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Endometriosis and risk of ovarian cancer: what do we know?

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Abstract

Purpose

Despite long and intensive research, endometriosis remains one of the leading causes of morbidity among premenopausal women. The majority of endometriosis-related ovarian carcinomas occur in the presence of atypical ovarian endometriosis. Nevertheless, despite the increased incidence of ovarian cancer in patients with endometriosis, our knowledge of the risk factors and mechanisms is still incomplete.

Method

Narrative overview, synthesizing the recent findings of literature retrieved from databases.

Results

Herein, we reviewed and summarized the most recent knowledge regarding endometriosis and ovarian cancer.

Conclusion

The evidence showing that patients with endometriosis have a higher risk of developing ovarian cancer is compelling. However, the question of how much higher the absolute risk is, is not fully clear.

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References

  1. de Ziegler D, Borghese B, Chapron C (2010) Endometriosis and infertility: pathophysiology and management. Lancet 376(9742):730–738. https://doi.org/10.1016/S0140-6736(10)60490-4

    Article  CAS  PubMed  Google Scholar 

  2. Baldi A, Campioni M, Signorile PG (2008) Endometriosis: pathogenesis, diagnosis, therapy and association with cancer (review). Oncol Rep 19(4):843–846

    CAS  PubMed  Google Scholar 

  3. von Rokytansky C (1860) Über Uterusdrüsen-Neubildung in Uterus- und Ovarial-Sarcomen. Z Ges Artze Wein 37:577–593

    Google Scholar 

  4. Dunselman GA, Vermeulen N, Becker C, Calhaz-Jorge C, D'Hooghe T, De Bie B, Heikinheimo O, Horne AW, Kiesel L, Nap A, Prentice A, Saridogan E, Soriano D, Nelen W, European Society of Human Reproduction Embryology (2014) ESHRE guideline: management of women with endometriosis. Hum Reprod 29(3):400–412. https://doi.org/10.1093/humrep/det457

    Article  CAS  PubMed  Google Scholar 

  5. Guerriero S, Condous G, van den Bosch T, Valentin L, Leone FP, Van Schoubroeck D, Exacoustos C, Installe AJ, Martins WP, Abrao MS, Hudelist G, Bazot M, Alcazar JL, Goncalves MO, Pascual MA, Ajossa S, Savelli L, Dunham R, Reid S, Menakaya U, Bourne T, Ferrero S, Leon M, Bignardi T, Holland T, Jurkovic D, Benacerraf B, Osuga Y, Somigliana E, Timmerman D (2016) Systematic approach to sonographic evaluation of the pelvis in women with suspected endometriosis, including terms, definitions and measurements: a consensus opinion from the International Deep Endometriosis Analysis (IDEA) group. Ultrasound Obstet Gynecol 48(3):318–332. https://doi.org/10.1002/uog.15955

    Article  CAS  PubMed  Google Scholar 

  6. Sofo V, Gotte M, Lagana AS, Salmeri FM, Triolo O, Sturlese E, Retto G, Alfa M, Granese R, Abrao MS (2015) Correlation between dioxin and endometriosis: an epigenetic route to unravel the pathogenesis of the disease. Arch Gynecol Obstet 292(5):973–986. https://doi.org/10.1007/s00404-015-3739-5

    Article  CAS  PubMed  Google Scholar 

  7. Vetvicka V, Kralickova M (2015) Current theories on endometriosis pathogenesis. Edorium J Mol Pathol 1:1–4

    Google Scholar 

  8. Vitale SG, La Rosa VL, Rapisarda AMC, Lagana AS (2017) Impact of endometriosis on quality of life and psychological well-being. J Psychosom Obstet Gynaecol 38(4):317–319. https://doi.org/10.1080/0167482X.2016.1244185

    Article  PubMed  Google Scholar 

  9. Kralickova M, Losan P, Vetvicka V (2014) Endometriosis and cancer. Women's Health 10(6):591–597. https://doi.org/10.2217/whe.14.43

    Article  CAS  PubMed  Google Scholar 

  10. Sampson JA (1925) Endometrial carcinoma of the ovary, arising in endometrial tissue in that organ. Arch Surg 10(1):1–72. https://doi.org/10.1001/archsurg.1925.01120100007001

