A comprehensive gene–environment interaction analysis in Ovarian Cancer using genome-wide significant common variants
Sehee Kim
Department of Biostatistics, University of Michigan School of Public Health, Ann Arbor, MI, USA
S.K. and M. W. contributed equally to this workSearch for more papers by this authorMiao Wang
Department of Biostatistics, University of Michigan School of Public Health, Ann Arbor, MI, USA
S.K. and M. W. contributed equally to this workSearch for more papers by this authorJonathan P. Tyrer
Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, United Kingdom
Search for more papers by this authorAllan Jensen
Department of Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Copenhagen, Denmark
Search for more papers by this authorAshley Wiensch
Department of Epidemiology, University of Michigan School of Public Health, Ann Arbor, MI, USA
Search for more papers by this authorGang Liu
Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, MA, USA
Search for more papers by this authorAlice W. Lee
Department of Public Health, California State University, Fullerton, Fullerton, CA, USA
Search for more papers by this authorRoberta B. Ness
University of Texas School of Public Health, Houston, TX, USA
Search for more papers by this authorMaxwell Salvatore
Department of Biostatistics, University of Michigan School of Public Health, Ann Arbor, MI, USA
Department of Epidemiology, University of Michigan School of Public Health, Ann Arbor, MI, USA
Search for more papers by this authorShelley S. Tworoger
Department of Cancer Epidemiology, Moffitt Cancer Center, Tampa, FL, USA
Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA
Search for more papers by this authorAlice S. Whittemore
Department of Health Research and Policy - Epidemiology, Stanford University School of Medicine, Stanford, CA, USA
Department of Biomedical Data Science, Stanford University School of Medicine, Stanford, CA, USA
Search for more papers by this authorHoda Anton-Culver
Department of Epidemiology, Genetic Epidemiology Research Institute, University of California Irvine, Irvine, CA, USA
Search for more papers by this authorWeiva Sieh
Department of Genetics and Genomic Sciences, Department of Population Health Science and Policy, Icahn School of Medicine at Mount Sinai, New York, NY, USA
Search for more papers by this authorSara H. Olson
Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, New York, NY, USA
Search for more papers by this authorAndrew Berchuck
Department of Obstetrics and Gynecology, Duke University Medical Center, Durham, NC, USA
Search for more papers by this authorEllen L. Goode
Department of Health Sciences Research, Mayo Clinic, Rochester, MN, USA
Search for more papers by this authorMarc T. Goodman
Cancer Prevention and Control, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, CA, USA
Department of Biomedical Sciences, Cedars-Sinai Medical Center, Community and Population Health Research Institute, Los Angeles, CA, USA
Search for more papers by this authorJennifer Anne Doherty
Department of Population Health Sciences, Huntsman Cancer Institute, University of Utah, Salt Lake City, UT, USA
Search for more papers by this authorGeorgia Chenevix-Trench
Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, QLD, Australia
Search for more papers by this authorMary Anne Rossing
Program in Epidemiology, Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA, USA
Department of Epidemiology, University of Washington, Seattle, WA, USA
Search for more papers by this authorPenelope M. Webb
Population Health Department, QIMR Berghofer Medical Research Institute, Brisbane, QLD, Australia
Search for more papers by this authorGraham G. Giles
Cancer Epidemiology & Intelligence Division, Cancer Council Victoria, Melbourne, VIC, Australia
Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Melbourne, Victoria, Australia
Department of Epidemiology and Preventive Medicine, Monash University, Melbourne, VIC, Australia
Search for more papers by this authorKathryn L. Terry
Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA
Obstetrics and Gynecology Epidemiology Center, Brigham and Women's Hospital, Boston, MA, USA
Search for more papers by this authorArgyrios Ziogas
Department of Epidemiology, Genetic Epidemiology Research Institute, University of California Irvine, Irvine, CA, USA
Search for more papers by this authorRenée T. Fortner
Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany
Search for more papers by this authorUsha Menon
Gynaecological Cancer Research Centre, Women's Cancer, Institute for Women's Health, University College London, London, United Kingdom
Search for more papers by this authorSimon A. Gayther
Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
Center for Cancer Prevention and Translational Genomics, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, CA, USA
Department of Biomedical Sciences, Cedars-Sinai Medical Center, Los Angeles, CA, USA
Search for more papers by this authorAnna H. Wu
Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
Search for more papers by this authorHonglin Song
Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, United Kingdom
Search for more papers by this authorAngela Brooks-Wilson
Genome Sciences Centre, BC Cancer Agency, Vancouver, BC, Canada
Department of Biomedical Physiology and Kinesiology, Simon Fraser University, Burnaby, BC, Canada
Search for more papers by this authorElisa V. Bandera
Cancer Prevention and Control Program, Rutgers Cancer Institute of New Jersey, New Brunswick, NJ, USA
Search for more papers by this authorLinda S. Cook
University of New Mexico Health Sciences Center, University of New Mexico, Albuquerque, NM, USA
Division of Cancer Care, Department of Population Health Research, Alberta Health Services, Calgary, AB, Canada
Search for more papers by this authorDaniel W. Cramer
Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA
Obstetrics and Gynecology Epidemiology Center, Brigham and Women's Hospital, Boston, MA, USA
Search for more papers by this authorRoger L. Milne
Cancer Epidemiology & Intelligence Division, Cancer Council Victoria, Melbourne, VIC, 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, VIC, Australia
Search for more papers by this authorStacey J. Winham
Department of Health Sciences Research, Mayo Clinic, Rochester, MN, USA
Search for more papers by this authorSusanne K. Kjaer
Department of Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Copenhagen, Denmark
Department of Gynaecology, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark
Search for more papers by this authorFrancesmary Modugno
Ovarian Cancer Center of Excellence, Womens Cancer Research Program, Magee-Womens Research Institute and Hillman Cancer Center, Pittsburgh, PA, USA
Department of Epidemiology, University of Pittsburgh Graduate School of Public Health, Pittsburgh, PA, USA
Division of Gynecologic Oncology, Department of Obstetrics, Gynecology and Reproductive Sciences, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
Search for more papers by this authorPamela J. Thompson
Cancer Prevention and Control, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, CA, USA
Search for more papers by this authorJenny Chang-Claude
Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany
Cancer Epidemiology Group, University Cancer Center Hamburg (UCCH), University Medical Center Hamburg-Eppendorf, Hamburg, Germany
Search for more papers by this authorHolly R. Harris
Program in Epidemiology, Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA, USA
Search for more papers by this authorJoellen M. Schildkraut
Department of Public Health Sciences, University of Virginia, Charlottesville, VA, USA
Search for more papers by this authorNhu D. Le
Cancer Control Research, BC Cancer Agency, Vancouver, BC, Canada
Search for more papers by this authorNico Wentzensen
Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA
Search for more papers by this authorBritton Trabert
Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA
Search for more papers by this authorEstrid 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
Search for more papers by this authorDavid Huntsman
British Columbia's Ovarian Cancer Research (OVCARE) program, Vancouver General Hospital, BC Cancer and University of British Columbia
Department of Pathology and Laboratory Medicine, and Obstetrics and Gynecology, University of British Columbia, Vancouver, BC, Canada
Search for more papers by this authorMalcolm C. Pike
Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, New York, NY, USA
Department of Preventive Medicine, Keck School of Medicine, University of Southern California Norris Comprehensive Cancer Center, Los Angeles, CA, USA
Search for more papers by this authorPaul D.P. Pharoah
Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, United Kingdom
Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom
Search for more papers by this authorCeleste Leigh Pearce
Department of Epidemiology, University of Michigan School of Public Health, Ann Arbor, MI, USA
Center for Cancer Prevention and Translational Genomics, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, CA, USA
Search for more papers by this authorCorresponding Author
Bhramar Mukherjee
Department of Biostatistics, University of Michigan School of Public Health, Ann Arbor, MI, USA
Correspondence to: Bhramar Mukherjee, SPH Tower, 1415 Washington Heights, Ann Arbor MI 48109, USA, Tel.: 734-764-6544; Fax: 734-764-3192, E-mail: [email protected]Search for more papers by this authorSehee Kim
Department of Biostatistics, University of Michigan School of Public Health, Ann Arbor, MI, USA
S.K. and M. W. contributed equally to this workSearch for more papers by this authorMiao Wang
Department of Biostatistics, University of Michigan School of Public Health, Ann Arbor, MI, USA
S.K. and M. W. contributed equally to this workSearch for more papers by this authorJonathan P. Tyrer
Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, United Kingdom
Search for more papers by this authorAllan Jensen
Department of Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Copenhagen, Denmark
Search for more papers by this authorAshley Wiensch
Department of Epidemiology, University of Michigan School of Public Health, Ann Arbor, MI, USA
