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Effect of Endometriosis on the Prognosis of Ovarian Clear Cell Carcinoma: A Two-Center Cohort Study and Meta-analysis

  • Gynecologic Oncology
  • Published:
Annals of Surgical Oncology Aims and scope Submit manuscript

Abstract

Background

Whether endometriosis affects the prognosis of ovarian clear cell carcinoma (OCCC) remains controversial despite the relationship between OCCC and endometriosis. A two-center cohort study and meta-analysis were performed to investigate the effect of endometriosis on the prognosis of OCCC.

Methods

The study reviewed the clinicopathologic data of 109 patients with OCCC arising (n = 47) or not arising (n = 62) in endometriosis between 1997 and 2012 at two tertiary medical centers. Tumor response and survival were compared between the two groups. For further evaluation, PubMed, EmBase, and the Cochrane Library were searched, and a meta-analysis was conducted using 10 cohort studies published from March 1996 to May 2014, including the current cohort study.

Results

Complete response did not differ between the patients with OCCC arising in endometriosis and those without endometriosis (77.5 vs. 87.3 %; P = 0.444). Early-stage disease and optimal debulking surgery were the only independent factors that reduced the risk of noncomplete response (adjusted odds ratios 0.203 and 0.038; 95 % confidence intervals [CIs] 0.045–0.920 and 0.006–0.226, respectively). Progression-free survival (PFS) and overall survival (OS) did not differ between the two groups. Early-stage disease and optimal debulking surgery were the only favorable factors that improved PFS (adjusted hazard ratios [HRs] 0.216 and 0.332; 95 % CIs 0.099–0.469 and 0.150–0.732, respectively) and OS (adjusted HRs 0.099 and 0.339; 95 % CIs 0.039–0.252 and 0.141–0.815, respectively). Furthermore, crude and subgroup meta-analyses showed no effect of endometriosis on PFS or OS in OCCC patients.

Conclusion

Endometriosis may not affect the tumor response or the prognosis of OCCC patients.

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References

  1. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin. 2014;64:9–29.

    Article  PubMed  Google Scholar 

  2. Reade CJ, Riva JJ, Busse JW, et al. Risks and benefits of screening asymptomatic women for ovarian cancer: a systematic review and meta-analysis. Gynecol Oncol. 2013;130:674–81.

    Article  PubMed  Google Scholar 

  3. Suh DH, Kim JW, Kang S, et al. Major clinical research advances in gynecologic cancer in 2013. J Gynecol Oncol. 2014;25:236–48.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  4. Kang HJ, Moon HS, Chung HW. The expression of FAS-associated factor a and heat shock protein 70 in ovarian cancer. Obstet Gynecol Sci. 2014;57:281–90.

    Article  PubMed Central  PubMed  Google Scholar 

  5. Heintz AP, Odicino F, Maisonneuve P, et al. Carcinoma of the ovary. FIGO 26th Annual Report on the Results of Treatment in Gynecologic Cancer. Int J Gynaecol Obstet. 2006;95(Suppl1):S161–92.

    Article  PubMed  Google Scholar 

  6. Kim HS, Kim TH, Chung HH, et al. Risk and prognosis of ovarian cancer in women with endometriosis: a meta-analysis. Br J Cancer. 2014;110:1878–90.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  7. Pearce 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.

    Article  PubMed Central  PubMed  Google Scholar 

  8. Swiersz LM. Role of endometriosis in cancer and tumor development. Ann N Y Acad Sci. 2002;955:281–92.

    Article  PubMed  Google Scholar 

  9. Yamaguchi K, Mandai M, Toyokuni S, et al. Contents of endometriotic cysts, especially the high concentration of free iron, are a possible cause of carcinogenesis in the cysts through the iron-induced persistent oxidative stress. Clin Cancer Res. 2008;14:32–40.

    Article  CAS  PubMed  Google Scholar 

  10. Wiegand KC, Shah SP, Al-Agha OM, et al. ARID1A mutations in endometriosis-associated ovarian carcinomas. N Engl J Med. 2010;363:1532–43.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  11. Erzen M, Rakar S, Klancar B, et al. Endometriosis-associated ovarian carcinoma (EAOC): an entity distinct from other ovarian carcinomas as suggested by a nested case-control study. Gynecol Oncol. 2001;83:100–8.

