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Endometriosis and Endometriosis-Associated Tumors

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Gynecologic and Obstetric Pathology, Volume 2

Abstract

Endometriosis is a chronic gynecologic disorder that affects ~10% of adolescent girls and premenopausal women. The condition, classically defined as the presence of endometrial glands and stroma outside of the uterine cavity, is multifactorial and highly recurrent, and causes considerable morbidities that can significantly diminish the quality of life of affected women. The disease is linked to immune dysfunctions, infertility, and increased risk for ovarian and other cancers. The histological diagnosis of endometriosis, while typically uncomplicated, may be compromised by the heterogeneity of the endometriotic foci which can manifest a spectrum of lesions with distinct and atypical features of stromal and glandular components. Moreover, signs and symptoms of endometriosis remain nonspecific and there is a current lack of predictive noninvasive markers. This chapter aims to provide current understanding of the etiology, pathogenesis, and clinicopathologic features of endometriosis and to highlight the remaining challenges clinicians and pathologists face in the diagnosis, management of symptoms, and provision of care in women with this condition.

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References

  1. Burney RO, Giudice LC. Pathogenesis and pathophysiology of endometriosis. Fertil Steril. 2012;98:511–9.

    Article  CAS  PubMed  Google Scholar 

  2. Vercellini P, Vigano P, Somigliana E, Fedele L. Endometriosis: pathogenesis and treatment. Nat Rev Endocrinol. 2014;10:261–75.

    Article  CAS  PubMed  Google Scholar 

  3. Practice Committee of American Society for Reproductive Medicine. Multiple gestation associated with infertility therapy: an American Society for Reproductive Medicine Practice Committee opinion. Fertil Steril. 2012;97:825–34.

    Article  Google Scholar 

  4. Fuldeore M, Yang H, Du EX, et al. Healthcare utilization and costs in women diagnosed with endometriosis before and after diagnosis: a longitudinal analysis of claims databases. Fertil Steril. 2015;103:163–71.

    Article  PubMed  Google Scholar 

  5. Soliman AM, Yang H, Du EX, Kelley C, Winkel C. The direct and indirect costs associated with endometriosis: a systematic literature review. Hum Reprod. 2016;31:712–22.

    Article  PubMed  Google Scholar 

  6. Parasar P, Ozcan P, Terry KL. Endometriosis: epidemiology, diagnosis and clinical management. Curr Obstet Gynecol Rep. 2017;6:34–41.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Bedaiwy MA, Alfaraj S, Yong P, Casper R. New developments in the medical treatment of endometriosis. Fertil Steril. 2017;107:555–65.

    Article  CAS  PubMed  Google Scholar 

  8. Krishnamoorthy K, Decherney AH. Genetics of endometriosis. Clin Obstet Gynecol. 2017;60:531–8.

    Article  PubMed  Google Scholar 

  9. Jiang QY, Wu RJ. Growth mechanisms of endometriotic cells in implanted places: a review. Gynecol Endocrinol. 2012;28:562–7.

    Article  PubMed  Google Scholar 

  10. Smorgick N, Marsh CA, As-Sanie S, Smith YR, Quint EH. Prevalence of pain syndromes, mood conditions, and asthma in adolescents and young women with endometriosis. J Pediatr Adolesc Gynecol. 2013;26:171–5.

    Article  PubMed  Google Scholar 

  11. Sinaii N, Cleary SD, Ballweg ML, Nieman LK, Stratton P. High rates of autoimmune and endocrine disorders, fibromyalgia, chronic fatigue syndrome and atopic diseases among women with endometriosis: a survey analysis. Hum Reprod. 2002;17:2715–24.

    Article  CAS  PubMed  Google Scholar 

  12. Fassbender A, Burney RO, O DF, D’Hooghe T, Giudice L. Update on biomarkers for the detection of endometriosis. Biomed Res Int. 2015;2015:130854.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Somigliana E, Vigano P, Benaglia L, et al. Management of endometriosis in the infertile patient. Semin Reprod Med. 2017;35:31–7.

    PubMed  Google Scholar 

  14. Gemmell LC, Webster KE, Kirtley S, et al. The management of menopause in women with a history of endometriosis: a systematic review. Hum Reprod Update. 2017;23:481–500.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Wilbur MA, Shih IM, Segars JH, Fader AN. Cancer implications for patients with endometriosis. Semin Reprod Med. 2017;35:110–6.

    Article  CAS  PubMed  Google Scholar 

  16. Marchino GL, Gennarelli G, Enria R, et al. Diagnosis of pelvic endometriosis with use of macroscopic versus histologic findings. Fertil Steril. 2005;84:12–5.

