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Friend or foe? The prognostic role of endometriosis in women with clear cell ovarian carcinoma. A UK population-based cohort study

  • Gynecologic Oncology
  • Published:
Archives of Gynecology and Obstetrics Aims and scope Submit manuscript

Abstract

Purpose

The prognostic role of endometriosis amongst women with ovarian clear cell carcinoma (OCCC) remains debatable. The aim of this study was to ascertain the effect of endometriosis on the prognosis of OCCC.

Methods

A retrospective review of the medical records of 94 women diagnosed and treated for OCCC at a tertiary gynaecological cancer centre in the UK, spanning the period 2010–2019. Women were divided into two groups according to the presence of endometriosis. Clinico-pathological characteristics, progression-free survival (PFS) and overall survival (OS) were collated between the two groups.

Results

Forty-six cases of endometriosis-free OCCC (Ef-OCCC) were collated with 48 cases of endometriosis-related OCCC (Er-OCCC). There was no significant difference between the two groups regarding age (p-value = 0.2), FIGO stage (p-value = 0.8), residual disease (RD) (p-value = 0.07), adjuvant chemotherapy agent (p-value = 0.4) or chemo-resistance (p-value = 0.9). The presence of endometriosis did not significantly affect either OS or PFS. The median OS in the Ef-OCCC and Er-OCCC was 55.00 (95% CI 32.00–189.00) and 71.00 (95% CI 47.00–97.00; log rank = 1.35, p-value = 0.2) months. The median PFS in the Ef-OCCC and Er-OCCC group was 39.00 (95% CI 19.00–143.00) and 39.00 (95% CI 19.00–62.00; log rank = 0.7, p-value = 0.4) months. Survival differences between the two groups were not significant after stratification analysis for independent prognosticators.

Conclusion

Endometriosis was not independently associated with the prognosis of OCCC either in crude analysis or after stratification for stage and RD. Further larger, well-designed prospective studies are warranted to draw firmer conclusions on the intrinsic link between endometriosis and OCCC.

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References

  1. Brinton LA, Sahasrabuddle V, Trabert B (2013) Epidemiology of gynecologic cancers. In: Barakat RR, Berchuck A, Markman M et al (eds) Principles and practice of gynecologic oncology, 6th edn. Lippincott Williams & Wilkins, Philadelphia, pp 1–29

    Google Scholar 

  2. Anglesio MS, Carey MS, Köbel M, Mackay H, Huntsman DG (2011) Vancouver ovarian clear cell symposium speakers. Clear cell carcinoma of the ovary: a report from the first Ovarian Clear Cell Symposium, June 24th, 2010. Gynecol Oncol 121:407–415

    Article  PubMed  Google Scholar 

  3. del Carmen MG, Birrer M, Schorge JO (2012) Clear cell carcinoma of the ovary: a review of the literature. Gynecol Oncol 126:481–490

    Article  PubMed  Google Scholar 

  4. Goff BA, de la Cuesta SR, Muntz HG et al (1996) Clear cell carcinoma of the ovary: a distinct histologic type with poor prognosis and resistance to platinum-based chemotherapy in stage III disease. Gynecol Oncol 60:412–417

    Article  CAS  PubMed  Google Scholar 

  5. Winter WE 3rd, Maxwell GL, Tian C et al (2007) Prognostic factors for stage III epithelial ovarian cancer: a Gynecologic Oncology Group Study. J Clin Oncol 25:3621–3627

    Article  PubMed  Google Scholar 

  6. Duska LR, Garrett L, Henretta M et al (2010) When ‘never-events’ occur despite adherence to clinical guidelines: the case of venous thromboembolism in clear cell cancer of the ovary compared with other epithelial histologic subtypes. Gynecol Oncol 116:374–377

    Article  PubMed  Google Scholar 

  7. Omura GA, Brady MF, Homesley HD et al (1991) Long-term follow-up and prognostic factor analysis in advanced ovarian carcinoma: the Gynecologic Oncology Group experience. J Clin Oncol 9:1138–1150

