Genome-wide Analysis Identifies Novel Loci Associated with Ovarian Cancer Outcomes: Findings from the Ovarian Cancer Association Consortium

Sharon E Johnatty; Jonathan P Tyrer; Siddhartha Kar; Jonathan Beesley; Yi Lu; Bo Gao; Peter A Fasching; Alexander Hein; Arif B Ekici; Matthias W Beckmann; Diether Lambrechts; Els Van Nieuwenhuysen; Ignace Vergote; Sandrina Lambrechts; Mary Anne Rossing; Jennifer A Doherty; Jenny Chang-Claude; Francesmary Modugno; Roberta B Ness; Kirsten B Moysich; Douglas A Levine; Lambertus A Kiemeney; Leon F A G Massuger; Jacek Gronwald; Jan Lubiński; Anna Jakubowska; Cezary Cybulski; Louise Brinton; Jolanta Lissowska; Nicolas Wentzensen; Honglin Song; Valerie Rhenius; Ian Campbell; Diana Eccles; Weiva Sieh; Alice S Whittemore; Valerie McGuire; Joseph H Rothstein; Rebecca Sutphen; Hoda Anton-Culver; Argyrios Ziogas; Simon A Gayther; Aleksandra Gentry-Maharaj; Usha Menon; Susan J Ramus; Celeste L Pearce; Malcolm C Pike; Daniel O Stram; Anna H Wu; Jolanta Kupryjanczyk; Agnieszka Dansonka-Mieszkowska; Iwona K Rzepecka; Beata Spiewankiewicz; Marc T Goodman; Lynne R Wilkens; Michael E Carney; Pamela J Thompson; Florian Heitz; Andreas du Bois; Ira Schwaab; Philipp Harter; Jacobus Pisterer; Peter Hillemanns; Beth Y Karlan; Christine Walsh; Jenny Lester; Sandra Orsulic; Stacey J Winham; Madalene Earp; Melissa C Larson; Zachary C Fogarty; Estrid Høgdall; Allan Jensen; Susanne Kruger Kjaer; Brooke L Fridley; Julie M Cunningham; Robert A Vierkant; Joellen M Schildkraut; Edwin S Iversen; Kathryn L Terry; Daniel W Cramer; Elisa V Bandera; Irene Orlow; Tanja Pejovic; Yukie Bean; Claus Høgdall; Lene Lundvall; Ian McNeish; James Paul; Karen Carty; Nadeem Siddiqui; Rosalind Glasspool; Thomas Sellers; Catherine Kennedy; Yoke-Eng Chiew; Andrew Berchuck; Stuart MacGregor; Paul D P Pharoah; Ellen L Goode; Anna deFazio; Penelope M Webb; Georgia Chenevix-Trench; Australian Ovarian Cancer Study Group

doi:10.1158/1078-0432.CCR-15-0632

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Genome-wide Analysis Identifies Novel Loci Associated with Ovarian Cancer Outcomes: Findings from the Ovarian Cancer Association Consortium

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Genome-wide Analysis Identifies Novel Loci Associated with Ovarian Cancer Outcomes: Findings from the Ovarian Cancer Association Consortium

Sharon E Johnatty, Jonathan P Tyrer, Siddhartha Kar, Jonathan Beesley, Yi Lu, Bo Gao, Peter A Fasching, Alexander Hein, Arif B Ekici, Matthias W Beckmann, …