    Article  PubMed  Google Scholar 

  17. Jansen RP, Russell P. Nonpigmented endometriosis: clinical, laparoscopic, and pathologic definition. Am J Obstet Gynecol. 1986;155:1154–9.

    Article  CAS  PubMed  Google Scholar 

  18. Albee RB Jr, Sinervo K, Fisher DT. Laparoscopic excision of lesions suggestive of endometriosis or otherwise atypical in appearance: relationship between visual findings and final histologic diagnosis. J Minim Invasive Gynecol. 2008;15:32–7.

    Article  PubMed  Google Scholar 

  19. Walter AJ, Hentz JG, Magtibay PM, Cornella JL, Magrina JF. Endometriosis: correlation between histologic and visual findings at laparoscopy. Am J Obstet Gynecol. 2001;184:1407–11; discussion 11–3

    Article  CAS  PubMed  Google Scholar 

  20. American Society for Reproductive Medicine. Revised American Society for Reproductive Medicine classification of endometriosis: 1996. Fertil Steril. 1997;67:817–21.

    Article  Google Scholar 

  21. Milingos S, Protopapas A, Drakakis P, et al. Laparoscopic management of patients with endometriosis and chronic pelvic pain. Ann N Y Acad Sci. 2003;997:269–73.

    Article  PubMed  Google Scholar 

  22. Johnson NP, Hummelshoj L, Adamson GD, et al. World Endometriosis Society consensus on the classification of endometriosis. Hum Reprod. 2017;32:315–24.

    Article  PubMed  Google Scholar 

  23. Hirsch M, Duffy JMN, Deguara CS, Davis CJ, Khan KS. Diagnostic accuracy of Cancer Antigen 125 (CA125) for endometriosis in symptomatic women: A multi-center study. Eur J Obstet Gynecol Reprod Biol. 2017;210:102–7.

    Article  CAS  PubMed  Google Scholar 

  24. Furuya M, Masuda H, Hara K, et al. ZEB1 expression is a potential indicator of invasive endometriosis. Acta Obstet Gynecol Scand. 2017;96:1128–35.

    Article  CAS  PubMed  Google Scholar 

  25. Gui B, Valentini AL, Ninivaggi V, et al. Shining light in a dark landscape: MRI evaluation of unusual localization of endometriosis. Diagn Interv Radiol. 2017;23:272–81.

    Article  PubMed  PubMed Central  Google Scholar 

  26. DiVasta AD, Vitonis AF, Laufer MR, Missmer SA. Spectrum of symptoms in women diagnosed with endometriosis during adolescence vs adulthood. Am J Obstet Gynecol. 2018;218:324 e1–e11.

    Article  Google Scholar 

  27. Mounsey AL, Wilgus A, Slawson DC. Diagnosis and management of endometriosis. Am Fam Physician. 2006;74:594–600.

    PubMed  Google Scholar 

  28. Nisenblat V, Bossuyt PM, Shaikh R, et al. Blood biomarkers for the non-invasive diagnosis of endometriosis. Cochrane Database Syst Rev. 2016;5:CD012179.

    Google Scholar 

  29. Seeber B, Sammel MD, Fan X, et al. Panel of markers can accurately predict endometriosis in a subset of patients. Fertil Steril. 2008;89:1073–81.

    Article  CAS  PubMed  Google Scholar 

  30. Drosdzol-Cop A, Skrzypulec-Plinta V. Selected cytokines and glycodelin A levels in serum and peritoneal fluid in girls with endometriosis. J Obstet Gynaecol Res. 2012;38:1245–53.

    Article  CAS  PubMed  Google Scholar 

  31. Seifer BJ, Su D, Taylor HS. Circulating miRNAs in murine experimental endometriosis. Reprod Sci. 2017;24:376–81.

    Article  CAS  PubMed  Google Scholar 

  32. Wang W-T, Zhao Y-N, Han B-W, Hong S-J, Chen Y-Q. Circulating microRNAs identified in a genome-wide serum microRNA expression analysis as noninvasive biomarkers for endometriosis. J Clin Endocrinol Metab. 2013;98:281–9.

    Article  CAS  PubMed  Google Scholar 

  33. Fritz MA, Speroff L. Clinical gynecologic endocrinology and infertility. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins; 2011.

    Google Scholar 

  34. Schenken RS. Endometriosis: pathogenesis, clinical features, and diagnosis. Waltham, MA: Walters Kluwer Health; 2016.