    Article  CAS  PubMed  Google Scholar 

  8. King CM, Barbara C, Prentice A, Brenton JD, Charnock-Jones DS (2016) Models of endometriosis and their utility in studying progression to ovarian clear cell carcinoma. J Pathol 238:185–196

    Article  PubMed  Google Scholar 

  9. Soigliana 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 101:331–341

    Article  Google Scholar 

  10. Hermens M, van Altena AM, Nieboer TE, Schoot BC, van Vliet HAAM, Siebers AG et al (2020) Incidence of endometriosis and clear-cell ovarian cancer in histological proven endometriosis: the ENOCA population-based cohort study. Am J Obstet Gynecol 107:e1-11

    Google Scholar 

  11. Kim HS, Kim TH, Song YS (2014) Risk and prognosis of ovarian cancer in women with endometriosis: a meta-analysis. Br J Cancer 110(7):1878–1890

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Kim HS, Kim MA, Lee M, Suh DH, Kim K, No JH et al (2015) 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

    Article  PubMed  Google Scholar 

  13. Samson JA (1925) Endometrial carcinoma of the ovary, arising in endometrial tissue in that organ. Arch Surg 10:1–72

    Article  Google Scholar 

  14. Scott RB (1953) Malignant changes in endometriosis. Obstet Gynecol 2:283–289

    CAS  PubMed  Google Scholar 

  15. Kondi-Pafiti A, Papakonstantinou E, Iavazzo C, Grigoriadis C, Salakos N, Gregoriou O (2012) Clinicopathological characteristics of ovarian carcinomas associated with endometriosis. Arch Gynecol Obstet 285:479–483

    Article  CAS  PubMed  Google Scholar 

  16. Erzen M, Rakar S, Klancnik B, Syrjänen K (2001) Endometriosis-associated ovarian carcinoma (EAOC): an entity distinct from other ovarian carcinomas as suggested by a nested case-control study. Gynecol Oncol 83:100–108

    Article  CAS  PubMed  Google Scholar 

  17. Scarfone G, Bergamini A, Noli S, Villa A, Cipriani S, Taccagni G, Vigano P et al (2014) Characteristics of clear cell ovarian cancer arising from endometriosis: a two center cohort study. Gynecol Oncol 133:480–484

    Article  PubMed  Google Scholar 

  18. Kumar S, Munkarah A, Arabi H, Bandyopadhyay S, Semaan A, Hayek K, Garg G et al (2011) Prognostic analysis of ovarian cancer associated with endometriosis. Am J Obstet Gynecol 204(63):e1-7

    Google Scholar 

  19. Pearce CL, Templeman C, Rossing MA, Lee A, Near AM, Webb PM, Nagle CM et al (2012) Association between endometriosis and risk of histological subtypes of ovarian cancer: a pooled analysis of case-control studies. Lancet Oncol 13:385–394

    Article  PubMed  PubMed Central  Google Scholar 

  20. Heidemann LN, Hartwell D, Heidemann CH, Jochumsen KM (2014) The relation between endometriosis and ovarian cancer—a review. Acta Obstet Gynecol Scand 93:20–31

    Article  PubMed  Google Scholar 

  21. Hermens M, van Altena AM, Nieboer TE, Schoot BC, van Vliet HAAM, Siebers AG, Bekkers RLM (2020) Incidence of endometrioid and clear-cell ovarian cancer in histological proven endometriosis: the ENOCA population-based cohort study. Am J Obstet Gynecol 223:107.e1-107.e11

    Article  Google Scholar 

  22. Tay SK, Cheong MA (2014) Evidence for ethnic and environmental contributions to frequency of ovarian clear cell carcinoma. Just N Z J Obstet Gynaecol 54:225–230

    Article  Google Scholar 

  23. Chan JK, Teoh D, Hu JM et al (2008) Do clear cell ovarian carcinomas have poorer prognosis compared to other epithelial cell types? A study of 1411 clear cell ovarian cancers. Gynecol Oncol 109:370–376

    Article  PubMed  Google Scholar 

  24. Kurman RJ, Shih IM (2010) The origin and pathogenesis of epithelial ovarian cancer: a proposed unifying theory. Am J Surg Pathol 34:433–443

