Cancer Causes & Control

, Volume 24, Issue 4, pp 665–674 | Cite as

Epidemiologic features of borderline ovarian tumors in California: a population-based study

  • Cyllene R. Morris
  • Lihua Liu
  • Anne O. Rodriguez
  • Rosemary D. Cress
  • Kurt Snipes
Original Paper

Abstract

Purpose

Borderline ovarian tumors (BOT) became no longer reportable in 2001, and few registries still collect information on these still poorly understood tumors. This study’s objective was to describe epidemiologic features, trends, and survival of BOTs compared with those of low-grade (LG) and high-grade (HG) epithelial ovarian cancer (EOC) in the large and diverse population of California.

Methods

Data from the California Cancer Registry were used to examine demographic and tumor characteristics among women diagnosed with BOT (n = 9,786), LG-EOC (n = 3,656), and HG-EOC (n = 40,611) from 1988 to 2010. Annual percent changes in BOT and LG-EOC incidence rates were estimated using Joinpoint regression; 5-year relative survival was calculated for both BOTs and LG-EOCs by age, race/ethnicity, and histology.

Results

Age-adjusted incidence rates of BOT in 2009 were 3.1, 2.3, 2.2, and 1.4 per 100,000 among whites, Latinas, African Americans, and Asian/Pacific Islanders, respectively. Incidence rates for LG-EOC decreased by 2.2 % per year; rates for BOT increased by 7.3 % per year until 1993, remained unchanged until 2006, and seemed to decline thereafter. Compared with LG-EOCs, BOTs were diagnosed in higher frequency among Latinas, at younger age, and were more likely to affect only one ovary. Overall, 5-year relative survival for BOT was 98.9 %; among women diagnosed with stage IV BOT, survival was 77.1 %.

Conclusions

In this study, differences between BOTs and LG-EOCs were marked but varied substantially by histologic subtype and were far less dramatic than differences between BOTs and HG-EOCs. Findings underscore the importance of understanding these enigmatic tumors.

Keywords

Epithelial ovarian cancer Borderline ovarian tumors Incidence rates Relative survival Race/ethnicity 