    Google Scholar 

  35. Sourial S, Tempest N, Hapangama DK. Theories on the pathogenesis of endometriosis. Int J Reprod Med. 2014;2014:9.

    Article  Google Scholar 

  36. D’Hooghe TM, Bambra CS, Suleman MA, et al. Development of a model of retrograde menstruation in baboons (Papio anubis). Fertil Steril. 1994;62:635–8.

    Article  PubMed  Google Scholar 

  37. Dehoux JP, Defrere S, Squifflet J, et al. Is the baboon model appropriate for endometriosis studies? Fertil Steril. 2011;96:728–33 e3.

    Article  PubMed  Google Scholar 

  38. Song X, Zhu L, Ding J, Xu T, Lang J. Clinical characteristics of congenital cervical atresia and associated endometriosis among 96 patients. Int J Gynaecol Obstet. 2016;134:252–5.

    Article  PubMed  Google Scholar 

  39. Sasson IE, Taylor HS. Stem cells and the pathogenesis of endometriosis. Ann N Y Acad Sci. 2008;1127:106–15.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Halme J, Hammond MG, Hulka JF, Raj SG, Talbert LM. Retrograde menstruation in healthy women and in patients with endometriosis. Obstet Gynecol. 1984;64:151–4.

    CAS  PubMed  Google Scholar 

  41. Hufnagel D, Li F, Cosar E, et al. The role of stem cells in the etiology and pathophysiology of endometriosis. Semin Reprod Med. 2015;33:333–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Vinatier D, Orazi G, Cosson M, Dufour P. Theories of endometriosis. Eur J Obstet Gynecol Reprod Biol. 2001;96:21–34.

    Article  CAS  PubMed  Google Scholar 

  43. Matsumoto T, Yamazaki M, Takahashi H, et al. Distinct β-catenin and PIK3CA mutation profiles in endometriosis-associated ovarian endometrioid and clear cell carcinomas. Am J Clin Pathol. 2015;144:452–63.

    Article  CAS  PubMed  Google Scholar 

  44. Troncon JK, Zani AC, Vieira AD, et al. Endometriosis in a patient with Mayer-Rokitansky-Kuster-Hauser syndrome. Case Rep Obstet Gynecol. 2014;2014:376231.

    PubMed  PubMed Central  Google Scholar 

  45. Mok-Lin EY, Wolfberg A, Hollinquist H, Laufer MR. Endometriosis in a patient with Mayer-Rokitansky-Kuster-Hauser syndrome and complete uterine agenesis: evidence to support the theory of coelomic metaplasia. J Pediatr Adolesc Gynecol. 2010;23:e35–7.

    Article  PubMed  Google Scholar 

  46. Cho MK, Kim CH, Oh ST. Endometriosis in a patient with Rokitansky-Kuster-Hauser syndrome. J Obstet Gynaecol Res. 2009;35:994–6.

    Article  PubMed  Google Scholar 

  47. Pluchino N, Taylor HS. Endometriosis and stem cell trafficking. Reprod Sci. 2016;23:1616–9.

    Article  CAS  PubMed  Google Scholar 

  48. Wang Y, Mang M, Wang Y, et al. Tubal origin of ovarian endometriosis and clear cell and endometrioid carcinoma. Am J Cancer Res. 2015;5:869–79.

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Zheng W, Li N, Wang J, et al. Initial endometriosis showing direct morphologic evidence of metaplasia in the pathogenesis of ovarian endometriosis. Int J Gynecol Pathol. 2005;24:164–72.

    Article  PubMed  Google Scholar 

  50. Li J, Abushahin N, Pang S, et al. Tubal origin of ‘ovarian’ low-grade serous carcinoma. Mod Pathol. 2011;24:1488.

    Article  CAS  PubMed  Google Scholar 

  51. Yuan Z, Wang L, Wang Y, et al. Tubal origin of ovarian endometriosis. Mod Pathol. 2014;27:1154–62.

    Article  CAS  PubMed  Google Scholar 

  52. Corzo C, Iniesta MD, Patrono MG, Lu KH, Ramirez PT. Role of fallopian tubes in the development of ovarian cancer. J Minim Invasive Gynecol. 2017;24:230–4.

    Article  PubMed  Google Scholar 

  53. Erickson BK, Conner MG, Landen CN Jr. The role of the fallopian tube in the origin of ovarian cancer. Am J Obstet Gynecol. 2013;209:409–14.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Li J, Fadare O, Xiang L, Kong B, Zheng W. Ovarian serous carcinoma: recent concepts on its origin and carcinogenesis. J Hematol Oncol. 2012;5:8.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Long Roche KC, Abu-Rustum NR, Nourmoussavi M, Zivanovic O. Risk-reducing salpingectomy: let us be opportunistic. Cancer. 2017;123:1714–20.