Clinical cancer research, Vol.21(23), pp.5264-5276

12/01/2015

DOI: https://doi.org/10.1158/1078-0432.CCR-15-0632

PMCID: PMC4624261

PMID: 26152742

Abstract

Alleles

Carcinoma, Ovarian Epithelial

Computational Biology - methods

Female

Genome-Wide Association Study

Genotype

Humans

Kaplan-Meier Estimate

Meta-Analysis as Topic

Neoplasms, Glandular and Epithelial - genetics

Neoplasms, Glandular and Epithelial - mortality

Neoplasms, Glandular and Epithelial - pathology

Ovarian Neoplasms - genetics

Ovarian Neoplasms - mortality

Ovarian Neoplasms - pathology

Ovarian Neoplasms - therapy

Patient Outcome Assessment

Polymorphism, Single Nucleotide

Prognosis

Quantitative Trait Loci

Chemotherapy resistance remains a major challenge in the treatment of ovarian cancer. We hypothesize that germline polymorphisms might be associated with clinical outcome. We analyzed approximately 2.8 million genotyped and imputed SNPs from the iCOGS experiment for progression-free survival (PFS) and overall survival (OS) in 2,901 European epithelial ovarian cancer (EOC) patients who underwent first-line treatment of cytoreductive surgery and chemotherapy regardless of regimen, and in a subset of 1,098 patients treated with ≥ 4 cycles of paclitaxel and carboplatin at standard doses. We evaluated the top SNPs in 4,434 EOC patients, including patients from The Cancer Genome Atlas. In addition, we conducted pathway analysis of all intragenic SNPs and tested their association with PFS and OS using gene set enrichment analysis. Five SNPs were significantly associated (P ≤ 1.0 × 10(-5)) with poorer outcomes in at least one of the four analyses, three of which, rs4910232 (11p15.3), rs2549714 (16q23), and rs6674079 (1q22), were located in long noncoding RNAs (lncRNAs) RP11-179A10.1, RP11-314O13.1, and RP11-284F21.8, respectively (P ≤ 7.1 × 10(-6)). ENCODE ChIP-seq data at 1q22 for normal ovary show evidence of histone modification around RP11-284F21.8, and rs6674079 is perfectly correlated with another SNP within the super-enhancer MEF2D, expression levels of which were reportedly associated with prognosis in another solid tumor. YAP1- and WWTR1 (TAZ)-stimulated gene expression and high-density lipoprotein (HDL)-mediated lipid transport pathways were associated with PFS and OS, respectively, in the cohort who had standard chemotherapy (pGSEA ≤ 6 × 10(-3)). We have identified SNPs in three lncRNAs that might be important targets for novel EOC therapies.