Search for more papers by this authorGang Liu
Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, MA, USA
Search for more papers by this authorAlice W. Lee
Department of Public Health, California State University, Fullerton, Fullerton, CA, USA
Search for more papers by this authorRoberta B. Ness
University of Texas School of Public Health, Houston, TX, USA
Search for more papers by this authorMaxwell Salvatore
Department of Biostatistics, University of Michigan School of Public Health, Ann Arbor, MI, USA
Department of Epidemiology, University of Michigan School of Public Health, Ann Arbor, MI, USA
Search for more papers by this authorShelley S. Tworoger
Department of Cancer Epidemiology, Moffitt Cancer Center, Tampa, FL, USA
Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA
Search for more papers by this authorAlice S. Whittemore
Department of Health Research and Policy - Epidemiology, Stanford University School of Medicine, Stanford, CA, USA
Department of Biomedical Data Science, Stanford University School of Medicine, Stanford, CA, USA
Search for more papers by this authorHoda Anton-Culver
Department of Epidemiology, Genetic Epidemiology Research Institute, University of California Irvine, Irvine, CA, USA
Search for more papers by this authorWeiva Sieh
Department of Genetics and Genomic Sciences, Department of Population Health Science and Policy, Icahn School of Medicine at Mount Sinai, New York, NY, USA
Search for more papers by this authorSara H. Olson
Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, New York, NY, USA
Search for more papers by this authorAndrew Berchuck
Department of Obstetrics and Gynecology, Duke University Medical Center, Durham, NC, USA
Search for more papers by this authorEllen L. Goode
Department of Health Sciences Research, Mayo Clinic, Rochester, MN, USA
Search for more papers by this authorMarc T. Goodman
Cancer Prevention and Control, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, CA, USA
Department of Biomedical Sciences, Cedars-Sinai Medical Center, Community and Population Health Research Institute, Los Angeles, CA, USA
Search for more papers by this authorJennifer Anne Doherty
Department of Population Health Sciences, Huntsman Cancer Institute, University of Utah, Salt Lake City, UT, USA
Search for more papers by this authorGeorgia Chenevix-Trench
Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, QLD, Australia
Search for more papers by this authorMary Anne Rossing
Program in Epidemiology, Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA, USA
Department of Epidemiology, University of Washington, Seattle, WA, USA
Search for more papers by this authorPenelope M. Webb
Population Health Department, QIMR Berghofer Medical Research Institute, Brisbane, QLD, Australia
Search for more papers by this authorGraham G. Giles
Cancer Epidemiology & Intelligence Division, Cancer Council Victoria, Melbourne, VIC, Australia
Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Melbourne, Victoria, Australia
Department of Epidemiology and Preventive Medicine, Monash University, Melbourne, VIC, Australia
Search for more papers by this authorKathryn L. Terry
Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA
Obstetrics and Gynecology Epidemiology Center, Brigham and Women's Hospital, Boston, MA, USA
Search for more papers by this authorArgyrios Ziogas
Department of Epidemiology, Genetic Epidemiology Research Institute, University of California Irvine, Irvine, CA, USA
Search for more papers by this authorRenée T. Fortner
Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany
Search for more papers by this authorUsha Menon
Gynaecological Cancer Research Centre, Women's Cancer, Institute for Women's Health, University College London, London, United Kingdom
Search for more papers by this authorSimon A. Gayther
Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
Center for Cancer Prevention and Translational Genomics, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, CA, USA
Department of Biomedical Sciences, Cedars-Sinai Medical Center, Los Angeles, CA, USA
Search for more papers by this authorAnna H. Wu
Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
Search for more papers by this authorHonglin Song
Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, United Kingdom
Search for more papers by this authorAngela Brooks-Wilson
Genome Sciences Centre, BC Cancer Agency, Vancouver, BC, Canada
Department of Biomedical Physiology and Kinesiology, Simon Fraser University, Burnaby, BC, Canada
Search for more papers by this authorElisa V. Bandera
Cancer Prevention and Control Program, Rutgers Cancer Institute of New Jersey, New Brunswick, NJ, USA
Search for more papers by this authorLinda S. Cook
University of New Mexico Health Sciences Center, University of New Mexico, Albuquerque, NM, USA
Division of Cancer Care, Department of Population Health Research, Alberta Health Services, Calgary, AB, Canada
Search for more papers by this authorDaniel W. Cramer
Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA
Obstetrics and Gynecology Epidemiology Center, Brigham and Women's Hospital, Boston, MA, USA