    Article  CAS  PubMed  Google Scholar 

  56. Walker JL, Powell CB, Chen LM, et al. Society of Gynecologic Oncology recommendations for the prevention of ovarian cancer. Cancer. 2015;121:2108–20.

    Article  PubMed  Google Scholar 

  57. Perez-Lopez FR, Ceausu I, Depypere H, et al. Interventions to reduce the risk of ovarian and fallopian tube cancer: A European Menopause and Andropause Society Position Statement. Maturitas. 2017;100:86–91.

    Article  PubMed  Google Scholar 

  58. Aghajanova L, Giudice LC. Molecular evidence for differences in endometrium in severe versus mild endometriosis. Reprod Sci. 2011;18:229–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Pabona JM, Simmen FA, Nikiforov MA, et al. Kruppel-like factor 9 and progesterone receptor coregulation of decidualizing endometrial stromal cells: implications for the pathogenesis of endometriosis. J Clin Endocrinol Metab. 2012;97:E376–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Fassbender A, Verbeeck N, Bornigen D, et al. Combined mRNA microarray and proteomic analysis of eutopic endometrium of women with and without endometriosis. Hum Reprod. 2012;27:2020–9.

    Article  CAS  PubMed  Google Scholar 

  61. Tamaresis JS, Irwin JC, Goldfien GA, et al. Molecular classification of endometriosis and disease stage using high-dimensional genomic data. Endocrinology. 2014;155:4986–99.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Browne H, Taylor H. HOXA10 expression in ectopic endometrial tissue. Fertil Steril. 2006;85:1386–90.

    Article  CAS  PubMed  Google Scholar 

  63. Fang Z, Yang S, Gurates B, et al. Genetic or enzymatic disruption of aromatase inhibits the growth of ectopic uterine tissue. J Clin Endocrinol Metab. 2002;87:3460–6.

    Article  CAS  PubMed  Google Scholar 

  64. Bulun SE, Zeitoun KM, Takayama K, Sasano H. Estrogen biosynthesis in endometriosis: molecular basis and clinical relevance. J Mol Endocrinol. 2000;25:35–42.

    Article  CAS  PubMed  Google Scholar 

  65. Han SJ, Hawkins SM, Begum K, et al. A new isoform of steroid receptor coactivator-1 is crucial for pathogenic progression of endometriosis. Nat Med. 2012;18:1102–11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Lin SC, Li YH, Wu MH, et al. Suppression of COUP-TFII by proinflammatory cytokines contributes to the pathogenesis of endometriosis. J Clin Endocrinol Metab. 2014;99:E427–37.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Yu J, Boicea A, Barrett KL, et al. Reduced connexin 43 in eutopic endometrium and cultured endometrial stromal cells from subjects with endometriosis. Mol Hum Reprod. 2014;20:260–70.

    Article  CAS  PubMed  Google Scholar 

  68. Heard ME, Simmons CD, Simmen FA, Simmen RC. Kruppel-like factor 9 deficiency in uterine endometrial cells promotes ectopic lesion establishment associated with activated notch and hedgehog signaling in a mouse model of endometriosis. Endocrinology. 2014;155:1532–46.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  69. Zhao Y, Chen Y, Kuang Y, et al. Multiple Beneficial roles of repressor of estrogen receptor activity (REA) in suppressing the progression of endometriosis. Endocrinology. 2016;157:900–12.

    Article  CAS  PubMed  Google Scholar 

  70. Lv J, Zhu Q, Jia X, Yu N, Li Q. In vitro and in vivo effects of tumor suppressor gene PTEN on endometriosis: an experimental study. Med Sci Monit. 2016;22:3727–36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Govatati S, Kodati VL, Deenadayal M, et al. Mutations in the PTEN tumor gene and risk of endometriosis: a case-control study. Hum Reprod. 2014;29:324–36.

    Article  CAS  PubMed  Google Scholar 

  72. Yoo JY, Kim TH, Fazleabas AT, et al. KRAS activation and over-expression of SIRT1/BCL6 contributes to the pathogenesis of endometriosis and progesterone resistance. Sci Rep. 2017;7:6765.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  73. Naqvi H, Ilagan Y, Krikun G, Taylor HS. Altered genome-wide methylation in endometriosis. Reprod Sci. 2014;21:1237–43.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Houshdaran S, Nezhat CR, Vo KC, et al. Aberrant endometrial DNA methylome and associated gene expression in women with endometriosis. Biol Reprod. 2016;95:93.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  75. Anglesio MS, Papadopoulos N, Ayhan A, et al. Cancer-associated mutations in endometriosis without cancer. N Engl J Med. 2017;376:1835–48.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Zondervan KT, Rahmioglu N, Morris AP, et al. Beyond endometriosis genome-wide association study: from genomics to phenomics to the patient. Semin Reprod Med. 2016;34:242–54.

