和全身治疗类型等预后因素，对 15 个乳腺癌患者亚组进行了全基因组关联分析。分析基于乳腺癌协会联盟的 91,686 名欧洲血统女性患者，其中包括 7531 名乳腺癌特异性死亡患者，中位随访时间为 8.1 年。Cox 回归用于评估常见种系变异与 15 年和 5 年乳腺癌特异性生存率的关联。我们通过贝叶斯错误发现概率 (BFDP < 0.15) 评估了这些关联为真阳性的概率。在三个患者亚组中观察到与乳腺癌特异性生存相关的证据，其中 3 级肿瘤患者中存在 rs5934618 变异（15 年风险比 (HR) [95% 置信区间 (CI)] 1.32 [1.20, 1.45] ，P = 1.4E−08，BFDP = 0.01，每个 G 等位基因）；接受内分泌治疗的 ER 阳性肿瘤患者中的变异 rs4679741（15 年 HR [95% CI] 1.18 [1.11, 1.26]，P = 1.6E−07，BFDP = 0.09，每个 G 等位基因）；变体 rs1106333（15 年 HR [95% CI] 1.68 [1.39,2.03]，P = 5.6E−08，BFDP = 0.12，每个 A 等位基因）和 rs78754389（5 年 HR [95% CI] 1.79 [ 1.46,2.20]，P = 1.7E−08，BFDP = 0.07，每个 A 等位基因），在接受化疗的 ER 阴性肿瘤患者中。我们在三个患者亚组中发现了四个与乳腺癌特异性生存相关的基因座的证据。其他患者亚组中存在关联的证据有限。然而，由于事件数量较少，许多小组的权力受到限制。即便如此，我们的结果表明，常见种系遗传变异对乳腺癌特异性生存的影响可能有限。

更新日期：2021-08-19

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