    Article  Google Scholar 

  11. Scott RB (1953) Malignant changes in endometriosis. Obstet Gynecol 2(3):283–289

    CAS  PubMed  Google Scholar 

  12. Hunn J, Rodriguez GC (2012) Ovarian cancer: etiology, risk factors, and epidemiology. Clin Obstet Gynecol 55(1):3–23. https://doi.org/10.1097/GRF.0b013e31824b4611

    Article  PubMed  Google Scholar 

  13. Olovsson M (2011) Immunological aspects of endometriosis: an update. Am J Reprod Immunol 66(Suppl 1):101–104. https://doi.org/10.1111/j.1600-0897.2011.01045.x

    Article  PubMed  Google Scholar 

  14. Sayasneh A, Tsivos D, Crawford R (2011) Endometriosis and ovarian cancer: a systematic review. ISRN Obstet Gynecol 2011:140310. https://doi.org/10.5402/2011/140310

    Article  PubMed  PubMed Central  Google Scholar 

  15. Vlahos NF, Kalampokas T, Fotiou S (2010) Endometriosis and ovarian cancer: a review. Gynecol Endocrinol 26(3):213–219. https://doi.org/10.1080/09513590903184050

    Article  PubMed  Google Scholar 

  16. Kvaskoff M, Horne AW, Missmer SA (2017) Informing women with endometriosis about ovarian cancer risk. Lancet 390(10111):2433–2434. https://doi.org/10.1016/S0140-6736(17)33049-0

    Article  PubMed  Google Scholar 

  17. LaGrenade A, Silverberg SG (1988) Ovarian tumors associated with atypical endometriosis. Hum Pathol 19(9):1080–1084

    Article  CAS  PubMed  Google Scholar 

  18. Maiorana A, Cicerone C, Niceta M, Alio L (2007) Evaluation of serum CA 125 levels in patients with pelvic pain related to endometriosis. Int J Biol Markers 22(3):200–202

    Article  CAS  PubMed  Google Scholar 

  19. Ness RB, Cottreau C (1999) Possible role of ovarian epithelial inflammation in ovarian cancer. J Natl Cancer Inst 91(17):1459–1467

    Article  CAS  PubMed  Google Scholar 

  20. Wang C, Liang Z, Liu X, Zhang Q, Li S (2016) The association between endometriosis, tubal ligation, hysterectomy and epithelial ovarian cancer: meta-analyses. Int J Environ Res Public Health 13:11. https://doi.org/10.3390/ijerph13111138

    Article  Google Scholar 

  21. Grandi G, Toss A, Cortesi L, Botticelli L, Volpe A, Cagnacci A (2015) The association between endometriomas and ovarian cancer: Preventive effect of inhibiting ovulation and menstruation during reproductive life. Biomed Res Int 2015:751571. https://doi.org/10.1155/2015/751571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Zorn KK, Tian C, McGuire WP, Hoskins WJ, Markman M, Muggia FM, Rose PG, Ozols RF, Spriggs D, Armstrong DK (2009) The prognostic value of pretreatment CA 125 in patients with advanced ovarian carcinoma: a Gynecologic Oncology Group study. Cancer 115(5):1028–1035. https://doi.org/10.1002/cncr.24084

    Article  PubMed  Google Scholar 

  23. Ruderman R, Pavone ME (2017) Ovarian cancer in endometriosis: an update on the clinical and molecular aspects. Minerva Ginecol 69(3):286–294. https://doi.org/10.23736/S0026-4784.17.04042-4

    Article  PubMed  Google Scholar 

  24. Ogawa S, Kaku T, Amada S, Kobayashi H, Hirakawa T, Ariyoshi K, Kamura T, Nakano H (2000) Ovarian endometriosis associated with ovarian carcinoma: a clinicopathological and immunohistochemical study. Gynecol Oncol 77(2):298–304. https://doi.org/10.1006/gyno.2000.5765

    Article  CAS  PubMed  Google Scholar 

  25. Wilbur MA, Shih IM, Segars JH, Fader AN (2017) Cancer implications for patients with endometriosis. Semin Reprod Med 35(1):110–116. https://doi.org/10.1055/s-0036-1597120

    Article  CAS  PubMed  Google Scholar 

  26. Mandai M, Yamaguchi K, Matsumura N, Baba T, Konishi I (2009) Ovarian cancer in endometriosis: molecular biology, pathology, and clinical management. Int J Clin Oncol 14(5):383–391. https://doi.org/10.1007/s10147-009-0935-y