    Article  PubMed  PubMed Central  Google Scholar 

  25. Bulun SE, Wan Y, Matei D (2019) Epithelial mutations in endometriosis: link to ovarian cancer. Endocrinology 160:626–638

    Article  PubMed  PubMed Central  Google Scholar 

  26. Saavalainen L, Lassus H, But A, Tiitinen A, Harkki P, Gissler M, Pukkala E, Heikinheimo O (2018) Risk of gynecologic cancer according to the type of endometriosis. Obstet Gynecol 131:1095–1102

    Article  PubMed  Google Scholar 

  27. Gadducci A, Lanfredini N, Tana R (2014) Novel insights on the malignant transformation of endometriosis into ovarian carcinoma. Gynecol Endocrinol 30(9):612–617

    Article  CAS  PubMed  Google Scholar 

  28. Paik ES, Kim TJ, Choi CH, Kim BG, Bae DS, Lee JW (2018) Clinical outcomes of patients with clear cell and endometrioid ovarian cancer arising from endometriosis. J Gynecol Oncol 29(2):e18

    Article  CAS  PubMed  Google Scholar 

  29. Scarfone G, Bergamini A, Noli S, Villa A, Cipriani S, Taccagni G, Vigano P et al (2014) Characteristics of clear cell ovarian cancer arising from endometriosis: a two center cohort study. Gynecol Oncol 133(3):480–484

    Article  PubMed  Google Scholar 

  30. Zhao T, Shao Y, Liu Y, Wang X, Guan L, Lu Y (2018) Endometriosis does not confer improved prognosis in ovarian clear cell carcinoma: a retrospective study at a single institute. J Ovarian Res 11(1):53

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Bai H, Cao D, Yuan F, Sha G, Yang J, Chen J, Wang Y et al (2016) Prognostic value of endometriosis in patients with stage I ovarian clear cell carcinoma: experiences at three academic institutions. Gynecol Oncol 143:526–531

    Article  PubMed  Google Scholar 

  32. Schnack TH, Høgdall E, Thomsen LN, Høgdall C (2017) Demographic, clinical, and prognostic factors of ovarian clear cell adenocarcinomas according to endometriosis status. Int J Gynecol Cancer 27:1804–1812

    Article  PubMed  Google Scholar 

  33. Ju UC, Kang WD, Kim SM (2019) The effect of concurrent endometriosis on the prognosis of women with ovarian clear cell or endometrioid carcinoma. Int J Gynaecol Obstet 146:177–183

    Article  CAS  PubMed  Google Scholar 

  34. Cool B, Laverty CRA, Fortune DW (1975) Clear cell carcinoma of the ovary—clinical and pathological features. Aust N Z J Obstet Gynaecol 15:40–46

    Article  Google Scholar 

  35. Crozier MA, Copeland LJ, Silva EG, Gershenson DM, Stringer CA (1989) Clear cell carcinoma of the ovary: a study of 59 cases. Gynecol Oncol 35:199–203

    Article  CAS  PubMed  Google Scholar 

  36. Komiyama S, Aoki D, Tominaga E, Susumu N, Udagawa Y, Nozawa S (1999) Prognosis of Japanese patients with ovarian clear cell carcinoma associated with pelvic endometriosis: clinicopathologic evaluation. Gynecol Oncol 72:342–346

    Article  CAS  PubMed  Google Scholar 

  37. Kita T, Kikuchi Y, Kudoh K, Takano M, Goto T, Hirata J, Tode T et al (2000) Exploratory study of effective chemotherapy to clear cell carcinoma of the ovary. Oncol Rep 7:327–331

    CAS  PubMed  Google Scholar 

  38. Orezzoli JP, Russell AH, Oliva E, Del Carmen MG, Eichhorn J, Fuller AF (2008) Prognostic implication of endometriosis in clear cell carcinoma of the ovary. Gynecol Oncol 110:336–344

    Article  CAS  PubMed  Google Scholar 

  39. Veras E, Mao TL, Ayhan A, Ueda S, Lai H, Hayran M, Shih IEM et al (2009) 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 33:844–853

