ArticleJournal of the National Cancer Institute2023
Lifetime ovulatory years and risk of epithelial ovarian cancer: a multinational pooled analysis.
Open access · greenAbstract read
In one paragraph
Article in Journal of the National Cancer Institute, 2023. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 16 papers.
0numbers the graph read from it
0cells of the map it votes in
16citing papers in PubMed
6.3field-weighted citation impact, top 3% of its field
What it found
Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.
The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.
The trial behind it
Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.
Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.
Who cites it
16 citing papers in PubMed, 23 citations in OpenAlex.
- The cervico-vaginal DNA methylation WID-qEC test: An epigenetic marker associated with ovarian cancer in the absence of endometrial and cervical cancer.International journal of cancer · 2026Article
- Single-nucleus profiling reveals age-associated remodeling opposed by parity in the postmenopausal human ovary.bioRxiv : the preprint server for biology · 2026Article
- Targeting Autophagy in Ovarian Cancer: The Emerging Role of Ginsenosides.Cancer medicine · 2026Review
- Reproductive Shifts and Ovarian Cancer Risk in Women Aged 40 Years or Older.JAMA network open · 2026Article
- Synchronous primary breast invasive carcinoma and breast metastasis from high-grade serous ovarian carcinoma: a case report and literature review.Frontiers in oncology · 2026Article
- Identification of anoikis-related tumor microenvironment characteristics and prognostic signature in ovarian cancer at bulk and single-cell levels.Discover oncology · 2025Article
- Patterns of Associations with Epidemiologic Factors by High-Grade Serous Ovarian Cancer Gene Expression Subtypes.Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology · 2025Article
- Macrophages and neutrophils in ovarian cancer microenvironment.Frontiers in immunology · 2025Review
- Epidermal growth factor receptor ligands enriched in follicular fluid exosomes promote oncogenesis of fallopian tube epithelial cells.Cancer cell international · 2024Article
- Global epidemiology of epithelial ovarian cancer.Nature reviews. Clinical oncology · 2024Review
- Salpingectomy for ectopic pregnancy reduces ovarian cancer risk-a nationwide study.JNCI cancer spectrum · 2024Article
- Biology-driven therapy advances in high-grade serous ovarian cancer.The Journal of clinical investigation · 2024Review
- Transcriptomic Analysis of the Aged Nulliparous Mouse Ovary Suggests a Stress State That Promotes Pro-Inflammatory Lipid Signaling and Epithelial Cell Enrichment.International journal of molecular sciences · 2023Article
- Early-Onset Ovarian Cancer <30 Years: What Do We Know about Its Genetic Predisposition?International journal of molecular sciences · 2023Review
- Primary prevention of ovarian cancer by salpingectomy: that's one small step for a surgeon, one giant leap for patients.Journal of cancer research and clinical oncology · 2023Article
- Estimated Ovulatory Years Prior to Menopause and Postmenopausal Endogenous Hormone Levels.Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology · 2023Article
Corrections and comments
PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.
Authors and funding
63 authors at 20 institutions in 7 countries.
Zhuxuan FuDepartment of Epidemiology, University of Pittsburgh School of Public Health, Pittsburgh, PA, USA.
Maria Mori BrooksDepartment of Epidemiology, University of Pittsburgh School of Public Health, Pittsburgh, PA, USA.
Sarah IrvinDivision of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD, USA.
Susan JordanThe School of Public Health, The University of Queensland, Brisbane, Queensland, Australia.
Katja K H AbenRadboud Institute for Health Sciences, Radboud University Medical Center, Nijmegen, The Netherlands.
Hoda Anton-CulverDepartment of Medicine, Genetic Epidemiology Research Institute, University of California Irvine, Irvine, CA, USA.ORCID 0000-0002-9603-0110
Elisa V BanderaCancer Prevention and Control Program, Rutgers Cancer Institute of New Jersey, New Brunswick, NJ, USA.
Matthias W BeckmannDepartment of Gynecology and Obstetrics, Comprehensive Cancer Center Erlangen-European Metropolitan Region of Nuremberg (EMN), Friedrich-Alexander University Erlangen-Nuremberg, University Hospital Erlangen, Erlangen, Germany.
Andrew BerchuckDivision of Gynecologic Oncology, Department of Obstetrics and Gynecology, Duke University Medical Center, Durham, NC, USA.
Angela Brooks-WilsonCanada's Michael Smith Genome Sciences Centre, BC Cancer, Vancouver, BC, Canada.
