Cancer Causes & Control

, Volume 29, Issue 11, pp 1081–1091 | Cite as

Benign gynecologic conditions are associated with ovarian cancer risk in African-American women: a case–control study

  • Hyo K. ParkEmail author
  • Joellen M. Schildkraut
  • Anthony J. Alberg
  • Elisa V. Bandera
  • Jill S. Barnholtz-Sloan
  • Melissa Bondy
  • Sydnee Crankshaw
  • Ellen Funkhouser
  • Patricia G. Moorman
  • Edward S. Peters
  • Paul Terry
  • Frances Wang
  • Julie J. Ruterbusch
  • Ann G. Schwartz
  • Michele L. Cote
Original paper



The association between common benign gynecologic conditions and ovarian cancer remains under-studied in African Americans. Therefore, we examine the association between self-reported history of benign gynecologic conditions and epithelial ovarian cancer risk in African-American women.


Data from a large population-based, multi-center case–control study of epithelial ovarian cancer in African-American women were analyzed to estimate the association between self-reported history of endometriosis, pelvic inflammatory disease (PID), fibroid, and ovarian cyst with epithelial ovarian cancer. Logistic regression was used to calculate odds ratios (OR) and 95% confidence intervals (CI) for the associations between individual and composite gynecologic conditions and ovarian cancer.


600 cases and 752 controls enrolled in the African American Cancer Epidemiology Study between 1 December 2010 and 31 December 2015 comprised the study population. After adjusting for potential confounders, a history of endometriosis was associated with ovarian cancer (OR 1.78; 95% CI 1.09–2.90). A non-significant association of similar magnitude was observed with PID (OR 1.33; 95% CI 0.82–2.16), while no association was observed in women with a history of fibroid or ovarian cyst. A positive trend was observed for an increasing number of reported gynecologic conditions (p = 0.006) with consistency across histologic subtypes and among both oral contraceptive users and non-users.


A self-reported history of endometriosis among African-American women was associated with increased risk of ovarian cancer. Having multiple benign gynecologic conditions also increased ovarian cancer risk.


Ovarian cancer African-American Endometriosis Pelvic inflammatory disease (PID) Ovarian cyst Uterine fibroid African-American Cancer Epidemiology Study (AACES) 



Pelvic inflammatory disease


Oral contraceptive


African-American Cancer Epidemiology Study


Surveillance, Epidemiology, and End Results


American Joint Committee on Cancer


Odds ratio


Confidence interval


Body mass index



We would like to acknowledge the AACES interviewers, Christine Bard, LaTonda Briggs, Whitney Franz (North Carolina) and Robin Gold (Detroit). We also acknowledge the individuals responsible for facilitating case ascertainment across the ten sites including: Jennifer Burczyk-Brown (Alabama); Rana Bayakly, Vicki Bennett and Judy Andrews (Georgia); the Louisiana Tumor Registry; Lisa Paddock and Manisha Narang (New Jersey); Diana Slone, Yingli Wolinsky, Steven Waggoner, Anne Heugel, Nancy Fusco, Kelly Ferguson, Peter Rose, Deb Strater, Taryn Ferber, Donna White, Lynn Borzi, Eric Jenison, Nairmeen Haller, Debbie Thomas, Vivian von Gruenigen, Michele McCarroll, Joyce Neading, John Geisler, Stephanie Smiddy, David Cohn, Michele Vaughan, Luis Vaccarello, Elayna Freese, James Pavelka, Pam Plummer, William Nahhas, Ellen Cato, John Moroney, Mark Wysong, Tonia Combs, Marci Bowling, Brandon Fletcher, (Ohio); Susan Bolick, Donna Acosta, Catherine Flanagan (South Carolina); Martin Whiteside (Tennessee) and Georgina Armstrong and the Texas Registry, Cancer Epidemiology and Surveillance Branch, Department of State Health Services.

Author contributions

JS, HP, and MC contributed to the conception and design of the study, analysis and interpretation of data, and drafting of the manuscript. JS, AA, JBS, EF, PT, JJR, and AS contributed to the interpretation of the data and critical revision of the manuscript. All authors reviewed and gave approval of the final version to be published.