    Article  CAS  PubMed  Google Scholar 

  12. Cool B, Laverty CRA, Fortune DW. Clear cell carcinoma of the ovary: clinical and pathological features. Aust N Z J Obstet Gynaecol. 1975;15:40–6.

    Article  Google Scholar 

  13. Crozier MA, Copeland LJ, Silva EG, et al. Clear cell carcinoma of the ovary: a study of 59 cases. Gynecol Oncol. 1989;35:199–203.

    Article  CAS  PubMed  Google Scholar 

  14. Komiyama S, Aoki D, Tominaga E, et al. Prognosis of Japanese patients with ovarian clear cell carcinoma associated with pelvic endometriosis: clinicopathologic evaluation. Gynecol Oncol. 1999;72:342–6.

    Article  CAS  PubMed  Google Scholar 

  15. Kita T, Kikuchi Y, Kudoh K, et al. Exploratory study of effective chemotherapy to clear cell carcinoma of the ovary. Oncol Rep. 2000;7:327–31.

    CAS  PubMed  Google Scholar 

  16. Orezzoli JP, Russell AH, Oliva E, et al. Prognostic implication of endometriosis in clear cell carcinoma of the ovary. Gynecol Oncol. 2008;110:336–44.

    Article  CAS  PubMed  Google Scholar 

  17. Veras E, Mao TL, Ayhan A, et al. Cystic and adenofibromatous clear cell carcinomas of the ovary: distinctive tumors that differ in their pathogenesis and behavior: a clinicopathologic analysis of 122 cases. Am J Surg Pathol. 2009;33:844–53.

    Article  PubMed  Google Scholar 

  18. Cuff J, Longacre TA. Endometriosis does not confer improved prognosis in ovarian carcinoma of uniform cell type. Am J Surg Pathol. 2012;36:688–95.

    Article  PubMed  Google Scholar 

  19. Katagiri A, Nakayama K, Rahman MT, et al. Loss of ARID1A expression is related to shorter progression-free survival and chemoresistance in ovarian clear cell carcinoma. Mod Pathol. 2012;25:282–8.

    CAS  PubMed  Google Scholar 

  20. Noli S, Cipriani S, Scarfone G, et al. Long-term survival of ovarian endometriosis associated clear cell and endometrioid ovarian cancers. Int J Gynecol Cancer. 2013;23:244–8.

    Article  PubMed  Google Scholar 

  21. Scarfone G, Bergamini A, Noli S, et al. Characteristics of clear cell ovarian cancer arising from endometriosis: a two-center cohort study. Gynecol Oncol. 2014;133:480–4.

    Article  PubMed  Google Scholar 

  22. Sampson J. Endometrial carcinoma of the ovary arising in endometrial tissue in that organ. Arch Surg. 1925;10:1–72.

    Article  Google Scholar 

  23. Scott R. Malignant change in endometriosis. Obstet Gynecol. 1953;2:293–9.

    Google Scholar 

  24. Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. J Clin Epidemiol. 2009;62:e1–34.

    Article  PubMed  Google Scholar 

  25. Wells GA, Shea B, O’Connell D, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp. Accessed 2 Sept 2014.

  26. Tierney JF, Stewart LA, Ghersi D, et al. Practical methods for incorporating summary time-to-event data into meta-analysis. Trials. 2007;8:16.

    Article  PubMed Central  PubMed  Google Scholar 

  27. Bast Jr RC, Hennessy B, Mills GB. The biology of ovarian cancer: new opportunities for translation. Nat Rev Cancer. 2009;9:415–28.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  28. Cho KR, Shih Ie M. Ovarian cancer. Ann Rev Pathol. 2009;4:287–313.

    Article  CAS  Google Scholar 

  29. Bulun SE. Endometriosis. N Engl J Med. 2009;360:268–79.

    Article  CAS  PubMed  Google Scholar 

  30. Somigliana E, Vigano P, Parazzini F, et al. Association between endometriosis and cancer: a comprehensive review and a critical analysis of clinical and epidemiological evidence. Gynecol Oncol. 2006;101:331–41.