Jenny Chang-ClaudeDivision of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany.
Linda S CookEpidemiology, School of Public Health, University of Colorado, Aurora, CO, USA.
Daniel W CramerDepartment of Obstetrics and Gynecology, Obstetrics and Gynecology Epidemiology Center, Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA.
Kara L Cushing-HaugenProgram in Epidemiology, Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
Jennifer A DohertyDepartment of Population Health Sciences, Huntsman Cancer Institute, University of Utah, Salt Lake City, UT, USA.
Arif B EkiciInstitute of Human Genetics, Comprehensive Cancer Center Erlangen-EMN, University Hospital Erlangen, Friedrich-Alexander University Erlangen-Nuremberg (FAU), Erlangen, Germany.
Peter A FaschingDepartment of Gynecology and Obstetrics, Comprehensive Cancer Center Erlangen-European Metropolitan Region of Nuremberg (EMN), Friedrich-Alexander University Erlangen-Nuremberg, University Hospital Erlangen, Erlangen, Germany.
Renée T FortnerDivision of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany.
Simon A GaytherCenter for Bioinformatics and Functional Genomics and the Cedars Sinai Genomics Core, Cedars-Sinai Medical Center, Los Angeles, CA, USA.
Aleksandra Gentry-MaharajMRC Clinical Trials Unit, Institute of Clinical Trials & Methodology, University College London, London, UK.
Graham G GilesCancer Epidemiology Division, Cancer Council Victoria, Melbourne, Victoria, Australia.ORCID 0000-0003-4946-9099
Ellen L GoodeDepartment of Quantitative Health Sciences, Division of Epidemiology, Mayo Clinic, Rochester, MN, USA.
Marc T GoodmanCancer Prevention and Control Program, Cedars-Sinai Cancer, Cedars-Sinai Medical Center, Los Angeles, CA, USA.
Holly R HarrisProgram in Epidemiology, Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
Alexander HeinDepartment of Gynecology and Obstetrics, Comprehensive Cancer Center Erlangen-European Metropolitan Region of Nuremberg (EMN), Friedrich-Alexander University Erlangen-Nuremberg, University Hospital Erlangen, Erlangen, Germany.
Rudolf KaaksDivision of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany.ORCID 0000-0003-3751-3929
Lambertus A KiemeneyRadboud Institute for Health Sciences, Radboud University Medical Center, Nijmegen, The Netherlands.
Martin KöbelDepartment of Pathology and Laboratory Medicine, University of Calgary, Foothills Medical Center, Calgary, AB, Canada.
Joanne KotsopoulosWomen's College Research Institute, Women's College Hospital, University of Toronto, Toronto, ON, Canada.ORCID 0000-0001-9624-4218
Nhu D LeCancer Control Research, BC Cancer, Vancouver, BC, Canada.
Alice W LeeDepartment of Health Science, California State University, Fullerton, Fullerton, CA, USA.
Keitaro MatsuoDivision of Cancer Epidemiology and Prevention, Aichi Cancer Center Research Institute, Nagoya, Japan.ORCID 0000-0003-1761-6314
Valerie McGuireDepartment of Epidemiology and Population Health, Stanford University School of Medicine, Stanford, CA, USA.
John R McLaughlinDalla Lana School of Public Health, University of Toronto, Toronto, ON, Canada.
Usha MenonMRC Clinical Trials Unit, Institute of Clinical Trials & Methodology, University College London, London, UK.ORCID 0000-0003-3708-1732
Roger L MilneCancer Epidemiology Division, Cancer Council Victoria, Melbourne, Victoria, Australia.
Kirsten B MoysichDepartment of Cancer Prevention and Control, Roswell Park Cancer Institute, Buffalo, NY, USA.
Celeste Leigh PearceDepartment of Epidemiology, University of Michigan School of Public Health, Ann Arbor, MI, USA.
Malcolm C PikeDepartment of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, New York, NY, USA.
Bo QinCancer Prevention and Control Program, Rutgers Cancer Institute of New Jersey, New Brunswick, NJ, USA.
Susan J RamusSchool of Clinical Medicine, University of New South Wales Medicine and Health, University of New South Wales Sydney, Sydney, New South Wales, Australia.ORCID 0000-0003-0005-7798
Marjorie J RigganDivision of Gynecologic Oncology, Department of Obstetrics and Gynecology, Duke University Medical Center, Durham, NC, USA.