Search for more papers by this authorRoger L. Milne
Cancer Epidemiology & Intelligence Division, Cancer Council Victoria, Melbourne, VIC, 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, VIC, Australia
Search for more papers by this authorStacey J. Winham
Department of Health Sciences Research, Mayo Clinic, Rochester, MN, USA
Search for more papers by this authorSusanne K. Kjaer
Department of Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Copenhagen, Denmark
Department of Gynaecology, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark
Search for more papers by this authorFrancesmary Modugno
Ovarian Cancer Center of Excellence, Womens Cancer Research Program, Magee-Womens Research Institute and Hillman Cancer Center, Pittsburgh, PA, USA
Department of Epidemiology, University of Pittsburgh Graduate School of Public Health, Pittsburgh, PA, USA
Division of Gynecologic Oncology, Department of Obstetrics, Gynecology and Reproductive Sciences, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
Search for more papers by this authorPamela J. Thompson
Cancer Prevention and Control, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, CA, USA
Search for more papers by this authorJenny Chang-Claude
Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany
Cancer Epidemiology Group, University Cancer Center Hamburg (UCCH), University Medical Center Hamburg-Eppendorf, Hamburg, Germany
Search for more papers by this authorHolly R. Harris
Program in Epidemiology, Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA, USA
Search for more papers by this authorJoellen M. Schildkraut
Department of Public Health Sciences, University of Virginia, Charlottesville, VA, USA
Search for more papers by this authorNhu D. Le
Cancer Control Research, BC Cancer Agency, Vancouver, BC, Canada
Search for more papers by this authorNico Wentzensen
Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA
Search for more papers by this authorBritton Trabert
Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA
Search for more papers by this authorEstrid 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
Search for more papers by this authorDavid Huntsman
British Columbia's Ovarian Cancer Research (OVCARE) program, Vancouver General Hospital, BC Cancer and University of British Columbia
Department of Pathology and Laboratory Medicine, and Obstetrics and Gynecology, University of British Columbia, Vancouver, BC, Canada
Search for more papers by this authorMalcolm C. Pike
Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, New York, NY, USA
Department of Preventive Medicine, Keck School of Medicine, University of Southern California Norris Comprehensive Cancer Center, Los Angeles, CA, USA
Search for more papers by this authorPaul D.P. Pharoah
Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, United Kingdom
Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom
Search for more papers by this authorCeleste Leigh Pearce
Department of Epidemiology, University of Michigan School of Public Health, Ann Arbor, MI, USA
Center for Cancer Prevention and Translational Genomics, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, CA, USA
Search for more papers by this authorCorresponding Author
Bhramar Mukherjee
Department of Biostatistics, University of Michigan School of Public Health, Ann Arbor, MI, USA
Correspondence to: Bhramar Mukherjee, SPH Tower, 1415 Washington Heights, Ann Arbor MI 48109, USA, Tel.: 734-764-6544; Fax: 734-764-3192, E-mail: [email protected]Search for more papers by this authorAbstract
As a follow-up to genome-wide association analysis of common variants associated with ovarian carcinoma (cancer), our study considers seven well-known ovarian cancer risk factors and their interactions with 28 genome-wide significant common genetic variants. The interaction analyses were based on data from 9971 ovarian cancer cases and 15,566 controls from 17 case–control studies. Likelihood ratio and Wald tests for multiplicative interaction and for relative excess risk due to additive interaction were used. The top multiplicative interaction was noted between oral contraceptive pill (OCP) use (ever vs. never) and rs13255292 (p value = 3.48 × 10−4). Among women with the TT genotype for this variant, the odds ratio for OCP use was 0.53 (95% CI = 0.46–0.60) compared to 0.71 (95%CI = 0.66–0.77) for women with the CC genotype. When stratified by duration of OCP use, women with 1–5 years of OCP use exhibited differential protective benefit across genotypes. However, no interaction on either the multiplicative or additive scale was found to be statistically significant after multiple testing correction. The results suggest that OCP use may offer increased benefit for women who are carriers of the T allele in rs13255292. On the other hand, for women carrying the C allele in this variant, longer (5+ years) use of OCP may reduce the impact of carrying the risk allele of this SNP. Replication of this finding is needed. The study presents a comprehensive analytic framework for conducting gene–environment analysis in ovarian cancer.
