BRCA1 Promoter Methylation and Clinical Outcomes in Ovarian Cancer: An Individual Patient Data Meta-Analysis.


Journal

Journal of the National Cancer Institute
ISSN: 1460-2105
Titre abrégé: J Natl Cancer Inst
Pays: United States
ID NLM: 7503089

Informations de publication

Date de publication:
14 12 2020
Historique:
received: 02 02 2020
revised: 23 04 2020
accepted: 11 05 2020
pubmed: 16 5 2020
medline: 29 4 2021
entrez: 16 5 2020
Statut: ppublish

Résumé

BRCA1 methylation has been associated with homologous recombination deficiency, a biomarker of platinum sensitivity. Studies evaluating BRCA1-methylated tubal and ovarian cancer (OC) do not consistently support improved survival following platinum chemotherapy. We examine the characteristics of BRCA1-methylated OC in a meta-analysis of individual participant data. Data of 2636 participants across 15 studies were analyzed. BRCA1-methylated tumors were defined according to their original study. Associations between BRCA1 methylation and clinicopathological characteristics were evaluated. The effects of methylation on overall survival (OS) and progression-free survival (PFS) were examined using mixed-effects models. All statistical tests were 2-sided. 430 (16.3%) tumors were BRCA1-methylated. BRCA1 methylation was associated with younger age and advanced-stage, high-grade serous OC. There were no survival differences between BRCA1-methylated and non-BRCA1-methylated OC (median PFS = 20.0 vs 18.5 months, hazard ratio [HR] = 1.01, 95% CI = 0.87 to 1.16; P = .98; median OS = 46.6 vs 48.0 months, HR = 1.02, 95% CI = 0.87 to 1.18; P = .96). Where BRCA1/2 mutations were evaluated (n = 1248), BRCA1 methylation displayed no survival advantage over BRCA1/2-intact (BRCA1/2 wild-type non-BRCA1-methylated) OC. Studies used different methods to define BRCA1 methylation. Where BRCA1 methylation was determined using methylation-specific polymerase chain reaction and gel electrophoresis (n = 834), it was associated with improved survival (PFS: HR = 0.80, 95% CI = 0.66 to 0.97; P = .02; OS: HR = 0.80, 95% CI = 0.63 to 1.00; P = .05) on mixed-effects modeling. BRCA1-methylated OC displays similar clinicopathological features to BRCA1-mutated OC but is not associated with survival. Heterogeneity within BRCA1 methylation assays influences associations. Refining these assays may better identify cases with silenced BRCA1 function and improved patient outcomes.

Sections du résumé

BACKGROUND
BRCA1 methylation has been associated with homologous recombination deficiency, a biomarker of platinum sensitivity. Studies evaluating BRCA1-methylated tubal and ovarian cancer (OC) do not consistently support improved survival following platinum chemotherapy. We examine the characteristics of BRCA1-methylated OC in a meta-analysis of individual participant data.
METHODS
Data of 2636 participants across 15 studies were analyzed. BRCA1-methylated tumors were defined according to their original study. Associations between BRCA1 methylation and clinicopathological characteristics were evaluated. The effects of methylation on overall survival (OS) and progression-free survival (PFS) were examined using mixed-effects models. All statistical tests were 2-sided.
RESULTS
430 (16.3%) tumors were BRCA1-methylated. BRCA1 methylation was associated with younger age and advanced-stage, high-grade serous OC. There were no survival differences between BRCA1-methylated and non-BRCA1-methylated OC (median PFS = 20.0 vs 18.5 months, hazard ratio [HR] = 1.01, 95% CI = 0.87 to 1.16; P = .98; median OS = 46.6 vs 48.0 months, HR = 1.02, 95% CI = 0.87 to 1.18; P = .96). Where BRCA1/2 mutations were evaluated (n = 1248), BRCA1 methylation displayed no survival advantage over BRCA1/2-intact (BRCA1/2 wild-type non-BRCA1-methylated) OC. Studies used different methods to define BRCA1 methylation. Where BRCA1 methylation was determined using methylation-specific polymerase chain reaction and gel electrophoresis (n = 834), it was associated with improved survival (PFS: HR = 0.80, 95% CI = 0.66 to 0.97; P = .02; OS: HR = 0.80, 95% CI = 0.63 to 1.00; P = .05) on mixed-effects modeling.
CONCLUSION
BRCA1-methylated OC displays similar clinicopathological features to BRCA1-mutated OC but is not associated with survival. Heterogeneity within BRCA1 methylation assays influences associations. Refining these assays may better identify cases with silenced BRCA1 function and improved patient outcomes.

Identifiants

pubmed: 32413141
pii: 5837681
doi: 10.1093/jnci/djaa070
pmc: PMC7735770
doi:

Substances chimiques

BRCA1 Protein 0
BRCA1 protein, human 0
Biomarkers, Tumor 0

Types de publication

Journal Article Meta-Analysis Research Support, Non-U.S. Gov't Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

1190-1203

Subventions

Organisme : NCI NIH HHS
ID : P50 CA217685
Pays : United States

Informations de copyright

© The Author(s) 2020. Published by Oxford University Press. All rights reserved. For permissions, please email: journals.permissions@oup.com.

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Auteurs

Roshni D Kalachand (RD)

Medical Oncology Group, Department of Molecular Medicine, Royal College of Surgeons in Ireland, Beaumont Hospital, Dublin, Ireland.