    Article  PubMed  Google Scholar 

  27. Yamashita Y, Akatsuka S, Shinjo K, Yatabe Y, Kobayashi H, Seko H, Kajiyama H, Kikkawa F, Takahashi T, Toyokuni S (2013) Met is the most frequently amplified gene in endometriosis-associated ovarian clear cell adenocarcinoma and correlates with worsened prognosis. PLoS ONE 8(3):e57724. https://doi.org/10.1371/journal.pone.0057724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Brinton LA, Gridley G, Persson I, Baron J, Bergqvist A (1997) Cancer risk after a hospital discharge diagnosis of endometriosis. Am J Obstet Gynecol 176(3):572–579

    Article  CAS  PubMed  Google Scholar 

  29. Kim HS, Kim TH, Chung HH, Song YS (2014) Risk and prognosis of ovarian cancer in women with endometriosis: a meta-analysis. Br J Cancer 110(7):1878–1890. https://doi.org/10.1038/bjc.2014.29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Gadducci A, Lanfredini N, Tana R (2014) Novel insights on the malignant transformation of endometriosis into ovarian carcinoma. Gynecol Endocrinol 30(9):612–617. https://doi.org/10.3109/09513590.2014.926325

    Article  CAS  PubMed  Google Scholar 

  31. Rossing MA, Cushing-Haugen KL, Wicklund KG, Doherty JA, Weiss NS (2008) Risk of epithelial ovarian cancer in relation to benign ovarian conditions and ovarian surgery. Cancer Causes Control 19(10):1357–1364. https://doi.org/10.1007/s10552-008-9207-9

    Article  PubMed  PubMed Central  Google Scholar 

  32. Chang WH, Wang KC, Lee WL, Huang N, Chou YJ, Feng RC, Yen MS, Huang BS, Guo CY, Wang PH (2014) Endometriosis and the subsequent risk of epithelial ovarian cancer. Taiwan J Obstet Gynecol 53(4):530–535. https://doi.org/10.1016/j.tjog.2014.04.025

    Article  PubMed  Google Scholar 

  33. Melin A, Sparen P, Persson I, Bergqvist A (2006) Endometriosis and the risk of cancer with special emphasis on ovarian cancer. Hum Reprod 21(5):1237–1242. https://doi.org/10.1093/humrep/dei462

    Article  CAS  PubMed  Google Scholar 

  34. Mogensen JB, Kjaer SK, Mellemkjaer L, Jensen A (2016) Endometriosis and risks for ovarian, endometrial and breast cancers: a nationwide cohort study. Gynecol Oncol 143(1):87–92. https://doi.org/10.1016/j.ygyno.2016.07.095

    Article  PubMed  Google Scholar 

  35. Kok VC, Tsai HJ, Su CF, Lee CK (2015) The risks for ovarian, endometrial, breast, colorectal, and other cancers in women with newly diagnosed endometriosis or adenomyosis: a population-based study. Int J Gynecol Cancer 25(6):968–976. https://doi.org/10.1097/IGC.0000000000000454

    Article  PubMed  Google Scholar 

  36. Wang Q, Wang L, Ding X, Liu A (2017) Expression and significance of ARID1A mRNA in endometriosis-associated ovarian cancer. J BUON 22(5):1314–1321

    PubMed  Google Scholar 

  37. Brilhante AV, Augusto KL, Portela MC, Sucupira LC, Oliveira LA, Pouchaim AJ, Nobrega LR, Magalhaes TF, Sobreira LR (2017) Endometriosis and ovarian cancer: an integrative review (endometriosis and ovarian cancer). Asian Pac J Cancer Prev 18(1):11–16. https://doi.org/10.22034/APJCP.2017.18.1.11

    Article  PubMed  PubMed Central  Google Scholar 

  38. Garrett LA, Growdon WB, Goodman A, Boruta DM, Schorge JO, del Carmen MG (2013) Endometriosis-associated ovarian malignancy: a retrospective analysis of presentation, treatment, and outcome. J Reprod Med 58(11–12):469–476

    PubMed  Google Scholar 

  39. Dinkelspiel HE, Matrai C, Pauk S, Pierre-Louis A, Chiu YL, Gupta D, Caputo T, Ellenson LH, Holcomb K (2016) Does the presence of endometriosis affect prognosis of ovarian cancer? Cancer Invest 34(3):148–154. https://doi.org/10.3109/07357907.2016.1139716