Joseph H RothsteinDepartment of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
Joellen M SchildkrautDepartment of Epidemiology, Rollins School of Public Health, Emory University, Atlanta, GA, USA.
Weiva SiehDepartment of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, USA.ORCID 0000-0003-0085-1190
Rebecca SutphenEpidemiology Center, College of Medicine, University of South Florida, Tampa, FL, USA.
Kathryn L TerryDepartment of Obstetrics and Gynecology, Obstetrics and Gynecology Epidemiology Center, Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA.
Pamela J ThompsonSamuel Oschin Comprehensive Cancer Institute, Cancer Prevention and Genetics Program, Cedars-Sinai Medical Center, Los Angeles, CA, USA.
Linda TitusMuskie School of Public Policy, Public Health, Portland, ME, USA.
Anne M van AltenaDepartment of Obstetrics and Gynaecology, Radboud University Medical Center, Nijmegen, The Netherlands.ORCID 0000-0003-2598-087X
Emily WhiteDepartment of Epidemiology, University of Washington, Seattle, WA, USA.
Alice S WhittemoreDepartment of Epidemiology and Population Health, Stanford University School of Medicine, Stanford, CA, USA.
Anna H WuDepartment of Population Health and Public Health Sciences, Keck School of Medicine, University of Southern California Norris Comprehensive Cancer Center, Los Angeles, CA, USA.
Wei ZhengDivision of Epidemiology, Department of Medicine, Vanderbilt Epidemiology Center, Vanderbilt-Ingram Cancer Center, Vanderbilt University School of Medicine, Nashville, TN, USA.
Argyrios ZiogasDepartment of Medicine, Genetic Epidemiology Research Institute, University of California Irvine, Irvine, CA, USA.ORCID 0000-0003-4529-3727
Sarah E TaylorDivision of Gynecologic Oncology, Department of Obstetrics, Gynecology and Reproductive Sciences, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.
Lu TangDepartment of Biostatistics, University of Pittsburgh School of Public Health, Pittsburgh, PA, USA.
Thomas SongerDepartment of Epidemiology, University of Pittsburgh School of Public Health, Pittsburgh, PA, USA.
Nicolas WentzensenDivision of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, USA.ORCID 0000-0003-1251-0836
Penelope M WebbThe School of Public Health, The University of Queensland, Brisbane, Queensland, Australia.
AOCS Group
Harvey A RischChronic Disease Epidemiology, Yale School of Public Health, New Haven, CT, USA.ORCID 0000-0001-5337-3941
Francesmary ModugnoDepartment of Epidemiology, University of Pittsburgh School of Public Health, Pittsburgh, PA, USA.ORCID 0000-0003-0637-1534
University of Pittsburgh · USUniversitätsklinikum Erlangen · DECedars-Sinai Medical Center · USRadboud University Nijmegen · NLBrigham and Women's Hospital · USDuke Medical Center · USGerman Cancer Research Center · DEIcahn School of Medicine at Mount Sinai · USMRC Clinical Trials Unit at UCL · GBNational Cancer Institute · USRutgers, The State University of New Jersey · USStanford University · USThe University of Melbourne · AUThe University of Queensland · AUUniversity of California, Irvine · USUniversity of Southern California · USUniversity of Toronto · CAUniversity of Washington · USAichi Cancer Center · JPCalifornia State University, Fullerton · US
Funding
X-RAY CRYSTALLOGRAPHYP30CA008748 · NCI · SLOAN-KETTERING INSTITUTE FOR CANCER RES · PI Hongbiao Carl Lekaye · 1985 to 2026
$347.4MUSC/NORRIS COMPREHENSIVE CANCER CENTER (CORE) SUPPORTP30CA014089 · NCI · UNIVERSITY OF SOUTHERN CALIFORNIA · PI MYLES G COCKBURN · 1985 to 2026
$181.4MWomen's Cancer ProgramP30CA015083 · NCI · MAYO CLINIC ROCHESTER · PI AKHILESH PANDEY · 1985 to 2026
$151.3MHormone-Related CancersZIACP010126 · NCI · DIVISION OF CANCER EPIDEMIOLOGY AND GENETICS · PI GIERACH, GRETCHEN · 2009 to 2025