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Title: Genome-wide Analysis Identifies Novel Loci Associated with Ovarian Cancer Outcomes: Findings from the Ovarian Cancer Association Consortium
Creators: Sharon E Johnatty - Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia
Jonathan P Tyrer - Department of Oncology, Department of Public Health and Primary Care, University of Cambridge, Strangeways Research Laboratory, Cambridge, United Kingdom
Siddhartha Kar - Department of Oncology, Department of Public Health and Primary Care, University of Cambridge, Strangeways Research Laboratory, Cambridge, United Kingdom
Jonathan Beesley - Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia
Yi Lu - Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia
Bo Gao - Department of Gynaecological Oncology, Westmead Hospital, Sydney, New South Wales, Australia. Center for Cancer Research, University of Sydney at Westmead Millennium Institute, Sydney, New South Wales, Australia
Peter A Fasching - Division of Hematology and Oncology, Department of Medicine, University of California at Los Angeles, David Geffen School of Medicine, Los Angeles, California. University Hospital Erlangen, Institute of Human Genetics, Friedrich-Alexander-University Erlangen-Nuremberg, Erlangen, Germany
Alexander Hein - University Hospital Erlangen, Department of Gynecology and Obstetrics, Friedrich-Alexander-University Erlangen-Nuremberg, Comprehensive Cancer Center Erlangen-EMN, Erlangen, Germany
Arif B Ekici - University Hospital Erlangen, Institute of Human Genetics, Friedrich-Alexander-University Erlangen-Nuremberg, Erlangen, Germany
Matthias W Beckmann - University Hospital Erlangen, Department of Gynecology and Obstetrics, Friedrich-Alexander-University Erlangen-Nuremberg, Comprehensive Cancer Center Erlangen-EMN, Erlangen, Germany
Diether Lambrechts - Vesalius Research Center, VIB, Leuven, Belgium. Laboratory for Translational Genetics, Department of Oncology, University of Leuven, Leuven, Belgium
Els Van Nieuwenhuysen - Department of Gynecologic Oncology, Leuven Cancer Institute, University of Leuven, Leuven, Belgium
Ignace Vergote - Department of Gynecologic Oncology, Leuven Cancer Institute, University of Leuven, Leuven, Belgium
Sandrina Lambrechts - Department of Gynecologic Oncology, Leuven Cancer Institute, University of Leuven, Leuven, Belgium
Mary Anne Rossing - Program in Epidemiology, Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, Washington. Department of Epidemiology, University of Washington, Seattle, Washington
Jennifer A Doherty - Department of Community and Family Medicine, Section of Biostatistics and Epidemiology, The Geisel School of Medicine at Dartmouth, Lebanon, New Hampshire
Jenny Chang-Claude - German Cancer Research Center (DKFZ), Division of Cancer Epidemiology, Heidelberg, Germany
Francesmary Modugno - Department of Obstetrics, Gynecology and Reproductive Sciences, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania. Department of Epidemiology, University of Pittsburgh Graduate School of Public Health, Pittsburgh, Pennsylvania. Women's Cancer Research Program, Magee-Women's Research Institute and University of Pittsburgh Cancer Institute, Pittsburgh, Pennsylvania
Roberta B Ness - The University of Texas School of Public Health, Houston, Texas
Kirsten B Moysich - Department of Cancer Prevention and Control, Roswell Park Cancer Institute, Buffalo, New York
Douglas A Levine - Gynecology Service, Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, New York
Lambertus A Kiemeney - Radboud University Medical Centre, Radboud Institute for Health Sciences, Nijmegen, the Netherlands
Leon F A G Massuger - Radboud University Medical Centre, Radboud Institute for Molecular Sciences, Nijmegen, the Netherlands
Jacek Gronwald - International Hereditary Cancer Center, Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland
Jan Lubiński - International Hereditary Cancer Center, Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland
Anna Jakubowska - International Hereditary Cancer Center, Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland
Cezary Cybulski - International Hereditary Cancer Center, Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland
Louise Brinton - Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, Maryland