References

  1. 1.
    Eltabbakh GH, Natarajan N, Piver MS, Mettlin CJ (1999) Epidemiologic differences between women with borderline ovarian tumors and women with epithelial ovarian cancer. Gynecol Oncol 74(1):103–107PubMedCrossRefGoogle Scholar
  2. 2.
    Frederiksen K, Hogdall EV, Glud E, Christensen L, Hogdall CK, Blaakaer J et al (2006) Association of reproductive factors, oral contraceptive use and selected lifestyle factors with the risk of ovarian borderline tumors: a Danish case-control study. Cancer Causes Control 17(6):821–829PubMedCrossRefGoogle Scholar
  3. 3.
    Kumle M, Weiderpass E, Braaten T, Adami HO, Lund E (2004) Risk for invasive and borderline epithelial ovarian neoplasias following use of hormonal contraceptives: the Norwegian-Swedish Women’s Lifestyle and Health Cohort Study. Br J Cancer 90(7):1386–1391PubMedCrossRefGoogle Scholar
  4. 4.
    Modugno F, Ness RB, Wheeler JE (2001) Reproductive risk factors for epithelial ovarian cancer according to histologic type and invasiveness. Ann Epidemiol 11(8):568–574PubMedCrossRefGoogle Scholar
  5. 5.
    Harris R, Whittemore AS, Itnyre J (1992) Characteristics relating to ovarian cancer risk: collaborative analysis of 12 US case-control studies. III. Epithelial tumors of low malignant potential in white women. Collaborative Ovarian Cancer Group. Am J Epidemiol 136(10):1204–1211PubMedGoogle Scholar
  6. 6.
    Riman T, Dickman PW, Nilsson S, Correia N, Nordlinder H, Magnusson CM et al (2001) Risk factors for epithelial borderline ovarian tumors: results of a Swedish case-control study. Gynecol Oncol 83(3):575–585PubMedCrossRefGoogle Scholar
  7. 7.
    Jordan SJ, Green AC, Whiteman DC, Webb PM (2007) Risk factors for benign, borderline and invasive mucinous ovarian tumors: epidemiological evidence of a neoplastic continuum? Gynecol Oncol 107(2):223–230PubMedCrossRefGoogle Scholar
  8. 8.
    Gotlieb WH, Chetrit A, Menczer J, Hirsh-Yechezkel G, Lubin F, Friedman E et al (2005) Demographic and genetic characteristics of patients with borderline ovarian tumors as compared to early stage invasive ovarian cancer. Gynecol Oncol 97(3):780–783PubMedCrossRefGoogle Scholar
  9. 9.
    Gotlieb WH, Friedman E, Bar-Sade RB, Kruglikova A, Hirsh-Yechezkel G, Modan B et al (1998) Rates of Jewish ancestral mutations in BRCA1 and BRCA2 in borderline ovarian tumors. J Natl Cancer Inst 90(13):995–1000PubMedCrossRefGoogle Scholar
  10. 10.
    Lu KH, Cramer DW, Muto MG, Li EY, Niloff J, Mok SC (1999) A population-based study of BRCA1 and BRCA2 mutations in Jewish women with epithelial ovarian cancer. Obstet Gynecol 93(1):34–37PubMedCrossRefGoogle Scholar
  11. 11.
    Auranen A, Grenman S, Makinen J, Pukkala E, Sankila R, Salmi T (1996) Borderline ovarian tumors in Finland: epidemiology and familial occurrence. Am J Epidemiol 144(6):548–553PubMedCrossRefGoogle Scholar
  12. 12.
    Bjorge T, Engeland A, Hansen S, Trope CG (1997) Trends in the incidence of ovarian cancer and borderline tumours in Norway, 1954–1993. Int J Cancer 71(5):780–786PubMedCrossRefGoogle Scholar
  13. 13.
    Hannibal CG, Huusom LD, Kjaerbye-Thygesen A, Tabor A, Kjaer SK (2011) Trends in incidence of borderline ovarian tumors in Denmark 1978–2006. Acta Obstet Gynecol Scand 90(4):305–312PubMedCrossRefGoogle Scholar
  14. 14.
    Skirnisdottir I, Garmo H, Wilander E, Holmberg L (2008) Borderline ovarian tumors in Sweden 1960–2005: trends in incidence and age at diagnosis compared to ovarian cancer. Int J Cancer 123(8):1897–1901PubMedCrossRefGoogle Scholar
  15. 15.
    Sherman ME, Berman J, Birrer MJ, Cho KR, Ellenson LH, Gorstein F et al (2004) Current challenges and opportunities for research on borderline ovarian tumors. Hum Pathol 35(8):961–970PubMedCrossRefGoogle Scholar
  16. 16.
    Fritz A, Percy C (2000) Introducing ICD-O-3: impact of the new edition. J Registry Manag 27(4):125–131Google Scholar
  17. 17.
    Fritz APC, Jack A, Shanmugaratnam K, Sobin L, Parkin DM, Whelan S (eds) (2000) ICD-O: international classification of diseases for oncology, 3rd edn. World Health Organization, GenevaGoogle Scholar
  18. 18.
    NAACCR Latino Research Work Group (2005) NAACCR guideline for enhancing hispanic/latino identification: revised NAACCR hispanic/latino identification algorithm [NHIA v2]. North American Association of Central Cancer Registries, Springfield, ILGoogle Scholar
  19. 19.
    Kim HJ, Fay MP, Feuer EJ, Midthune DN (2000) Permutation tests for joinpoint regression with applications to cancer rates. Stat Med 19(3):335–351PubMedCrossRefGoogle Scholar
  20. 20.
    Tung KH, Goodman MT, Wu AH, McDuffie K, Wilkens LR, Kolonel LN et al (2003) Reproductive factors and epithelial ovarian cancer risk by histologic type: a multiethnic case-control study. Am J Epidemiol 158(7):629–638PubMedCrossRefGoogle Scholar