    Article  PubMed  PubMed Central  Google Scholar 

  40. Taniguchi F (2017) New knowledge and insights about the malignant transformation of endometriosis. J Obstet Gynaecol Res 43(7):1093–1100. https://doi.org/10.1111/jog.13372

    Article  PubMed  Google Scholar 

  41. Szubert M, Suzin J, Obirek K, Sochacka A, Loszakiewicz M (2016) Clear cell ovarian cancer and endometriosis: is there a relationship? Prz Menopauzalny 15(2):85–89. https://doi.org/10.5114/pm.2016.61190

    Article  PubMed  PubMed Central  Google Scholar 

  42. Noli S, Cipriani S, Scarfone G, Villa A, Grossi E, Monti E, Vercellini P, Parazzini F (2013) Long term survival of ovarian endometriosis associated clear cell and endometrioid ovarian cancers. Int J Gynecol Cancer 23(2):244–248. https://doi.org/10.1097/IGC.0b013e31827aa0bb

    Article  PubMed  Google Scholar 

  43. Bounous VE, Ferrero A, Fuso L, Ravarino N, Ceccaroni M, Menato G, Biglia N (2016) Endometriosis-associated ovarian cancer: a distinct clinical entity? Anticancer Res 36(7):3445–3449

    PubMed  Google Scholar 

  44. Melin A, Lundholm C, Malki N, Swahn ML, Sparen P, Bergqvist A (2011) Endometriosis as a prognostic factor for cancer survival. Int J Cancer 129(4):948–955. https://doi.org/10.1002/ijc.25718

    Article  CAS  PubMed  Google Scholar 

  45. Melin AS, Lundholm C, Malki N, Swahn ML, Sparen P, Bergqvist A (2013) Hormonal and surgical treatments for endometriosis and risk of epithelial ovarian cancer. Acta Obstet Gynecol Scand 92(5):546–554. https://doi.org/10.1111/aogs.12123

    Article  PubMed  Google Scholar 

  46. Kobayashi H (2016) Potential scenarios leading to ovarian cancer arising from endometriosis. Redox Rep 21(3):119–126. https://doi.org/10.1179/1351000215Y.0000000038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Fontana J, Zima M, Vetvicka V (2018) Biological markers of oxidative stress in cardiovascular diseases: after so many studies, what do we know? Immunol Invest. https://doi.org/10.1080/08820139.2018.1523925

    Article  PubMed  Google Scholar 

  48. Vercellini P, Vigano P, Buggio L, Makieva S, Scarfone G, Cribiu FM, Parazzini F, Somigliana E (2018) Perimenopausal management of ovarian endometriosis and associated cancer risk: when is medical or surgical treatment indicated? Best Pract Res Clin Obstet Gynaecol 51:151–168. https://doi.org/10.1016/j.bpobgyn.2018.01.017

    Article  PubMed  Google Scholar 

  49. Dzatic-Smiljkovic O, Vasiljevic M, Djukic M, Vugdelic R, Vugdelic J (2011) Frequency of ovarian endometriosis in epithelial ovarian cancer patients. Clin Exp Obstet Gynecol 38(4):394–398

    CAS  PubMed  Google Scholar 

  50. Lagana AS, Triolo O, Salmeri FM, Granese R, Palmara VI, Ban Frangez H, Vrtcnik Bokal E, Sofo V (2016) Natural killer T cell subsets in eutopic and ectopic endometrium: a fresh look to a busy corner. Arch Gynecol Obstet 293(5):941–949. https://doi.org/10.1007/s00404-015-4004-7

    Article  CAS  PubMed  Google Scholar 

  51. Riccio LGC, Baracat EC, Chapron C, Batteux F, Abrao MS (2017) The role of the B lymphocytes in endometriosis: a systematic review. J Reprod Immunol 123:29–34. https://doi.org/10.1016/j.jri.2017.09.001