Jolanta Lissowska - Department of Cancer Epidemiology and Prevention, Maria Sklodowska-Curie Memorial Cancer Center and Institute of Oncology, Warsaw, Poland
Nicolas Wentzensen - Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, Maryland
Honglin Song - Department of Oncology, University of Cambridge, Strangeways Research Laboratory, Cambridge, United Kingdom
Valerie Rhenius - Department of Oncology, University of Cambridge, Strangeways Research Laboratory, Cambridge, United Kingdom
Ian Campbell - Cancer Genetics Laboratory, Research Division, Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia. Department of Oncology, The University of Melbourne, Melbourne, Victoria, Australia
Diana Eccles - Faculty of Medicine, University of Southampton, University Hospital Southampton, Southampton, Hampshire, United Kingdom
Weiva Sieh - Department of Health Research and Policy - Epidemiology, Stanford University School of Medicine, Stanford, California
Alice S Whittemore - Department of Health Research and Policy - Epidemiology, Stanford University School of Medicine, Stanford, California
Valerie McGuire - Department of Health Research and Policy - Epidemiology, Stanford University School of Medicine, Stanford, California
Joseph H Rothstein - Department of Health Research and Policy - Epidemiology, Stanford University School of Medicine, Stanford, California
Rebecca Sutphen - Epidemiology Center, College of Medicine, University of South Florida, Tampa, Florida
Hoda Anton-Culver - Department of Epidemiology, Center for Cancer Genetics Research and Prevention, School of Medicine, University of California Irvine, Irvine, California
Argyrios Ziogas - Department of Epidemiology, University of California Irvine, Irvine, California
Simon A Gayther - Department of Preventive Medicine, Keck School of Medicine, University of Southern California Norris Comprehensive Cancer Center, Los Angeles, California
Aleksandra Gentry-Maharaj - Women's Cancer, UCL EGA Institute for Women's Health, London, United Kingdom
Usha Menon - Women's Cancer, UCL EGA Institute for Women's Health, London, United Kingdom
Susan J Ramus - Department of Preventive Medicine, Keck School of Medicine, University of Southern California Norris Comprehensive Cancer Center, Los Angeles, California
Celeste L Pearce - Department of Preventive Medicine, Keck School of Medicine, University of Southern California Norris Comprehensive Cancer Center, Los Angeles, California. Department of Epidemiology, University of Michigan School of Public Health, Ann Arbor, Michigan
Malcolm C Pike - Department of Preventive Medicine, Keck School of Medicine, University of Southern California Norris Comprehensive Cancer Center, Los Angeles, California. Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, New York, New York
Daniel O Stram - Department of Preventive Medicine, Keck School of Medicine, University of Southern California Norris Comprehensive Cancer Center, Los Angeles, California
Anna H Wu - Department of Preventive Medicine, Keck School of Medicine, University of Southern California Norris Comprehensive Cancer Center, Los Angeles, California
Jolanta Kupryjanczyk - Department of Pathology and Laboratory Diagnostics, The Maria Sklodowska-Curie Memorial Cancer Center and Institute of Oncology, Warsaw, Poland
Agnieszka Dansonka-Mieszkowska - Department of Pathology and Laboratory Diagnostics, The Maria Sklodowska-Curie Memorial Cancer Center and Institute of Oncology, Warsaw, Poland
Iwona K Rzepecka - Department of Pathology and Laboratory Diagnostics, The Maria Sklodowska-Curie Memorial Cancer Center and Institute of Oncology, Warsaw, Poland
Beata Spiewankiewicz - Department of Gynecologic Oncology, The Maria Sklodowska-Curie Memorial Cancer Center and Institute of Oncology, Warsaw, Poland
Marc T Goodman - Cancer Prevention and Control, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, California. Community and Population Health Research Institute, Department of Biomedical Sciences, Cedars-Sinai Medical Center, Los Angeles, California
Lynne R Wilkens - Cancer Epidemiology Program, University of Hawaii Cancer Center, Honolulu, Hawaii
Michael E Carney - Cancer Epidemiology Program, University of Hawaii Cancer Center, Honolulu, Hawaii