Abstract
What's new?
Genetic and environmental risk factors for ovarian cancer have been identified separately but interactions between both remain largely unexplored. The authors identified a new gene x environment interaction between oral contraceptive pill (OCP) use and a single nucleotide polymorphism in the PVT1 gene, a long-noncoding RNA located on chromosome 8. The data suggest that the protective benefit of OCP use may be strongest in women with the T allele of PVT1 underscoring the need to tailor prevention strategies to individual genotypic profiles.
Supporting Information
| Filename | Description |
|---|---|
| IJC_SupplementalMaterial_revision_111518.docxWord 2007 document , 755.2 KB |
Figure S1 – Site-specific missing data structure for raw E data and harmonized E data Figure S2 – Estimated Absolute risk for ovarian cancer given type of HT use and number of risk alleles in rs11658063 Table S1 – Characteristics of 19 case–control studies from the ovarian cancer association consortium (OCAC) included in the analyses Table S2 – Odds ratios for marginal associations of seven environmental risk factors in complete cases analysis and multiple imputation analysis. Table S3 – LRTs for multiplicative and additive interactions between 28 SNP and 7 risk factor (showing p value < 0.2) Table S4 – Estimated ARs stratified by OCP use or duration of OCP use and number of risk allele of rs1325292 Table S5 – Observed and expected OR under multiplicative and additive null for six gene–environment pairs (showing p value < 0.01 on Global LRT) |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- 1 Society AC. Cancer Facts & Figures 2017. American Cancer Society 2017.
- 2Jacobs IJ, Menon U, Ryan A, et al. Ovarian cancer screening and mortality in the UK collaborative trial of Ovarian Cancer screening (UKCTOCS): a randomised controlled trial. Lancet (London, England) 2016; 387: 945–56.
- 3Pearce CL, Rossing MA, Lee AW, et al. Combined and interactive effects of environmental and GWAS-identified risk factors in ovarian cancer. Cancer Epidemiol Biomarkers Prev 2013; 22: 880–90.
- 4Trabert B, Ness RB, Lo-Ciganic WH, et al. Aspirin, nonaspirin nonsteroidal anti-inflammatory drug, and acetaminophen use and risk of invasive epithelial ovarian cancer: a pooled analysis in the Ovarian Cancer association consortium. J Natl Cancer Inst 2014; 106: djt431.
- 5Sieh W, Salvador S, McGuire V, et al. Tubal ligation and risk of ovarian cancer subtypes: a pooled analysis of case-control studies. Int J Epidemiol 2013; 42: 579–89.
- 6Falconer H, Yin L, Gronberg H, et al. Ovarian cancer risk after salpingectomy: a nationwide population-based study. J Natl Cancer Inst 2015; 107: dju410.
- 7Lessard-Anderson CR, Handlogten KS, Molitor RJ, et al. Effect of tubal sterilization technique on risk of serous epithelial ovarian and primary peritoneal carcinoma. Gynecol Oncol 2014; 135: 423–7.
- 8Madsen C, Baandrup L, Dehlendorff C, et al. Tubal ligation and salpingectomy and the risk of epithelial ovarian cancer and borderline ovarian tumors: a nationwide case-control study. Acta Obstet Gynecol Scand 2015; 94: 86–94.
- 9Yoon SH, Kim SN, Shim SH, et al. Bilateral salpingectomy can reduce the risk of ovarian cancer in the general population: a meta-analysis. Eur J Cancer 2016; 55: 38–46.