    Article  PubMed  PubMed Central  Google Scholar 

  77. Bulun SE, Monsavais D, Pavone ME, et al. Role of estrogen receptor-beta in endometriosis. Semin Reprod Med. 2012;30:39–45.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Han SJ, Jung SY, Wu SP, et al. Estrogen receptor beta modulates apoptosis complexes and the inflammasome to drive the pathogenesis of endometriosis. Cell. 2015;163:960–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Simmen RC, Kelley AS. Reversal of fortune: estrogen receptor-beta in endometriosis. J Mol Endocrinol. 2016;57:F23–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Al-Sabbagh M, Lam EW, Brosens JJ. Mechanisms of endometrial progesterone resistance. Mol Cell Endocrinol. 2012;358:208–15.

    Article  CAS  PubMed  Google Scholar 

  81. Grandi G, Mueller MD, Papadia A, et al. Inflammation influences steroid hormone receptors targeted by progestins in endometrial stromal cells from women with endometriosis. J Reprod Immunol. 2016;117:30–8.

    Article  CAS  PubMed  Google Scholar 

  82. Tosti C, Biscione A, Morgante G, et al. Hormonal therapy for endometriosis: from molecular research to bedside. Eur J Obstet Gynecol Reprod Biol. 2017;209:61–6.

    Article  CAS  PubMed  Google Scholar 

  83. Donnez J, Taylor RN, Taylor HS. Partial suppression of estradiol: a new strategy in endometriosis management? Fertil Steril. 2017;107:568–70.

    Article  PubMed  Google Scholar 

  84. Taylor HS, Giudice LC, Lessey BA, et al. Treatment of endometriosis-associated pain with elagolix, an oral GnRH antagonist. N Engl J Med. 2017;377:28–40.

    Article  CAS  PubMed  Google Scholar 

  85. Matalliotakis I, Cakmak H, Matalliotakis M, Kappou D, Arici A. High rate of allergies among women with endometriosis. J Obstet Gynaecol. 2012;32:291–3.

    Article  CAS  PubMed  Google Scholar 

  86. Harris HR, Costenbader KH, Mu F, et al. Endometriosis and the risks of systemic lupus erythematosus and rheumatoid arthritis in the Nurses’ Health Study II. Ann Rheum Dis. 2016;75:1279–84.

    Article  CAS  PubMed  Google Scholar 

  87. Ahn SH, Khalaj K, Young SL, et al. Immune-inflammation gene signatures in endometriosis patients. Fertil Steril. 2016;106:1420–31 e7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Monsanto SP, Edwards AK, Zhou J, et al. Surgical removal of endometriotic lesions alters local and systemic proinflammatory cytokines in endometriosis patients. Fertil Steril. 2016;105:968–77 e5.

    Article  CAS  PubMed  Google Scholar 

  89. Burns KA, Thomas SY, Hamilton KJ, et al. Early endometriosis in females is directed by immune-mediated estrogen receptor alpha and IL-6 cross-talk. Endocrinology. 2018;159:103–18.

    Article  PubMed  Google Scholar 

  90. Greaves E, Temp J, Esnal-Zufiurre A, et al. Estradiol is a critical mediator of macrophage-nerve cross talk in peritoneal endometriosis. Am J Pathol. 2015;185:2286–97.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Zhao Y, Gong P, Chen Y, et al. Dual suppression of estrogenic and inflammatory activities for targeting of endometriosis. Sci Transl Med. 2015;7:271ra9.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  92. Grandi G, Mueller M, Bersinger N, et al. Progestin suppressed inflammation and cell viability of tumor necrosis factor-alpha-stimulated endometriotic stromal cells. Am J Reprod Immunol. 2016;76:292–8.

    Article  CAS  PubMed  Google Scholar 

  93. Ahmad SF, Akoum A, Horne AW. Selective modulation of the prostaglandin F2alpha pathway markedly impacts on endometriosis progression in a xenograft mouse model. Mol Hum Reprod. 2015;21:905–16.

    Article  CAS  PubMed  Google Scholar 

  94. Rudzitis-Auth J, Menger MD, Laschke MW. Resveratrol is a potent inhibitor of vascularization and cell proliferation in experimental endometriosis. Hum Reprod. 2013;28:1339–47.