    Article  PubMed  Google Scholar 

  40. Katagiri A, Nakayama K, Rahman MT, Rahman M, Katagiri H, Nakayama N, Ishikawa M et al (2012) Loss of ARID1A expression is related to shorter progression-free survival and chemoresistance in ovarian clear cell carcinoma. Mod Pathol 25:282–288

    Article  CAS  PubMed  Google Scholar 

  41. Ye S, Yang J, You Y, Cao D, Bai H, Lang J, Chen J et al (2014) Comparative study of ovarian clear cell carcinoma with and without endometriosis in People’s Republic of China. Fertil Steril 102:1656–1662

    Article  PubMed  Google Scholar 

  42. Ishibashi H, Takano M, Miyamoto M, Soyama H, Matsuura H, Aoyama T, Yoshikawa T et al (2017) Role of endometriosis as a prognostic factor for post-progression survival in ovarian clear cell carcinoma. Mol Clin Oncol 7:1027–1031

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Kawabata A, Yanaihara N, Nagata C, Saito M, Noguchi D, Takenaka M, Iida Y et al (2017) Prognostic impact of interleukin-6 expression in stage I ovarian clear cell carcinoma. Gynecol Oncol 146:609–614

    Article  CAS  PubMed  Google Scholar 

  44. Park JY, Kim DY, Suh DS, Kim JH, Kim YM, Kim YT, Nam JH (2018) Significance of ovarian endometriosis on the prognosis of ovarian clear cell carcinoma. Int J Gynecol Cancer 28:11–18

    Article  PubMed  Google Scholar 

  45. Lee HY, Hong JH, Byun JH, Kim HJ, Baek SK, Kim JY, Kim KH et al (2020) Clinical characteristics of clear cell ovarian cancer: a retrospective multicenter experience of 308 patients in South Korea. Cancer Res Treat 52:277–283

    Article  PubMed  Google Scholar 

  46. Colombo N, Sessa C, du Bois A et al (2019) ESMO-ESGO consensus conference recommendations on ovarian cancer: pathology and molecular biology, early and advanced stages, borderline tumours and recurrent disease†. Ann Oncol 30:672–705

    Article  CAS  PubMed  Google Scholar 

  47. Timmers PJ, Zwinderman AH, Teodorovic I et al (2009) Clear cell carcinoma compared to serous carcinoma in early ovarian cancer: same prognosis in a large randomized trial. Int J Gynecol Cancer 19:88–93

    Article  CAS  PubMed  Google Scholar 

  48. Oseledchyk A, Leitao MM, Konner J et al (2017) Adjuvant chemotherapy in patients with stage I endometrioid or clear cell ovarian cancer in the platinum era: a surveillance, epidemiology, and end results cohort study, 2000–2013. Ann Oncol 28:2985–2993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Bogani G, Ditto A, Lopez S et al (2020) Adjuvant chemotherapy vs. observation in stage I clear cell ovarian carcinoma: a systematic review and meta-analysis. Gynecol Oncol 157:293–298

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors would like thank Dr. Bindya Gupta for her invaluable support and clinical expertise. We would also like to thank the women whose details from the basis of this study and all members of the gynaecological MDT at Pan-Birmingham Gynaecological Cancer Centre.

Funding

The authors have not declared a specific grant for this research from any funding agency in the public, commercial, or not-for-profit sectors.

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Project development: AT and BG, data collection: AK, AL, FB, data analysis: AT, manuscript writing: AT, AL, AK, manuscript editing: JB, JY, KS. All authors approved the final submitted draft.

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Correspondence to Anastasios Tranoulis.

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Tranoulis, A., Buruiana, F.H., Gupta, B. et al. Friend or foe? The prognostic role of endometriosis in women with clear cell ovarian carcinoma. A UK population-based cohort study. Arch Gynecol Obstet 305, 1279–1289 (2022). https://doi.org/10.1007/s00404-021-06191-8

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  • DOI: https://doi.org/10.1007/s00404-021-06191-8

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