  21. 21.
    Akeson M, Zetterqvist BM, Dahllof K, Jakobsen AM, Brannstrom M, Horvath G (2008) Population-based cohort follow-up study of all patients operated for borderline ovarian tumor in western Sweden during an 11-year period. Int J Gynecol Cancer 18(3):453–459PubMedCrossRefGoogle Scholar
  22. 22.
    Wong HF, Low JJ, Chua Y, Busmanis I, Tay EH, Ho TH (2007) Ovarian tumors of borderline malignancy: a review of 247 patients from 1991 to 2004. Int J Gynecol Cancer 17(2):342–349PubMedCrossRefGoogle Scholar
  23. 23.
    Chao TM, Yen MS, Chao KC, Ng HT (1996) Epithelial ovarian tumors of borderline malignancy. Zhonghua Yi Xue Za Zhi (Taipei) 58(2):97–102Google Scholar
  24. 24.
    Mink PJ, Sherman ME, Devesa SS (2002) Incidence patterns of invasive and borderline ovarian tumors among white women and black women in the United States. Results from the SEER Program, 1978–1998. Cancer 95(11):2380–2389PubMedCrossRefGoogle Scholar
  25. 25.
    Taylor TH, Bringman D, Anton-Culver H (2006) Malignancies following in situ cervical cancer in hispanic americans and non-hispanic whites. Gynecol Oncol 103(3):1012–1016PubMedCrossRefGoogle Scholar
  26. 26.
    American Cancer Society, California Department of Public Health, California Cancer Registry. California Cancer facts and Figures (2011). American Cancer Society, California Division, Oakland, CAGoogle Scholar
  27. 27.
    Morris CR, Rodriguez AO, Epstein J, Cress RD (2008) Declining trends of epithelial ovarian cancer in California. Gynecol Oncol 108(1):207–213PubMedCrossRefGoogle Scholar
  28. 28.
    Harlow BL, Weiss NS, Lofton S (1987) Epidemiology of borderline ovarian tumors. J Natl Cancer Inst 78(1):71–74PubMedGoogle Scholar
  29. 29.
    Yahata T, Banzai C, Tanaka K (2012) Histology-specific long-term trends in the incidence of ovarian cancer and borderline tumor in Japanese females: a population-based study from 1983 to 2007 in Niigata. J Obstet Gynaecol Res 38(4):645–650PubMedCrossRefGoogle Scholar
  30. 30.
    Menczer J, Sadetzki S, Murad H, Barda G, Andreev H, Barchana M (1999) Childhood and adolescent ovarian malignant tumors in Israel. A nationwide study. Acta Obstet Gynecol Scand 78(9):813–817PubMedCrossRefGoogle Scholar
  31. 31.
    Silverberg SG, Bell DA, Kurman RJ, Seidman JD, Prat J, Ronnett BM et al (2004) Borderline ovarian tumors: key points and workshop summary. Hum Pathol 35(8):910–917PubMedCrossRefGoogle Scholar
  32. 32.
    Sherman ME, Mink PJ, Curtis R, Cote TR, Brooks S, Hartge P et al (2004) Survival among women with borderline ovarian tumors and ovarian carcinoma: a population-based analysis. Cancer 100(5):1045–1052PubMedCrossRefGoogle Scholar
  33. 33.
    Benito V, Lubrano A, Arencibia O, Medina N, Alvarez Eva E, Andujar M, et al (2010) Serous and mucinous borderline ovarian tumors: are there real differences between these two entities? Eur J Obstet Gynecol Reprod Biol 153(2):188–192Google Scholar
  34. 34.
    McCluggage WG (2010) The pathology of and controversial aspects of ovarian borderline tumours. Curr Opin Oncol 22(5):462–72Google Scholar
  35. 35.
    Lenhard MS, Mitterer S, Kumper C, Stieber P, Mayr D, Ditsch N et al (2009) Long-term follow-up after ovarian borderline tumor: relapse and survival in a large patient cohort. Eur J Obstet Gynecol Reprod Biol 145(2):189–194PubMedCrossRefGoogle Scholar
  36. 36.
    Morris CR, Sands MT, Smith LH (2010) Ovarian cancer: predictors of early-stage diagnosis. Cancer Causes Control 21(8):1203–1211PubMedCrossRefGoogle Scholar
  37. 37.
    Gilks CB, Ionescu DN, Kalloger SE, Kobel M, Irving J, Clarke B et al (2008) Tumor cell type can be reproducibly diagnosed and is of independent prognostic significance in patients with maximally debulked ovarian carcinoma. Hum Pathol 39(8):1239–1251PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Cyllene R. Morris
    • 1
  • Lihua Liu
    • 2
  • Anne O. Rodriguez
    • 3
  • Rosemary D. Cress
    • 4
    • 5
  • Kurt Snipes
    • 6
  1. 1.California Cancer Registry, Institute for Population Health ImprovementUniversity of California Davis Health SystemSacramentoUSA
  2. 2.Los Angeles Cancer Surveillance Program, Keck School of MedicineUniversity of Southern CaliforniaLos AngelesUSA
  3. 3.Division of Gynecologic OncologyUniversity of California Davis Medical CenterSacramentoUSA
  4. 4.Department of Public Health Sciences, School of MedicineUniversity of CaliforniaDavisUSA
  5. 5.Cancer Registry of Greater CaliforniaPublic Health InstituteSacramentoUSA
  6. 6.Chronic Diseases Surveillance and Research BranchCalifornia Department of Public HealthSacramentoUSA

Personalised recommendations