    Article  CAS  PubMed  Google Scholar 

  52. Hanada T, Tsuji S, Nakayama M, Wakinoue S, Kasahara K, Kimura F, Mori T, Ogasawara K, Murakami T (2018) Suppressive regulatory T cells and latent transforming growth factor-beta-expressing macrophages are altered in the peritoneal fluid of patients with endometriosis. Reprod Biol Endocrinol 16(1):9. https://doi.org/10.1186/s12958-018-0325-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Salmeri FM, Lagana AS, Sofo V, Triolo O, Sturlese E, Retto G, Pizzo A, D'Ascola A, Campo S (2015) Behavior of tumor necrosis factor-alpha and tumor necrosis factor receptor 1/tumor necrosis factor receptor 2 system in mononuclear cells recovered from peritoneal fluid of women with endometriosis at different stages. Reprod Sci 22(2):165–172. https://doi.org/10.1177/1933719114536472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Sturlese E, Salmeri FM, Retto G, Pizzo A, De Dominici R, Ardita FV, Borrielli I, Licata N, Lagana AS, Sofo V (2011) Dysregulation of the Fas/FasL system in mononuclear cells recovered from peritoneal fluid of women with endometriosis. J Reprod Immunol 92(1–2):74–81. https://doi.org/10.1016/j.jri.2011.08.005

    Article  CAS  PubMed  Google Scholar 

  55. Vetvicka V, Lagana AS, Salmeri FM, Triolo O, Palmara VI, Vitale SG, Sofo V, Kralickova M (2016) Regulation of apoptotic pathways during endometriosis: from the molecular basis to the future perspectives. Arch Gynecol Obstet 294(5):897–904. https://doi.org/10.1007/s00404-016-4195-6

    Article  CAS  PubMed  Google Scholar 

  56. Jorgensen H, Hill AS, Beste MT, Kumar MP, Chiswick E, Fedorcsak P, Isaacson KB, Lauffenburger DA, Griffith LG, Qvigstad E (2017) Peritoneal fluid cytokines related to endometriosis in patients evaluated for infertility. Fertil Steril 107(5):1191–1199. https://doi.org/10.1016/j.fertnstert.2017.03.013

    Article  CAS  PubMed  Google Scholar 

  57. Haraguchi H, Koga K, Takamura M, Makabe T, Sue F, Miyashita M, Urata Y, Izumi G, Harada M, Hirata T, Hirota Y, Wada-Hiraike O, Oda K, Kawana K, Fujii T, Osuga Y (2016) Development of ovarian cancer after excision of endometrioma. Fertil Steril 106(6):1432–1437. https://doi.org/10.1016/j.fertnstert.2016.07.1077

    Article  PubMed  Google Scholar 

  58. Xu XR, Wang X, Zhang H, Liu MY, Chen Q (2018) The clinical significance of the combined detection of serum Smac, HE4 and CA125 in endometriosis-associated ovarian cancer. Cancer Biomark 21(2):471–477. https://doi.org/10.3233/CBM-170720

    Article  CAS  PubMed  Google Scholar 

  59. Capriglione S, Luvero D, Plotti F, Terranova C, Montera R, Scaletta G, Schiro T, Rossini G, Benedetti Panici P, Angioli R (2017) Ovarian cancer recurrence and early detection: may HE4 play a key role in this open challenge? A systematic review of literature. Med Oncol 34(9):164. https://doi.org/10.1007/s12032-017-1026-y

    Article  CAS  PubMed  Google Scholar 

  60. Pan Q, Luo X, Toloubeydokhti T, Chegini N (2007) The expression profile of micro-RNA in endometrium and endometriosis and the influence of ovarian steroids on their expression. Mol Hum Reprod 13(11):797–806. https://doi.org/10.1093/molehr/gam063

    Article  CAS  PubMed  Google Scholar 

  61. Wu RL, Ali S, Bandyopadhyay S, Alosh B, Hayek K, Daaboul MF, Winer I, Sarkar FH, Ali-Fehmi R (2015) Comparative analysis of differentially expressed miRNAs and their downstream mRNAs in ovarian cancer and its associated endometriosis. J Cancer Sci Ther 7(7):258–265. https://doi.org/10.4172/1948-5956.1000359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Suryawanshi S, Vlad AM, Lin HM, Mantia-Smaldone G, Laskey R, Lee M, Lin Y, Donnellan N, Klein-Patel M, Lee T, Mansuria S, Elishaev E, Budiu R, Edwards RP, Huang X (2013) Plasma microRNAs as novel biomarkers for endometriosis and endometriosis-associated ovarian cancer. Clin Cancer Res 19(5):1213–1224. https://doi.org/10.1158/1078-0432.CCR-12-2726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Meng Q, Sun W, Jiang J, Fletcher NM, Diamond MP, Saed GM (2011) Identification of common mechanisms between endometriosis and ovarian cancer. J Assist Reprod Genet 28(10):917–923. https://doi.org/10.1007/s10815-011-9573-1