    Article  CAS  PubMed  Google Scholar 

  95. Taguchi A, Wada-Hiraike O, Kawana K, et al. Resveratrol suppresses inflammatory responses in endometrial stromal cells derived from endometriosis: a possible role of the sirtuin 1 pathway. J Obstet Gynaecol Res. 2014;40:770–8.

    Article  CAS  PubMed  Google Scholar 

  96. Mendes da Silva D, Gross LA, Neto EPG, Lessey BA, Savaris RF. The use of resveratrol as an adjuvant treatment of pain in endometriosis: a randomized clinical trial. J Endocr Soc. 2017;1:359–69.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  97. Nezhat C, Li A, Falik R, et al. Bowel endometriosis: diagnosis and management. Am J Obstet Gynecol. 2017;218(6):549–62.

    Article  PubMed  Google Scholar 

  98. Jaiman S, Gundabattula SR, Pochiraju M, Sangireddy JR. Polypoid endometriosis of the cervix: a case report and review of the literature. Arch Gynecol Obstet. 2014;289:915–20.

    Article  PubMed  Google Scholar 

  99. Benacerraf BR, Groszmann Y, Hornstein MD, Bromley B. Deep infiltrating endometriosis of the bowel wall: the comet sign. J Ultrasound Med. 2015;34:537–42.

    Article  PubMed  Google Scholar 

  100. Yantiss RK, Clement PB, Young RH. Endometriosis of the intestinal tract: a study of 44 cases of a disease that may cause diverse challenges in clinical and pathologic evaluation. Am J Surg Pathol. 2001;25:445–54.

    Article  CAS  PubMed  Google Scholar 

  101. Nezhat C, Kazerooni T, Berker B, et al. Laparoscopic management of hepatic endometriosis: report of two cases and review of the literature. J Minim Invasive Gynecol. 2005;12:196–200.

    Article  PubMed  Google Scholar 

  102. Seval MM, Cavkaytar S, Atak Z, Guresci S. Postcoital bleeding due to cervical endometriosis. BMJ Case Rep. 2013;2013

    Google Scholar 

  103. Hensen JH, Van Breda Vriesman AC, Puylaert JB. Abdominal wall endometriosis: clinical presentation and imaging features with emphasis on sonography. AJR Am J Roentgenol. 2006;186:616–20.

    Article  PubMed  Google Scholar 

  104. Koninckx PR, Ussia A, Adamyan L, et al. Deep endometriosis: definition, diagnosis, and treatment. Fertil Steril. 2012;98:564–71.

    Article  PubMed  Google Scholar 

  105. Tosti C, Pinzauti S, Santulli P, et al. Pathogenetic mechanisms of deep infiltrating endometriosis. Reprod Sci. 2015;22:1053–9.

    Article  CAS  PubMed  Google Scholar 

  106. Redwine DB. Diaphragmatic endometriosis: diagnosis, surgical management, and long-term results of treatment. Fertil Steril. 2002;77:288–96.

    Article  PubMed  Google Scholar 

  107. Nezhat C, Main J, Paka C, et al. Multidisciplinary treatment for thoracic and abdominopelvic endometriosis. JSLS. 2014;18:e2014.00312.

    Article  PubMed  PubMed Central  Google Scholar 

  108. Parker RL, Dadmanesh F, Young RH, Clement PB. Polypoid endometriosis: a clinicopathologic analysis of 24 cases and a review of the literature. Am J Surg Pathol. 2004;28:285–97.

    Article  PubMed  Google Scholar 

  109. Stewart CJ, Bharat C. Clinicopathological and immunohistological features of polypoid endometriosis. Histopathology. 2016;68:398–404.

    Article  PubMed  Google Scholar 

  110. Syrcle S, Pelch K, Schroder A, et al. Altered gene expression profile in vaginal polypoid endometriosis resembles peritoneal endometriosis and is consistent with increased local estrogen production. Gynecol Obstet Investig. 2011;71:77–86.

    Article  CAS  Google Scholar 

  111. Boyle DP, McCluggage WG. Peritoneal stromal endometriosis: a detailed morphological analysis of a large series of cases of a common and under-recognised form of endometriosis. J Clin Pathol. 2009;62:530–3.

    Article  CAS  PubMed  Google Scholar 

  112. Clement PB. The pathology of endometriosis: a survey of the many faces of a common disease emphasizing diagnostic pitfalls and unusual and newly appreciated aspects. Adv Anat Pathol. 2007;14:241–60.