- 10Bojesen SE, Pooley KA, Johnatty SE, et al. Multiple independent variants at the TERT locus are associated with telomere length and risks of breast and ovarian cancer. Nat Genet 2013; 45: 371–84. 84e1-2.
- 11Bolton KL, Tyrer J, Song H, et al. Common variants at 19p13 are associated with susceptibility to ovarian cancer. Nat Genet 2010; 42: 880–4.
- 12Goode EL, Chenevix-Trench G, Song H, et al. A genome-wide association study identifies susceptibility loci for ovarian cancer at 2q31 and 8q24. Nat Genet 2010; 42: 874–9.
- 13Kar SP, Beesley J, Amin Al Olama A, et al. Genome-wide meta-analyses of breast, Ovarian, and prostate Cancer association studies identify multiple new susceptibility loci shared by at least two Cancer types. Cancer Discov 2016; 6: 1052–67.
- 14Kelemen LE, Lawrenson K, Tyrer J, et al. Genome-wide significant risk associations for mucinous ovarian carcinoma. Nat Genet 2015; 47: 888–97.
- 15Kuchenbaecker KB, Ramus SJ, Tyrer J, et al. Identification of six new susceptibility loci for invasive epithelial ovarian cancer. Nat Genet 2015; 47: 164–71.
- 16Permuth-Wey J, Lawrenson K, Shen HC, et al. Identification and molecular characterization of a new ovarian cancer susceptibility locus at 17q21.31. Nature communications 2013; 4: 1627.
- 17Pharoah PD, Tsai YY, Ramus SJ, et al. GWAS meta-analysis and replication identifies three new susceptibility loci for ovarian cancer. Nat Genet 2013; 45: 362–70. 70e1-2.
- 18Phelan CM, Kuchenbaecker KB, Tyrer JP, et al. Identification of 12 new susceptibility loci for different histotypes of epithelial ovarian cancer. Nat Genet 2017; 49: 680–91.
- 19Shen H, Fridley BL, Song H, et al. Epigenetic analysis leads to identification of HNF1B as a subtype-specific susceptibility gene for ovarian cancer. Nat Commun 2013; 4: 1628.
- 20Song H, Ramus SJ, Tyrer J, et al. A genome-wide association study identifies a new ovarian cancer susceptibility locus on 9p22.2. Nat Genet 2009; 41: 996–1000.
- 21Auranen A, Pukkala E, Makinen J, et al. Cancer incidence in the first-degree relatives of ovarian cancer patients. Duodecim; laaketieteellinen aikakauskirja 1997; 113: 46–50.
- 22Stratton JF, Pharoah P, Smith SK, et al. A systematic review and meta-analysis of family history and risk of ovarian cancer. Br J Obstet Gynaecol 1998; 105: 493–9.
- 23Lee AW, Ness RB, Roman LD, et al. Association between menopausal estrogen-only therapy and Ovarian carcinoma risk. Obstet Gynecol 2016; 127: 828–36.
- 24Pearce CL, Chung K, Pike MC, et al. Increased ovarian cancer risk associated with menopausal estrogen therapy is reduced by adding a progestin. Cancer 2009; 115: 531–9.
- 25 Collaborative Group On Epidemiological Studies Of Ovarian C, Beral V, Gaitskell K, et al. Menopausal hormone use and ovarian cancer risk: individual participant meta-analysis of 52 epidemiological studies. Lancet (London, England) 2015; 385: 1835–42.
- 26Olsen CM, Nagle CM, Whiteman DC, et al. Obesity and risk of ovarian cancer subtypes: evidence from the Ovarian Cancer association consortium. Endocr Relat Cancer 2013; 20: 251–62.
- 27Pearce CL, Templeman C, Rossing MA, et al. Association between endometriosis and risk of histological subtypes of ovarian cancer: a pooled analysis of case-control studies. Lancet Oncol 2012; 13: 385–94.
- 28 SEER Cancer Statistics Review 1975-2014, Based on November 2016 SEER data submission, posted to the SEER web site, April 2017.
- 29Pearce CL, Stram DO, Ness RB, et al. Population distribution of lifetime risk of Ovarian Cancer in the United States. Cancer Epidemiol Biomarkers Prev 2015; 24: 671–6.