This study was supported by the National Cancer Institute (R01CA142081). Additional support was provided by the Metropolitan Detroit Cancer Surveillance System with funding from the National Cancer Institute, National Institute of Health, and the Department of Health and Human Services (Contract HHSN261201000028C), and the Epidemiology Research Core, supported in part by the National Cancer Institute (P30CA22453) to the Karmanos Cancer Institute, Wayne State University School of Medicine. The New Jersey State Cancer Registry, Cancer Epidemiology Services, New Jersey Department of Health, is funded by the Surveillance, Epidemiology and End Results (SEER) Program of the National Cancer Institute under contract HHSN261201300021I, the National Program of Cancer Registries (NPCR), Centers for Disease Control and Prevention under grant 5U58DP003931-02 as well as the State of New Jersey and the Rutgers Cancer Institute of New Jersey.

Compliance with ethical standards

Ethics approval and consent to participate

The study protocol and questionnaire were approved by the Institutional Review Boards at Duke University Medical Center, Baylor College of Medicine, Case Western Reserve University School of Medicine, Louisiana State University, Robert Wood Johnson Medical School/Rutgers Cancer Institute, Wayne State University, the University of Alabama-Birmingham, the Medical University of South Carolina, and the University of Tennessee-Knoxville. Additionally, the protocol was approved by central cancer registries in the states of Alabama, Georgia, North Carolina, South Carolina, Tennessee, and Texas, SEER registries in New Jersey, Louisiana, and the Detroit metropolitan area, and 9 individual hospital systems in Ohio. All study participants completed informed consent prior to enrollment.

Availability of data and materials

The dataset used and analyzed in this study is available after review from the AACES study investigators and with proper IRB approvals.

Conflict of interest

The authors declare that they have no competing interests.

Supplementary material

10552_2018_1082_MOESM1_ESM.docx (22 kb)
Supplementary material 1 (DOCX 22 KB)