Britta Stordal (B)

Department of Natural Sciences, Middlesex University, Hendon, London NW4 4BT, UK.

Stephen Madden (S)

Data Science Centre, Royal College of Surgeons in Ireland, Beaux Lane House, Dublin, Ireland.

Benjamin Chandler (B)

Department of Radiation Oncology, University of Michigan, Ann Arbor, MI, USA.

Julie Cunningham (J)

Division of Experimental Pathology, Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN, USA.

Ellen L Goode (EL)

Division of Epidemiology, Department of Health Sciences Research, Mayo Clinic, Rochester, MN, USA.

Ilary Ruscito (I)

Department of Gynecology, European Competence Center for Ovarian Cancer, Campus Virchow Klinikum, Charité-Universitätsmedizin Berlin, Corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Berlin Institute of Health, Berlin, Germany.
Cell Therapy Unit and Laboratory of Tumor Immunology, Department of Experimental Medicine, Sapienza University of Rome, Rome, Italy.

Elena I Braicu (EI)

Department of Gynecology, European Competence Center for Ovarian Cancer, Campus Virchow Klinikum, Charité-Universitätsmedizin Berlin, Corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Berlin Institute of Health, Berlin, Germany.

Jalid Sehouli (J)

Department of Gynecology, European Competence Center for Ovarian Cancer, Campus Virchow Klinikum, Charité-Universitätsmedizin Berlin, Corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Berlin Institute of Health, Berlin, Germany.

Atanas Ignatov (A)

Department of Gynecology and Obstetrics, University Medical Center, Regensburg, Germany.

Herbert Yu (H)

University of Hawaii Cancer Centre, Honolulu, HI, USA.

Dionyssios Katsaros (D)

AOU Citta della Salute and Department of Surgical Sciences, Gynecologic Oncology, University of Torino, Italy.

Gordon B Mills (GB)

Department of Cell, Development and Cancer Biology Knight Cancer Institute, Oregon Health and Sciences University, Portland, OR, USA.

Karen H Lu (KH)

University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Mark S Carey (MS)

Division of Gynecologic Oncology, Department of Obstetrics and Gynaecology, University of British Columbia, Vancouver, British Columbia, Canada.

Kirsten M Timms (KM)

Myriad Genetics, Inc, Salt Lake City, UT, USA.

Jolanta Kupryjanczyk (J)

Department of Pathology and Laboratory Diagnostics, Maria Sklodowska-Curie Institute-Oncology Center, Warsaw, Poland.

Iwona K Rzepecka (IK)

Department of Pathology and Laboratory Diagnostics, Maria Sklodowska-Curie Institute-Oncology Center, Warsaw, Poland.

Agnieszka Podgorska (A)

Department of Pathology and Laboratory Diagnostics, Maria Sklodowska-Curie Institute-Oncology Center, Warsaw, Poland.

Jessica N McAlpine (JN)

Division of Gynecologic Oncology, Department of Obstetrics and Gynaecology, University of British Columbia, Vancouver, British Columbia, Canada.

Elizabeth M Swisher (EM)

University of Washington School of Medicine, Seattle, WA, USA.

Sarah S Bernards (SS)

University of Washington School of Medicine, Seattle, WA, USA.

Ciaran O'Riain (C)

Department of Histopathology, Trinity College Dublin, Central Pathology Laboratory, St. James's Hospital, Dublin, Ireland.

Sharon O'Toole (S)

Department of Obstetrics and Gynaecology/Histopathology, Trinity College Dublin, Trinity Centre for Health Sciences, St. James's Hospital, Dublin, Ireland.
Emer Casey Research Laboratory, Molecular Pathology Laboratory, The Coombe Women and Infants University Hospital, Dublin, Ireland.

John J O'Leary (JJ)

Department of Histopathology, Trinity College Dublin, Central Pathology Laboratory, St. James's Hospital, Dublin, Ireland.
Emer Casey Research Laboratory, Molecular Pathology Laboratory, The Coombe Women and Infants University Hospital, Dublin, Ireland.

David D Bowtell (DD)

Peter MacCallum Cancer Centre, Melbourne, Australia.

David M Thomas (DM)

Genomic Cancer Medicine, Cancer Division, Garvan Institute of Medical Research, The Kinghorn Cancer Centre, Darlinghurst, Australia.

Katharina Prieske (K)

Department of Gynecology and Gynecologic Oncology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Simon A Joosse (SA)

Department of Tumor Biology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Linn Woelber (L)

Department of Gynecology and Gynecologic Oncology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Parvesh Chaudhry (P)

Department of Radiotherapy, Postgraduate Institute of Medical Education and Research, Chandigarh, India.

Norman Häfner (N)

Department for Gynaecology and Reproductive Medicine, Jena University Hospital-Friedrich Schiller University Jena, Jena, Germany.

Ingo B Runnebaum (IB)

Department for Gynaecology and Reproductive Medicine, Jena University Hospital-Friedrich Schiller University Jena, Jena, Germany.

Bryan T Hennessy (BT)

Medical Oncology Group, Department of Molecular Medicine, Royal College of Surgeons in Ireland, Beaumont Hospital, Dublin, Ireland.
Department of Medical Oncology, Beaumont Hospital, Dublin, Ireland.
Our Lady of Lourdes Hospital, Drogheda, Ireland.

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