$103.5MUse of microfluidic tumor cultures to enable clinical trials of therapies for ovarian cancerP50CA136393 · NCI · MAYO CLINIC ROCHESTER · PI ELLEN L. GOODE · 2009 to 2026
$37.0MUSC CANCER EPIDEMIOLOGY &BIOSTATISTICS UNITP01CA017054 · NCI · UNIVERSITY OF SOUTHERN CALIFORNIA · PI HENDERSON, BRIAN E · 1985 to 2009
$18.2MRelating Molecular Subgroups of Endometriosis-Associated Ovarian Cancers to Survival and RiskR01CA248288 · NCI · MAYO CLINIC ROCHESTER · PI Stacey J Winham · 2021 to 2026
$4.8MCOLLABORATIVE STUDY OF OVARIAN CANCER IN TWO RISK GROUPSR01CA058598 · NCI · UNIVERSITY OF HAWAII AT MANOA · PI GOODMAN, MARC T · 1993 to 2012
$4.6MEpidemiology of Ovarian Cancer:New HypothesesR01CA087538 · NCI · FRED HUTCHINSON CANCER RESEARCH CENTER · PI ROSSING, MARY ANNE · 2002 to 2006
$3.5MSteroid Hormone Genes and Ovarian Cancer RiskR01CA112523 · NCI · FRED HUTCHINSON CANCER RESEARCH CENTER · PI ROSSING, MARY ANNE · 2006 to 2010
$3.3MSURVEILLANCE EPIDEMIOLOGY &END RESULTS PROGRAMN01PC067010 · PC · UNIVERSITY OF SOUTHERN CALIFORNIA · PI ROSS, RONALD K · 1996 to 2000
$2.4MCASE CONTROL STUDY OF OVARIAN CANCER HORMONAL ETIOLOGYR01CA074850 · NCI · YALE UNIVERSITY · PI RISCH, HARVEY A · 1997 to 2002
$965kMedical Research Council MC_UU_00004/01NCI NIH HHS K05 CA154337NCI NIH HHS N01 CN025403NCI NIH HHS N01 PC067010NCI NIH HHS P01 CA017054NCI NIH HHS P30 CA008748NCI NIH HHS P30 CA014089NCI NIH HHS P30 CA015083NCI NIH HHS P50 CA136393NCI NIH HHS R01 CA058598NCI NIH HHS R01 CA063678NCI NIH HHS R01 CA074850NCI NIH HHS R01 CA080742NCI NIH HHS R01 CA087538NCI NIH HHS R01 CA112523NCI NIH HHS R01 CA248288NCI NIH HHS R03 CA113148NCI NIH HHS R03 CA115195NIH HHS K05-CA154337NIH HHS P01CA17054NIH HHS R01-CA112523NIH HHS R01-CA58598
Abstract
backgroundThe role of ovulation in epithelial ovarian cancer (EOC) is supported by the consistent protective effects of parity and oral contraceptive use. Whether these factors protect through anovulation alone remains unclear. We explored the association between lifetime ovulatory years (LOY) and EOC.
methodsLOY was calculated using 12 algorithms. Odds ratios (ORs) and 95% confidence intervals (CIs) estimated the association between LOY or LOY components and EOC among 26 204 control participants and 21 267 case patients from 25 studies. To assess whether LOY components act through ovulation suppression alone, we compared beta coefficients obtained from regression models with expected estimates assuming 1 year of ovulation suppression has the same effect regardless of source.
resultsLOY was associated with increased EOC risk (OR per year increase = 1.014, 95% CI = 1.009 to 1.020 to OR per year increase = 1.044, 95% CI = 1.041 to 1.048). Individual LOY components, except age at menarche, also associated with EOC. The estimated model coefficient for oral contraceptive use and pregnancies were 4.45 times and 12- to 15-fold greater than expected, respectively. LOY was associated with high-grade serous, low-grade serous, endometrioid, and clear cell histotypes (ORs per year increase = 1.054, 1.040, 1.065, and 1.098, respectively) but not mucinous tumors. Estimated coefficients of LOY components were close to expected estimates for high-grade serous but larger than expected for low-grade serous, endometrioid, and clear cell histotypes.
conclusionsLOY is positively associated with nonmucinous EOC. Differences between estimated and expected model coefficients for LOY components suggest factors beyond ovulation underlie the associations between LOY components and EOC in general and for non-HGSOC.
Indexed as
Ovarian NeoplasmsCarcinoma, Ovarian EpithelialCase-Control StudiesContraceptives, OralFemaleHumansParityPregnancyRisk FactorsContraceptives, Oral
Identifiers
What OpenQuestion holds
Textmetadata
LicenceCC BY
Read underepoch 390
Registered trials
None linked
Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.