    Article  PubMed  Google Scholar 

  113. Wei JJ, William J, Bulun S. Endometriosis and ovarian cancer: a review of clinical, pathologic, and molecular aspects. Int J Gynecol Pathol. 2011;30:553–68.

    Article  PubMed  PubMed Central  Google Scholar 

  114. Ogi Y, Yamaguchi T, Kinugasa Y, et al. A case of small intestinal endometrioid adenocarcinoma. Surg Case Rep. 2016;2:97.

    Article  PubMed  PubMed Central  Google Scholar 

  115. Scott RB. Malignant changes in endometriosis. Obstet Gynecol. 1953;2:283–9.

    CAS  PubMed  Google Scholar 

  116. Krawczyk N, Banys-Paluchowski M, Schmidt D, Ulrich U, Fehm T. Endometriosis-associated malignancy. Geburtshilfe Frauenheilkd. 2016;76:176–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Karpathiou G, Chauleur C, Corsini T, et al. Seromucinous ovarian tumor. A comparison with the rest of ovarian epithelial tumors. Ann Diagn Pathol. 2017;27:28–33.

    Article  PubMed  Google Scholar 

  118. Somigliana E, Parazzini F, Stoppelli S, 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 

  119. Schnack TH, Høgdall E, Thomsen LN, Høgdall C. Demographic, clinical, and prognostic factors of ovarian clear cell adenocarcinomas according to endometriosis status. Int J Gynecol Cancer. 2017;27:1804–12.

    Article  PubMed  Google Scholar 

  120. Park J-Y, Kim D-Y, Suh D-S, et al. Significance of ovarian endometriosis on the prognosis of ovarian clear cell carcinoma. Int J Gynecol Cancer. 2018;28:11–8.

    Article  PubMed  Google Scholar 

  121. Kim SI, Lee JW, Lee M, et al. Genomic landscape of ovarian clear cell carcinoma via whole exome sequencing. Gynecol Oncol. 2018;148:375–82.

    Article  CAS  PubMed  Google Scholar 

  122. Czernobilsky B, Morris WJ. A histologic study of ovarian endometriosis with emphasis on hyperplastic and atypical changes. Obstet Gynecol. 1979;53:318–23.

    CAS  PubMed  Google Scholar 

  123. Fukunaga M, Nomura K, Ishikawa E, Ushigome S. Ovarian atypical endometriosis: its close association with malignant epithelial tumours. Histopathology. 1997;30:249–55.

    Article  CAS  PubMed  Google Scholar 

  124. Terada T. Endometrioid adenocarcinoma of the ovary arising in atypical endometriosis. Int J Clin Exp Pathol. 2012;5:924–7.

    PubMed  PubMed Central  Google Scholar 

  125. Moll UM, Chumas JC, Chalas E, Mann WJ. Ovarian carcinoma arising in atypical endometriosis. Obstet Gynecol. 1990;75:537–9.

    CAS  PubMed  Google Scholar 

  126. Tanase Y, Furukawa N, Kobayashi H, Matsumoto T. Malignant transformation from endometriosis to atypical endometriosis and finally to endometrioid adenocarcinoma within 10 years. Case Rep Oncol. 2013;6:480–4.

    Article  PubMed  PubMed Central  Google Scholar 

  127. 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  PubMed Central  Google Scholar 

  128. Ayhan A, Mao T-L, Seckin T, et al. 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. 2012;22:1310.

    Article  PubMed  PubMed Central  Google Scholar 

  129. Yamamoto S, Tsuda H, Takano M, et al. Loss of ARID1A protein expression occurs as an early event in ovarian clear-cell carcinoma development and frequently coexists with PIK3CA mutations. Mod Pathol. 2012;25:615.

    Article  CAS  PubMed  Google Scholar 

  130. Lakshminarasimhan R, Andreu-Vieyra C, Lawrenson K, et al. Down-regulation of ARID1A is sufficient to initiate neoplastic transformation along with epigenetic reprogramming in non-tumorigenic endometriotic cells. Cancer Lett. 2017;401:11–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Chene G, Ouellet V, Rahimi K, et al. The ARID1A pathway in ovarian clear cell and endometrioid carcinoma, contiguous endometriosis, and benign endometriosis. Int J Gynaecol Obstet. 2015;130:27–30.

    Article  CAS  PubMed  Google Scholar 

  132. Stamp JP, Gilks CB, Wesseling M, et al. BAF250a expression in atypical endometriosis and endometriosis-associated ovarian cancer. Int J Gynecol Cancer. 2016;26:825–32.