- 30Liu G, Lee S, Lee AW, et al. Robust tests for additive gene-environment interaction in case-control studies using gene-environment Independence. Am J Epidemiol 2017; 187: 366–377.
- 31Garcia-Closas M, Rothman N, Figueroa JD, et al. Common genetic polymorphisms modify the effect of smoking on absolute risk of bladder cancer. Cancer Res 2013; 73: 2211–20.
- 32Knol MJ, Vanderweele TJ, Groenwold RH, et al. Estimating measures of interaction on an additive scale for preventive exposures. Eur J Epidemiol 2011; 26: 433–8.
- 33Liu G, Mukherjee B, Lee S, et al. Robust tests for additive gene-environment interaction in case-control studies using gene-environment Independence. Am J Epidemiol 2018; 187: 366–77.
- 34Vanderweele TJ, Vansteelandt S. A weighting approach to causal effects and additive interaction in case-control studies: marginal structural linear odds models. Am J Epidemiol 2011; 174: 1197–203.
- 35Vanderweele TJ. Sample size and power calculations for additive interactions. Epidemiol Methods 2012; 1: 159–88.
- 36Bolton KL, Ganda C, Berchuck A, et al. Role of common genetic variants in ovarian cancer susceptibility and outcome: progress to date from the Ovarian Cancer association consortium (OCAC). J Intern Med 2012; 271: 366–78.
- 37 Little RJA, Rubin DB. Chapter 10: Bayes and multiple imputation statistical analysis with missing data, 2nd edn. NJ: John Wiley & Sons, 2002.
10.1002/9781119013563 Google Scholar
- 38Nickels S, Truong T, Hein R, et al. Evidence of gene-environment interactions between common breast cancer susceptibility loci and established environmental risk factors. PLoS Genet 2013; 9: e1003284.
- 39Bhattacharjee S Cn, Han S and Wheeler W. CGEN: An R package for analysis of case-control studies in genetic epidemiology, 2012.
- 40Han SS, Rosenberg PS, Garcia-Closas M, et al. Likelihood ratio test for detecting gene (G)-environment (E) interactions under an additive risk model exploiting G-E independence for case-control data. Am J Epidemiol 2012; 176: 1060–7.
- 41 SEER, ed. Cancer stat facts: Ovarian Cancer. In: SEER, ed., vol. 2017. National Cancer Institute. Bethesda, MD.
- 42Haiman CA, Patterson N, Freedman ML, et al. Multiple regions within 8q24 independently affect risk for prostate cancer. Nat Genet 2007; 39: 638–44.
- 43Shi J, Zhang Y, Zheng W, et al. Fine-scale mapping of 8q24 locus identifies multiple independent risk variants for breast cancer. Int J Cancer 2016; 139: 1303–17.
- 44Tseng YY, Bagchi A. The PVT1-MYC duet in cancer. Mol Cell Oncol 2015; 2: e974467.
- 45Shang Y, Brown M. Molecular determinants for the tissue specificity of SERMs. Science 2002; 295: 2465–8.
- 46Wang C, Mayer JA, Mazumdar A, et al. Estrogen induces c-myc gene expression via an upstream enhancer activated by the estrogen receptor and the AP-1 transcription factor. Mol Endocrinol 2011; 25: 1527–38.
- 47Lee AW, Bomkamp A, Bandera EV, et al. A splicing variant of TERT identified by GWAS interacts with menopausal estrogen therapy in risk of ovarian cancer. Int J Cancer 2016; 139: 2646–54.
- 48Usset JL, Raghavan R, Tyrer JP, et al. Assessment of multifactor gene-environment interactions and Ovarian Cancer risk: candidate genes, obesity, and hormone-related risk factors. Cancer Epidemiol Biomarkers Prev 2016; 25: 780–90.
- 49Dimitrakopoulou VI, Travis RC, Shui IM, et al. Interactions between genome-wide significant genetic variants and circulating concentrations of 25-Hydroxyvitamin D in relation to prostate Cancer risk in the National Cancer Institute BPC3. Am J Epidemiol 2017; 185: 452–64.
- 50McAllister K, Mechanic LE, Amos C, et al. Current challenges and new opportunities for gene-environment interaction studies of complex diseases. Am J Epidemiol 2017; 186: 753–61.
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