    Article  PubMed  Google Scholar 

  31. Yamada Y, Shigetomi H, Onogi A, et al. Redox-active iron-induced oxidative stress in the pathogenesis of clear cell carcinoma of the ovary. Int J Gynecol Cancer. 2011;21:1200–7.

    PubMed  Google Scholar 

  32. Kobayashi H, Yamada Y, Kanayama S, et al. The role of hepatocyte nuclear factor-1beta in the pathogenesis of clear cell carcinoma of the ovary. Int J Gynecol Cancer. 2009;19:471–9.

    Article  PubMed  Google Scholar 

  33. Kumar S, Munkarah A, Arabi H, et al. Prognostic analysis of ovarian cancer associated with endometriosis. Am J Obstet Gynecol. 2011;204:e61–7.

    Google Scholar 

  34. McMeekin DS, Burger RA, Manetta A, et al. Endometrioid adenocarcinoma of the ovary and its relationship to endometriosis. Gynecol Oncol. 1995;59:81–6.

    Article  CAS  PubMed  Google Scholar 

  35. Garrett LA, Growdon WB, Goodman A, et al. Endometriosis-associated ovarian malignancy: a retrospective analysis of presentation, treatment, and outcome. J Reprod Med. 2013;58:469–76.

    PubMed  Google Scholar 

  36. Tay SK, Cheong MA. Evidence for ethnic and environmental contributions to frequency of ovarian clear cell carcinoma. Aust N Z J Obstet Gynaecol. 2014;54:225–30.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by grants from the Seoul National University Hospital research fund (Nos. 04-2012-0890 and 03-2012-0170) and the Priority Research Centers Program (No. 2009-0093820), the Basic Science Research Program (No. 2011-0025394), and the BK21 plus program (No. 5256-20140100) through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology. Moreover, it also was supported by a grant of the Korean Health Technology R&D Project, Ministry of Health of Welfare (HI14C2404).

Conflict of interest

There are no conflicts of interest.

Author information

Authors and Affiliations

  1. Department of Obstetrics and Gynecology, Seoul National University College of Medicine, Seoul, Republic of Korea

    Hee Seung Kim MD, Maria Lee MD, Hyun Hoon Chung MD, PhD & Yong Sang Song MD, PhD

  2. Cancer Research Institute, Seoul National University College of Medicine, Seoul, Republic of Korea

    Hee Seung Kim MD & Yong Sang Song MD, PhD

  3. Department of Pathology, Seoul National University College of Medicine, Seoul, Republic of Korea

    Min A. Kim MD, PhD

  4. Department of Obstetrics and Gynecology, Seoul National University Bundang Hospital, Seongnam, Republic of Korea

    Dong Hoon Suh MD, Kidong Kim MD, PhD, Jae Hong No MD, PhD & Yong Beom Kim MD, PhD

  5. Major in Biomodulation, World Class University, Seoul National University, Seoul, Republic of Korea

    Yong Sang Song MD, PhD

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  1. Hee Seung Kim MD
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  2. Min A. Kim MD, PhD
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Correspondence to Yong Sang Song MD, PhD.

Electronic Supplementary Material

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Search strategy and number of studies identified for inclusion in this meta-analysis. (PPTX 63 kb)

10434_2014_4319_MOESM2_ESM.pptx

Funnel plots with Egger’s tests representing no publication bias in this meta-analysis for comparing (a) progression-free survival and (b) overall survival between patients who have ovarian clear cell carcinoma (OCCC) with endometriosis and those without endometriosis. (PPTX 70 kb)

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Supplementary material 5 (DOCX 25 kb)

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Kim, H.S., Kim, M.A., Lee, M. et al. Effect of Endometriosis on the Prognosis of Ovarian Clear Cell Carcinoma: A Two-Center Cohort Study and Meta-analysis. Ann Surg Oncol 22, 2738–2745 (2015). https://doi.org/10.1245/s10434-014-4319-9

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  • DOI: https://doi.org/10.1245/s10434-014-4319-9

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