  1. 1.
    Pearce CL, Templeman C, Rossing MA, Lee A, Near AM, Webb PM et al (2012) Association between endometriosis and risk of histological subtypes of ovarian cancer: a pooled analysis of case–control studies. Lancet Oncol 13:385–394CrossRefGoogle Scholar
  2. 2.
    Somigliana E, Vigano P, Parazzini F, Stoppelli S, Giambattista E, Vercellini P (2006) Association between endometriosis and cancer: a comprehensive review and a critical analysis of clinical and epidemiological evidence. Gynecol Oncol 101:331–341CrossRefGoogle Scholar
  3. 3.
    Brinton LA, Sakoda LC, Sherman ME, Frederiksen K, Kjaer SK, Graubard BI et al (2005) Relationship of benign gynecologic diseases to subsequent risk of ovarian and uterine tumors. Cancer Epidemiol Biomark Prev 14:2929–2935CrossRefGoogle Scholar
  4. 4.
    Merritt MA, Green AC, Nagle CM, Webb PM (2008) Talcum powder, chronic pelvic inflammation and NSAIDs in relation to risk of epithelial ovarian cancer. Int J Cancer 122:170–176CrossRefGoogle Scholar
  5. 5.
    Ness RB (2003) Endometriosis and ovarian cancer: thoughts on shared pathophysiology. Am J Obstet Gynecol 189:280–294CrossRefGoogle Scholar
  6. 6.
    Prefumo F, Todeschini F, Fulcheri E, Venturini PL (2002) Epithelial abnormalities in cystic ovarian endometriosis. Gynecol Oncol 84:280–284CrossRefGoogle Scholar
  7. 7.
    Lee AW, Templeman C, Stram DA, Beesley J, Tyrer J, Berchuck A et al (2015) Evidence of a genetic link between endometriosis and ovarian cancer. Fertil Steril 105:35–43CrossRefGoogle Scholar
  8. 8.
    Wiegand KC, Shah SP, Al-Agha OM, Zhao Y, Tse K, Zeng T et al (2010) ARID1A mutations in endometriosis-associated ovarian carcinomas. N Engl J Med 363:1532–1543CrossRefGoogle Scholar
  9. 9.
    Risch HA, Howe GR (1995) Pelvic inflammatory disease and risk of epithelial ovarian cancer. Cancer Epidemiol Biomark Prev 4:447–451Google Scholar
  10. 10.
    Lin HW, Tu YY, Lin SY, Su WJ, Lin WL, Lin WZ et al (2011) Risk of ovarian cancer in women with pelvic inflammatory disease: a population-based study. Lancet Oncol 12:900–904CrossRefGoogle Scholar
  11. 11.
    McAlpine JN, Lisonkova S, Joseph KS, McComb PF (2014) Pelvic inflammation and the pathogenesis of ovarian cancer: a cohort study. Int J Gynecol Cancer 24:1406–1413CrossRefGoogle Scholar
  12. 12.
    Rossing MA, Cushing-Haugen KL, Wicklung KG, Doherty JA, Weiss NS (2008) Risk of epithelial ovarian cancer in relation to benign ovarian conditions and ovarian surgery. Cancer Causes Control 19:1357–1364CrossRefGoogle Scholar
  13. 13.
    Parazzini F, Vecchia CL, Negri E, Moroni S, dal Pino D, Fedele L (1996) Pelvic inflammatory disease and risk of ovarian cancer. Cancer Epidemiol Biomark Prev 5:667–669Google Scholar
  14. 14.
    Rasmussen CB, Faber MT, Jensen A, Hogdall E, Hogdall C, Blaakaer J et al (2013) Pelvic inflammatory disease and risk of invasive ovarian cancer and ovarian borderline tumors. Cancer Causes Control 24:1489–1494CrossRefGoogle Scholar
  15. 15.
    Hartge P, Hayes R, Reding D, Sherman ME, Prorok P, Schiffman M et al (2000) Complex ovarian cysts in postmenopausal women are not associated with ovarian cancer risk factors: preliminary data from the prostate, lung, colon, and ovarian cancer screening trial. Am J Obstet Gynecol 183:1232–1237CrossRefGoogle Scholar
  16. 16.
    Valentin L, Ameye L, Franchi D, Guerriero S, Jurkovic D, Savelli L et al (2013) Risk of malignancy in unilocular cysts: a study of 1148 adnexal masses classified as unilovular cysts at transvaginal ultrasound and review of the literature. Ultrasound Obstet Gynecol 41:80–89CrossRefGoogle Scholar
  17. 17.
    Jacoby VL, Fujimoto VY, Giudice LC, Kuppermann M, Washington AE (2010) Racial and ethnic disparities in benign gynecologic conditions and associated surgeries. Am J Obstet Gynecol 202:514–521CrossRefGoogle Scholar
  18. 18.
    Wise LA, Palmer JR, Stewart EA, Rosenberg L (2005) Age-specific incidence rates for self-reported uterine leiomyomata in the black women’s health study. Obstet Gynecol 105:563–568CrossRefGoogle Scholar
  19. 19.
    Hankinson SE, Hunter DJ, Colditz GA, Willett WC, Stampfer MJ, Rosner B et al (1993) Tubal ligation, hysterectomy, and risk of ovarian cancer. A prospective study. JAMA 270:2813–2818CrossRefGoogle Scholar