    Article  PubMed  PubMed Central  Google Scholar 

  64. Wei JJ, William J, Bulun S (2011) Endometriosis and ovarian cancer: a review of clinical, pathologic, and molecular aspects. Int J Gynecol Pathol 30(6):553–568. https://doi.org/10.1097/PGP.0b013e31821f4b85

    Article  PubMed  PubMed Central  Google Scholar 

  65. Pavone ME, Lyttle BM (2015) Endometriosis and ovarian cancer: links, risks, and challenges faced. Int J Womens Health 7:663–672. https://doi.org/10.2147/IJWH.S66824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Lagana AS, Colonese F, Colonese E, Sofo V, Salmeri FM, Granese R, Chiofalo B, Ciancimino L, Triolo O (2015) Cytogenetic analysis of epithelial ovarian cancer's stem cells: an overview on new diagnostic and therapeutic perspectives. Eur J Gynaecol Oncol 36(5):495–505

    CAS  PubMed  Google Scholar 

  67. Schuijer M, Berns EM (2003) TP53 and ovarian cancer. Hum Mutat 21(3):285–291. https://doi.org/10.1002/humu.10181

    Article  CAS  PubMed  Google Scholar 

  68. Matsumoto T, Yamazaki M, Takahashi H, Kajita S, Suzuki E, Tsuruta T, Saegusa M (2015) Distinct beta-catenin and PIK3CA mutation profiles in endometriosis-associated ovarian endometrioid and clear cell carcinomas. Am J Clin Pathol 144(3):452–463. https://doi.org/10.1309/AJCPZ5T2POOFMQVN

    Article  CAS  PubMed  Google Scholar 

  69. Ayhan A, Mao TL, Seckin T, Wu CH, Guan B, Ogawa H, Futagami M, Mizukami H, Yokoyama Y, Kurman RJ, Shih Ie M (2012) Loss of ARID1A expression is an early molecular event in tumor progression from ovarian endometriotic cyst to clear cell and endometrioid carcinoma. Int J Gynecol Cancer 22(8):1310–1315. https://doi.org/10.1097/IGC.0b013e31826b5dcc

    Article  PubMed  PubMed Central  Google Scholar 

  70. Xia Y, Xiong N, Huang Y (2018) Relationship between methylation status of RASSF2A gene promoter and endometriosis-associated ovarian cancer. J Biol Regul Homeost Agents 32(1):21–28

    CAS  PubMed  Google Scholar 

  71. Worley MJ Jr, Liu S, Hua Y, Kwok JS, Samuel A, Hou L, Shoni M, Lu S, Sandberg EM, Keryan A, Wu D, Ng SK, Kuo WP, Parra-Herran CE, Tsui SK, Welch W, Crum C, Berkowitz RS, Ng SW (2015) Molecular changes in endometriosis-associated ovarian clear cell carcinoma. Eur J Cancer 51(13):1831–1842. https://doi.org/10.1016/j.ejca.2015.05.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Govatati S, Kodati VL, Deenadayal M, Chakravarty B, Shivaji S, Bhanoori M (2014) Mutations in the PTEN tumor gene and risk of endometriosis: a case-control study. Hum Reprod 29(2):324–336. https://doi.org/10.1093/humrep/det387

    Article  CAS  PubMed  Google Scholar 

  73. Sato N, Tsunoda H, Nishida M, Morishita Y, Takimoto Y, Kubo T, Noguchi M (2000) Loss of heterozygosity on 10q2.33 and mutation of the tumor suppressor gene PTEN in benign endometrial cyst of the ovary: possible sequence progression from benign endometrial cyst to endometrioid carcinoma and clear cell carcinoma of the ovary. Cancer Res 60(24):7052–7056