Pamela J Thompson - Cancer Prevention and Control, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, California. Community and Population Health Research Institute, Department of Biomedical Sciences, Cedars-Sinai Medical Center, Los Angeles, California
Florian Heitz - Department of Gynecology and Gynecologic Oncology, Kliniken Essen-Mitte, Essen, Germany. Department of Gynecology and Gynecologic Oncology, Dr. Horst Schmidt Kliniken Wiesbaden, Wiesbaden, Germany
Andreas du Bois - Department of Gynecology and Gynecologic Oncology, Kliniken Essen-Mitte, Essen, Germany. Department of Gynecology and Gynecologic Oncology, Dr. Horst Schmidt Kliniken Wiesbaden, Wiesbaden, Germany
Ira Schwaab - Institut für Humangenetik Wiesbaden, Wiesbaden, Germany
Philipp Harter - Department of Gynecology and Gynecologic Oncology, Kliniken Essen-Mitte, Essen, Germany. Department of Gynecology and Gynecologic Oncology, Dr. Horst Schmidt Kliniken Wiesbaden, Wiesbaden, Germany
Jacobus Pisterer - Zentrum für Gynäkologische Onkologie, Kiel, Germany
Peter Hillemanns - Department of Obstetrics and Gynaecology, Hannover Medical School, Hannover, Germany
Beth Y Karlan - Women's Cancer Program at the Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, California
Christine Walsh - Women's Cancer Program at the Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, California
Jenny Lester - Women's Cancer Program at the Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, California
Sandra Orsulic - Women's Cancer Program at the Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, California
Stacey J Winham - Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota
Madalene Earp - Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota
Melissa C Larson - Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota
Zachary C Fogarty - Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota
Estrid Høgdall - Department of Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Copenhagen, Denmark. Molecular Unit, Department of Pathology, Herlev Hospital, University of Copenhagen, Copenhagen, Denmark
Allan Jensen - Department of Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Copenhagen, Denmark
Susanne Kruger Kjaer - Department of Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Copenhagen, Denmark. Department of Gynecology, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark
Brooke L Fridley - Biostatistics and Informatics Shared Resource, University of Kansas Medical Center, Kansas City, Kansas
Julie M Cunningham - Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, Minnesota
Robert A Vierkant - Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota
Joellen M Schildkraut - Department of Community and Family Medicine, Duke University Medical Center, Durham, North Carolina. Cancer Control and Population Sciences, Duke Cancer Institute, Durham, North Carolina
Edwin S Iversen - Department of Statistical Science, Duke University, Durham, North Carolina
Kathryn L Terry - Obstetrics and Gynecology Epidemiology Center, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts. Harvard School of Public Health, Boston, Massachusetts
Daniel W Cramer - Obstetrics and Gynecology Epidemiology Center, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts. Harvard School of Public Health, Boston, Massachusetts
Elisa V Bandera - Cancer Prevention and Control Program, Rutgers Cancer Institute of New Jersey, The State University of New Jersey, New Brunswick, New Jersey
Irene Orlow - Memorial Sloan Kettering Cancer Center, Department of Epidemiology and Biostatistics, Epidemiology Service, New York, New York
Tanja Pejovic - Department of Obstetrics and Gynecology, Oregon Health and Science University, Portland, Oregon. Knight Cancer Institute, Portland, Oregon
Yukie Bean - Department of Obstetrics and Gynecology, Oregon Health and Science University, Portland, Oregon. Knight Cancer Institute, Portland, Oregon
Claus Høgdall - Department of Gynaecology, The Juliane Marie Centre, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark
Lene Lundvall - Department of Gynaecology, The Juliane Marie Centre, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark
Ian McNeish - Institute of Cancer Sciences, University of Glasgow, Wolfson Wohl Cancer Research Centre, Beatson Institute for Cancer Research, Glasgow, United Kingdom