    Article  PubMed  Google Scholar 

  133. Er TK, Su YF, Wu CC, et al. Targeted next-generation sequencing for molecular diagnosis of endometriosis-associated ovarian cancer. J Mol Med. 2016;94:835–47.

    Article  CAS  PubMed  Google Scholar 

  134. Cochrane DR, Tessier-Cloutier B, Lawrence KM, et al. Clear cell and endometrioid carcinomas: are their differences attributable to distinct cells of origin? J Pathol. 2017;243:26–36.

    Article  CAS  PubMed  Google Scholar 

  135. Blanco LZ Jr, Kuhn E, Morrison JC, et al. Steroid hormone synthesis by the ovarian stroma surrounding epithelial ovarian tumors: a potential mechanism in ovarian tumorigenesis. Mod Pathol. 2017;30:563–76.

    Article  CAS  PubMed  Google Scholar 

  136. Taylor J, McCluggage WG. Ovarian seromucinous carcinoma: report of a series of a newly categorized and uncommon neoplasm. Am J Surg Pathol. 2015;39:983–92.

    Article  PubMed  Google Scholar 

  137. Wu CH, Mao TL, Vang R, et al. Endocervical-type mucinous borderline tumors are related to endometrioid tumors based on mutation and loss of expression of ARID1A. Int J Gynecol Pathol. 2012;31:297–303.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Hauptmann S, Friedrich K, Redline R, Avril S. Ovarian borderline tumors in the 2014 WHO classification: evolving concepts and diagnostic criteria. Virchows Arch. 2017;470:125–42.

    Article  CAS  PubMed  Google Scholar 

  139. Akbarzadeh-Jahromi M, Shekarkhar G, Sari Aslani F, et al. Prevalence of endometriosis in malignant epithelial ovarian tumor. Arch Iran Med. 2015;18:844–8.

    PubMed  Google Scholar 

  140. Buis CC, van Leeuwen FE, Mooij TM, et al. Increased risk for ovarian cancer and borderline ovarian tumours in subfertile women with endometriosis. Hum Reprod. 2013;28:3358–69.

    Article  CAS  PubMed  Google Scholar 

  141. 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  PubMed Central  Google Scholar 

  142. Liu H, Leng J, Lang J, Cui Q. Clear cell carcinoma arising from abdominal wall endometriosis: a unique case with bladder and lymph node metastasis. World J Surg Oncol. 2014;12:51.

    Article  PubMed  PubMed Central  Google Scholar 

  143. Ferrandina G, Palluzzi E, Fanfani F, et al. Endometriosis-associated clear cell carcinoma arising in caesarean section scar: a case report and review of the literature. World J Surg Oncol. 2016;14:300.

    Article  PubMed  PubMed Central  Google Scholar 

  144. Mederos MA, Villafañe N, Dhingra S, et al. Pancreatic endometrial cyst mimics mucinous cystic neoplasm of the pancreas. World J Gastroenterol. 2017;23:1113.

    Article  PubMed  PubMed Central  Google Scholar 

  145. Klingbeil KD, Azab B, Moller MG. Low-grade appendiceal mucinous neoplasm and endometriosis of the appendix. World J Surg Oncol. 2017;15:226.

    Article  PubMed  PubMed Central  Google Scholar 

  146. Kilzieh R, Rakislova N, Torné A, et al. Endometrial stromal sarcoma arising in colorectal endometriosis. Int J Gynecol Pathol. 2017;36:433–7.

    Article  PubMed  Google Scholar 

  147. Cozzolino M, Nasioudis D, Sisti G, Coccia ME. Malignant transformation of vaginal endometriosis—a review of literature. Gynecol Obstet Investig. 2017;82:105–12.

    Article  Google Scholar 

  148. Hashiguchi M, Kai K, Nishiyama S, et al. Clear cell carcinoma of the uterine cervix presented as a submucosal tumor arising in a background of cervical endometriosis. Int J Gynecol Pathol. 2018;37:88–92.

    PubMed  Google Scholar 

  149. Tarumi Y, Mori T, Kusuki I, et al. Endometrioid adenocarcinoma arising from deep infiltrating endometriosis involving the bladder: a case report and review of the literature. Gynecol Oncol Rep. 2015;13:68.

    Article  PubMed  PubMed Central  Google Scholar 

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Simmen, R.C.M., Quick, C.M., Kelley, A.S., Zheng, W. (2019). Endometriosis and Endometriosis-Associated Tumors. In: Zheng, W., Fadare, O., Quick, C., Shen, D., Guo, D. (eds) Gynecologic and Obstetric Pathology, Volume 2. Springer, Singapore. https://doi.org/10.1007/978-981-13-3019-3_12

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