    CAS  PubMed  Google Scholar 

  74. Ramaswamy S, Nakamura N, Vazquez F, Batt DB, Perera S, Roberts TM, Sellers WR (1999) Regulation of G1 progression by the PTEN tumor suppressor protein is linked to inhibition of the phosphatidylinositol 3-kinase/Akt pathway. Proc Natl Acad Sci USA 96(5):2110–2115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Anglesio MS, Bashashati A, Wang YK, Senz J, Ha G, Yang W, Aniba MR, Prentice LM, Farahani H, Li Chang H, Karnezis AN, Marra MA, Yong PJ, Hirst M, Gilks B, Shah SP, Huntsman DG (2015) Multifocal endometriotic lesions associated with cancer are clonal and carry a high mutation burden. J Pathol 236(2):201–209. https://doi.org/10.1002/path.4516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Anglesio MS, Papadopoulos N, Ayhan A, Nazeran TM, Noe M, Horlings HM, Lum A, Jones S, Senz J, Seckin T, Ho J, Wu RC, Lac V, Ogawa H, Tessier-Cloutier B, Alhassan R, Wang A, Wang Y, Cohen JD, Wong F, Hasanovic A, Orr N, Zhang M, Popoli M, McMahon W, Wood LD, Mattox A, Allaire C, Segars J, Williams C, Tomasetti C, Boyd N, Kinzler KW, Gilks CB, Diaz L, Wang TL, Vogelstein B, Yong PJ, Huntsman DG, Shih IM (2017) Cancer-associated mutations in endometriosis without cancer. N Engl J Med 376(19):1835–1848. https://doi.org/10.1056/NEJMoa1614814

    Article  PubMed  PubMed Central  Google Scholar 

  77. Burghaus S, Fasching PA, Haberle L, Rubner M, Buchner K, Blum S, Engel A, Ekici AB, Hartmann A, Hein A, Beckmann MW, Renner SP (2017) Genetic risk factors for ovarian cancer and their role for endometriosis risk. Gynecol Oncol 145(1):142–147. https://doi.org/10.1016/j.ygyno.2017.02.022

    Article  CAS  PubMed  Google Scholar 

  78. Maruyama T, Yoshimura Y (2012) Stem cell theory for the pathogenesis of endometriosis. Front Biosci (Elite Ed) 4:2754–2763

    Article  Google Scholar 

  79. Lagana AS, Vitale SG, Salmeri FM, Triolo O, Ban Frangez H, Vrtacnik-Bokal E, Stojanovska L, Apostolopoulos V, Granese R, Sofo V (2017) Unus pro omnibus, omnes pro uno: a novel, evidence-based, unifying theory for the pathogenesis of endometriosis. Med Hypotheses 103:10–20. https://doi.org/10.1016/j.mehy.2017.03.032

    Article  CAS  PubMed  Google Scholar 

  80. Lagana AS, Salmeri FM, Vitale SG, Triolo O, Gotte M (2018) Stem cell trafficking during endometriosis: may epigenetics play a pivotal role? Reprod Sci 25(7):978–979. https://doi.org/10.1177/1933719116687661

    Article  PubMed  Google Scholar 

  81. Masuda H, Matsuzaki Y, Hiratsu E, Ono M, Nagashima T, Kajitani T, Arase T, Oda H, Uchida H, Asada H, Ito M, Yoshimura Y, Maruyama T, Okano H (2010) Stem cell-like properties of the endometrial side population: implication in endometrial regeneration. PLoS ONE 5(4):e10387. https://doi.org/10.1371/journal.pone.0010387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Deane JA, Gualano RC, Gargett CE (2013) Regenerating endometrium from stem/progenitor cells: is it abnormal in endometriosis, Asherman's syndrome and infertility? Curr Opin Obstet Gynecol 25(3):193–200. https://doi.org/10.1097/GCO.0b013e32836024e7

    Article  PubMed  Google Scholar 

  83. Kralickova M, Vetvicka V (2015) Endometriosis: are stem cells involved? Int J Clin Exp Med Sci 1:65–69

    Article  Google Scholar 

  84. Cheng W, Liu J, Yoshida H, Rosen D, Naora H (2005) Lineage infidelity of epithelial ovarian cancers is controlled by HOX genes that specify regional identity in the reproductive tract. Nat Med 11(5):531–537. https://doi.org/10.1038/nm1230

    Article  CAS  PubMed  Google Scholar 

  85. Taylor HS, Vanden Heuvel GB, Igarashi P (1997) A conserved Hox axis in the mouse and human female reproductive system: late establishment and persistent adult expression of the Hoxa cluster genes. Biol Reprod 57(6):1338–1345