James Paul - Cancer Research UK Clinical Trials Unit, Glasgow, The Beatson West of Scotland Cancer Centre, Glasgow, United Kingdom
Karen Carty - Cancer Research UK Clinical Trials Unit, Glasgow, The Beatson West of Scotland Cancer Centre, Glasgow, United Kingdom
Nadeem Siddiqui - Department of Gynaecological Oncology, Glasgow Royal Infirmary, Glasgow, United Kingdom
Rosalind Glasspool - Cancer Research UK Clinical Trials Unit, Glasgow, The Beatson West of Scotland Cancer Centre, Glasgow, United Kingdom
Thomas Sellers - Department of Cancer Epidemiology, Moffitt Cancer Center, Tampa, Florida
Catherine Kennedy - Department of Gynaecological Oncology, Westmead Hospital, Sydney, New South Wales, Australia. Center for Cancer Research, University of Sydney at Westmead Millennium Institute, Sydney, New South Wales, Australia
Yoke-Eng Chiew - Department of Gynaecological Oncology, Westmead Hospital, Sydney, New South Wales, Australia. Center for Cancer Research, University of Sydney at Westmead Millennium Institute, Sydney, New South Wales, Australia
Andrew Berchuck - Department of Obstetrics and Gynecology, Duke University Medical Center, Durham, North Carolina
Stuart MacGregor - Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia
Paul D P Pharoah - Department of Oncology, Department of Public Health and Primary Care, University of Cambridge, Strangeways Research Laboratory, Cambridge, United Kingdom
Ellen L Goode - Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota
Anna deFazio - Department of Gynaecological Oncology, Westmead Hospital, Sydney, New South Wales, Australia. Center for Cancer Research, University of Sydney at Westmead Millennium Institute, Sydney, New South Wales, Australia
Penelope M Webb - Department of Population Health, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia
Georgia Chenevix-Trench - Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia. georgia.trench@qimrberghofer.edu.au
Australian Ovarian Cancer Study Group
Publication Details: Clinical cancer research, Vol.21(23), pp.5264-5276
Date published: 12/01/2015
Grant note: R03 CA113148 / NCI NIH HHS K22-CA138563 / NCI NIH HHS N01 CN025403 / NCI NIH HHS A10119 / Cancer Research UK R01CA095023 / NCI NIH HHS K22 CA138563 / NCI NIH HHS M01-RR000056 / NCRR NIH HHS R03 CA115195 / NCI NIH HHS P30 CA071789 / NCI NIH HHS Canadian Institutes of Health Research U19 CA148537 / NCI NIH HHS 1U19 CA148537 / NCI NIH HHS R01 CA058598 / NCI NIH HHS R01 CA128978 / NCI NIH HHS C1287/A10710 / Cancer Research UK M01 RR000056 / NCRR NIH HHS P01 CA017054 / NCI NIH HHS C490/A10124 / Cancer Research UK N01PC67010 / NCI NIH HHS K07-CA80668 / NCI NIH HHS R01CA61132 / NCI NIH HHS P50 CA105009 / NCI NIH HHS R01 CA83918 / NCI NIH HHS R01 CA083918 / NCI NIH HHS C5047/A8384 / Cancer Research UK R01 CA054419 / NCI NIH HHS R01 CA095023 / NCI NIH HHS K07 CA080668 / NCI NIH HHS R01 CA076016 / NCI NIH HHS R01-CA87538 / NCI NIH HHS C536/A6689 / Cancer Research UK R01 CA087538 / NCI NIH HHS C490/A16561 / Cancer Research UK R01 CA122443 / NCI NIH HHS A13086 / Cancer Research UK R03CA115195 / NCI NIH HHS CA128978 / NCI NIH HHS C490/A8339 / Cancer Research UK P30CA14089 / NCI NIH HHS C490/A10119 / Cancer Research UK R01-CA126841 / NCI NIH HHS P30 CA015083 / NCI NIH HHS K07 CA095666 / NCI NIH HHS R01 CA112523 / NCI NIH HHS 1U19 CA148112 / NCI NIH HHS P30-CA072720 / NCI NIH HHS NIH R01-CA112523 / NCI NIH HHS U19 CA148065 / NCI NIH HHS R03CA113148 / NCI NIH HHS 10124 / Cancer Research UK P50 CA159981 / NCI NIH HHS U19 CA148112 / NCI NIH HHS C5047/A15007 / Cancer Research UK C490/A6187 / Cancer Research UK UL1 TR000124 / NCATS NIH HHS P30-CA008748 / NCI NIH HHS C5047/A10692 / Cancer Research UK N01CN025403 / NCI NIH HHS C1287/A10118 / Cancer Research UK N01 PC067010 / NCI NIH HHS UL1TR000124 / NCATS NIH HHS 1U19 CA148065 / NCI NIH HHS P30 CA008748 / NCI NIH HHS C12292/A11174 / Cancer Research UK P01CA17054 / NCI NIH HHS P50-CA159981 / NCI NIH HHS C536/A13086 / Cancer Research UK P50 CA136393 / NCI NIH HHS R01 CA126841 / NCI NIH HHS MR/N005813/1 / Medical Research Council C8197/A16565 / Cancer Research UK C1281/A12014 / Cancer Research UK P30 CA014089 / NCI NIH HHS R01 CA 058598 / NCI NIH HHS P30 CA072720 / NCI NIH HHS
Academic Unit: Cancer Epidemiology and Health Outcomes
Language: English
Resource Type: Journal article
Identifiers: 991031665320004646