  20. 20.
    Rice MS, Hankinson SE, Tworoger SS (2014) Tubal ligation, hysterectomy, unilateral oophorectomy, and risk of ovarian cancer in the Nurses’ Health Studies. Fertil Steril 102:192–8CrossRefGoogle Scholar
  21. 21.
    Rice MS, Murphy MA, Vitonis AF, Cramer DW, Titus LJ, Tworoger SS et al (2013) Tubal ligation, hysterectomy and epithelial ovarian cancer in the New England Case–control Study. Int J Cancer 133:2415–2421CrossRefGoogle Scholar
  22. 22.
    Schildkraut JM, Alberg AJ, Bandera EV, Barnholtz-Sloan J, Bondy M, Cote ML et al (2014) A multi-center population-based case–control study of ovarian cancer in African-American women: the African American Cancer Epidemiology Study (AACES). BMC Cancer 14:688CrossRefGoogle Scholar
  23. 23.
    Rasmussen CB, Kjaer SK, Albieri V, Bandera EV, Doherty JA, Hogdall E et al (2017) Pelvic inflammatory disease and the risk of ovarian cancer and borderline ovarian tumors: a pooled analysis of 13 case–control studies. Am J Epidmiol 185:8–20CrossRefGoogle Scholar
  24. 24.
    Terry KL, Karageorgi S, Shvetsov YB, Merritt MA, Lurie G, Thompson PJ et al (2013) Genital powder use and risk of ovarian cancer: a pooled analysis of 8,525 cases and 9,859 controls. Cancer Prev Res 6:811–821CrossRefGoogle Scholar
  25. 25.
    Ness RB, Cramer DW, Goodman MT, Kjaer SK, Mallin K, Mosgaard BJ et al (2002) Infertility, fertility drugs, and ovarian cancer: a pooled analysis of case–control studies. Am J Epidemiol 155:217–224CrossRefGoogle Scholar
  26. 26.
    Lee WL, Chang WH, Wang KC, Guo CY, Chou YJ, Huang N et al (2015) The risk of epithelial ovarian cancer of women with endometriosis may be varied greatly if diagnostic criteria are different. Medicine 94:e1633CrossRefGoogle Scholar
  27. 27.
    Schildkraut JM, Calingaert B, Marchbanks PA, Moorman PG, Rodriguez GC (2002) Impact of progestin and estrogen potency in oral contraceptives on ovarian cancer risk. J Natl Cancer Inst 94:32–38CrossRefGoogle Scholar
  28. 28.
    Anderson GL, Judd HL, Kaunitz AM, Barad DH, Beresford SA, Pettinger M, Liu J et al (2003) Effects of estrogen plus progestin on gynecologic cancers and associated diagnostic procedures: the Women’s Health Initiative randomized trial. JAMA 290:1739–1748CrossRefGoogle Scholar
  29. 29.
    Schildkraut JM, Abbot SE, Alberg AJ, Bandera EV, Barnholtz-Sloan JS, Bondy ML et al (2016) Association between body powder use and ovarian cancer: the African American Cancer Epidemiology Study (AACES). Cancer Epidemiol Biomark Prev 25:1411–1417CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Hyo K. Park
    • 1
    Email author
  • Joellen M. Schildkraut
    • 2
  • Anthony J. Alberg
    • 3
  • Elisa V. Bandera
    • 4
  • Jill S. Barnholtz-Sloan
    • 5
  • Melissa Bondy
    • 6
  • Sydnee Crankshaw
    • 7
  • Ellen Funkhouser
    • 8
  • Patricia G. Moorman
    • 7
  • Edward S. Peters
    • 9
  • Paul Terry
    • 10
  • Frances Wang
    • 7
  • Julie J. Ruterbusch
    • 1
  • Ann G. Schwartz
    • 1
  • Michele L. Cote
    • 1
  1. 1.Department of Oncology and the Karmanos Cancer Institute, Population Studies and Disparities Research ProgramWayne State University School of MedicineDetroitUSA
  2. 2.Department of Public Health SciencesUniversity of VirginiaCharlottesvilleUSA
  3. 3.Hollings Cancer Center and Department of Public Health SciencesMedical University of South CarolinaCharlestonUSA
  4. 4.Department of Population ScienceRutgers Cancer Institute of New JerseyNew BrunswickUSA
  5. 5.Case Comprehensive Cancer CenterCase Western Reserve University School of MedicineClevelandUSA
  6. 6.Cancer Prevention and Population Sciences ProgramBaylor College of MedicineHoustonUSA
  7. 7.Department of Community and Family Medicine, Cancer Control and Population SciencesDuke University School of MedicineDurhamUSA
  8. 8.Division of Preventive MedicineUniversity of Alabama at BirminghamBirminghamUSA
  9. 9.Epidemiology ProgramLouisiana State University Health Sciences Center School of Public HealthNew OrleansUSA
  10. 10.Department of MedicineUniversity of Tennessee Graduate School of MedicineKnoxvilleUSA

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