    Article  CAS  PubMed  Google Scholar 

  86. Bapat SA, Mali AM, Koppikar CB, Kurrey NK (2005) Stem and progenitor-like cells contribute to the aggressive behavior of human epithelial ovarian cancer. Cancer Res 65(8):3025–3029. https://doi.org/10.1158/0008-5472.CAN-04-3931

    Article  CAS  PubMed  Google Scholar 

  87. Taylor HS, Osteen KG, Bruner-Tran KL, Lockwood CJ, Krikun G, Sokalska A, Duleba AJ (2011) Novel therapies targeting endometriosis. Reprod Sci 18(9):814–823. https://doi.org/10.1177/1933719111410713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Pearce CL, Templeman C, Rossing MA, Lee A, Near AM, Webb PM, Nagle CM, Doherty JA, Cushing-Haugen KL, Wicklund KG, Chang-Claude J, Hein R, Lurie G, Wilkens LR, Carney ME, Goodman MT, Moysich K, Kjaer SK, Hogdall E, Jensen A, Goode EL, Fridley BL, Larson MC, Schildkraut JM, Palmieri RT, Cramer DW, Terry KL, Vitonis AF, Titus LJ, Ziogas A, Brewster W, Anton-Culver H, Gentry-Maharaj A, Ramus SJ, Anderson AR, Brueggmann D, Fasching PA, Gayther SA, Huntsman DG, Menon U, Ness RB, Pike MC, Risch H, Wu AH, Berchuck A (2012) Association between endometriosis and risk of histological subtypes of ovarian cancer: a pooled analysis of case–control studies. Lancet Oncol 13(4):385–394. https://doi.org/10.1016/S1470-2045(11)70404-1

    Article  PubMed  PubMed Central  Google Scholar 

  89. Iwabuchi T, Yoshimoto C, Shigetomi H, Kobayashi H (2015) Oxidative stress and antioxidant defense in endometriosis and its malignant transformation. Oxid Med Cell Longev 2015:848595. https://doi.org/10.1155/2015/848595

    Article  PubMed  PubMed Central  Google Scholar 

  90. Riccio LGC, Santulli P, Marcellin L, Abrao MS, Batteux F, Chapron C (2018) Immunology of endometriosis. Best Pract Res Clin Obstet Gynaecol 50:39–49. https://doi.org/10.1016/j.bpobgyn.2018.01.010

    Article  PubMed  Google Scholar 

  91. Dawson A, Fernandez ML, Anglesio M, Yong PJ, Carey MS (2018) Endometriosis and endometriosis-associated cancers: new insights into the molecular mechanisms of ovarian cancer development. Ecancermedicalscience 12:803. https://doi.org/10.3332/ecancer.2018.803

    Article  PubMed  PubMed Central  Google Scholar 

  92. Maniglio P, Ricciardi E, Lagana AS, Triolo O, Caserta D (2016) Epigenetic modifications of primordial reproductive tract: a common etiologic pathway for Mayer–Rokitansky–Kuster–Hauser Syndrome and endometriosis? Med Hypotheses 90:4–5. https://doi.org/10.1016/j.mehy.2016.02.015

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Histology and Embryology, Faculty of Medicine, Charles University, Plzen, Czech Republic

    Milena Králíčková

  2. Department of Obstetrics and Gynecology, University Hospital, Faculty of Medicine, Charles University, Plzen, Czech Republic

    Milena Králíčková

  3. Biomedical Centre, Faculty of Medicine in Plzen, Charles University, Plzen, Czech Republic

    Milena Králíčková

  4. Department of Obstetrics and Gynecology, Filippo Del Ponte Hospital, University of Insubria, Varese, Italy

    Antonio Simone Laganà & Fabio Ghezzi

  5. Department of Pathology, University of Louisville, Louisville, KY, 40292, USA

    Vaclav Vetvicka

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  1. Milena Králíčková
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  2. Antonio Simone Laganà
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  3. Fabio Ghezzi
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  4. Vaclav Vetvicka
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Králíčková, M., Laganà, A.S., Ghezzi, F. et al. Endometriosis and risk of ovarian cancer: what do we know?. Arch Gynecol Obstet 301, 1–10 (2020). https://doi.org/10.1007/s00404-019-05358-8

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