DOI QR코드

DOI QR Code

Endometriosis, Leiomyoma and Adenomyosis: the Risk of Gynecologic Malignancy

  • Verit, Fatma Ferda (Department of Obstetrics and Gynecology, Research and Training Hospital, Infertility Research and Treatment Center) ;
  • Yucel, Oguz (Department of Obstetrics and Gynecology, Research and Training Hospital, Infertility Research and Treatment Center)
  • Published : 2013.10.30

Abstract

The aim of this review article was to evaluate the relationship and the possible etiological mechanisms between endometriosis, leiomyoma (LM) and adenomyosis and gynecological cancers, such as ovarian and endometrial cancer and leiomyosarcoma (LMS). MEDLINE was searched for all articles written in the English literature from July 1966 to May 2013. Reports were collected systematically and all the references were also reviewed. Malignant transformation of gynecologic benign diseases such as endometriosis, adenomyosis and LM to ovarian and endometrial cancer remains unclear. Hormonal factors, inflammation, familial predisposition, genetic alterations, growth factors, diet, altered immune system, environmental factors and oxidative stress may be causative factors in carcinogenesis. Early menarche, low parity, late menopause and infertility have also been implicated in the pathogenesis of these cancers. Ovarian cancers and endometriosis have been shown to have common genetic alterations such as loss of heterozygosity (LOH), PTEN, p53, ARID1A mutations. MicroRNAs have also been implicated in malignant transformation. Inflammation releases proinflammatory cytokines, and activates tumor associated macrophages (TAMS) and nuclear factor kappa b (NF-KB) signaling pathways that promote genetic mutations and carcinogenesis. MED12 mutations in LM and smooth muscle tumors of undetermined malignant potential (STUMP) may contribute to malignant transformation to LMS. A hyperestrogenic state may be shared in common with pathogenesis of adenomyosis, LM and endometrial cancer. However, the effect of these benign gynecologic diseases on endometrial cancer should be studied in detail. This review study indicates that endometriosis, LM, adenomyosis may be associated with increased risk of gynecological cancers such as endometrial and ovarian cancers. The patients who have these gynecological benign diseases should be counseled about the future risks of developing cancer. Further studies are needed to investigate the relationship between STUMPs, LMS and LM and characteristics and outcome endometrial carcinoma in adenomyotic patients.

Keywords

Endometriosis;adenomyosis;leiomyoma;gynecologic cancers

References

  1. Aris A (2010). Endometriosis-associated ovarian cancer: a ten-year cohort study of women living in the estrie region of Quebec, Canada. J Ovarian Res, 3, 2. https://doi.org/10.1186/1757-2215-3-2
  2. Abushahin N, Zhang T, Chiang S, et al (2011). Serous endometrial intraepithelial carcinoma arising in adenomyosis: a report of 5 cases. Int J Gynecol Pathol, 30, 271-81.
  3. Ali-Fehmi R, Khalifeh I, Bandyopadhyay S, et al (2006). Patterns of loss of heterozygosity at 10q23.3 and microsatellite instability in endometriosis, atypical endometriosis, and ovarian carcinoma arising in association with endometriosis. Int J Gynecol Pathol, 25, 223-9. https://doi.org/10.1097/01.pgp.0000192274.44061.36
  4. Atkins KA, Arronte N, Darus CJ, Rice LW (2008). The use of p16 in enhancing the histologic classification of uterine smooth muscle tumors. Am J Surg Pathol, 32, 98-102. https://doi.org/10.1097/PAS.0b013e3181574d1e
  5. Attar E, Tokunaga H, Imir G, et al (2009). Prostaglandin E2 via steroidogenic factor-1 coordinately regulates transcription of steroidogenic genes necessary for estrogen synthesis in endometriosis. J Clin Endocrinol Metab, 94, 623-31. https://doi.org/10.1210/jc.2008-1180
  6. Borgfeldt C, Andolf E (2004). Cancer risk after hospital discharge diagnosis of benign ovarian cysts and endometriosis. Acta Obstet Gynecol Scand, 83, 395-400. https://doi.org/10.1080/j.0001-6349.2004.00305.x
  7. Bernard H, Garmy-Susini B, Ainaoui N, et al (2013). The p53 isoform, ${\Delta}133p53{\alpha}$, stimulates angiogenesis and tumour progression. Oncogene, 32, 2150-60. https://doi.org/10.1038/onc.2012.242
  8. Birrer MJ (2010). The origin of ovarian cancer-is it getting clearer? N Engl J Med, 363, 1574-5. https://doi.org/10.1056/NEJMe1009527
  9. Boes AS, Tousseyn T, Vandenput I, et al (2011). Pitfall in the diagnosis of endometrial cancer: case report of an endometrioid adenocarcinoma arising from uterine adenomyosis. Eur J Gynaecol Oncol, 32, 431-4.
  10. 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, 572-9. https://doi.org/10.1016/S0002-9378(97)70550-7
  11. Brinton LA, Lamb EJ, Moghissi KS, et al (2004). Ovarian cancer risk associated with varying causes of infertility. Fertil Steril, 82, 405-14. https://doi.org/10.1016/j.fertnstert.2004.02.109
  12. Brinton LA, Sakoda LC, Sherman ME, et al (2005a). Relationship of benign gynecologic diseases to subsequent risk of ovarian and uterine tumors. Cancer Epidemiol Biomarkers Prev, 14, 2929-35. https://doi.org/10.1158/1055-9965.EPI-05-0394
  13. Brinton LA,Westhoff CL, Scoccia B, et al (2005b). Causes of infertility as predictors of subsequent cancer risk. Epidemiol, 16, 500-7. https://doi.org/10.1097/01.ede.0000164812.02181.d5
  14. Budiu RA, Mantia-Smaldone G, Elishaev E, et al (2011). Soluble MUC1 and serum MUC1-specific antibodies are potential prognostic biomarkers for platinum-resistant ovarian cancer. Cancer Immunol Immunother, 60, 975-84. https://doi.org/10.1007/s00262-011-1010-x
  15. Bukulmez O, Hardy DB, Carr BR, Word RA, Mendelson CR (2008). Inflammatory status influences aromatase and steroid receptor expression in endometriosis. Endocrinol, 149, 1190-204. https://doi.org/10.1210/en.2007-0665
  16. Conaway RC, Conaway JW (2011). Function and regulation of the Mediator complex. Curr Opin Genet Dev, 21, 225-30. https://doi.org/10.1016/j.gde.2011.01.013
  17. Bulun SE, Lin Z, Imir G, et al (2005). Regulation of aromatase expression in estrogen-responsive breast and uterine disease: from bench to treatment. Pharmacol Rev Sep, 57, 359-83. https://doi.org/10.1124/pr.57.3.6
  18. Carli C, Metz CN, Al-Abed Y, Naccache PH, Akoum A (2009). Up-regulation of cyclooxygenase-2 expression and prostaglandin E2 production in human endometriotic cells by macrophage migration inhibitory factor: involvement of novel kinase signaling pathways. Endocrinol, 150, 3128-37. https://doi.org/10.1210/en.2008-1088
  19. Cheng CW, Kuo CY, Fan CC, et al (2013). Overexpression of Lon contributes to survival and aggressive phenotype of cancer cells through mitochondrial complex I-mediated generation of reactive oxygen species. Cell Death Dis, 4, 681 https://doi.org/10.1038/cddis.2013.204
  20. Condon JC, Hardy DB, Kovaric K, Mendelson CR (2006). Up-regulation of the progesterone receptor (PR)-C isoform in laboring myometrium by activation of nuclear factor-kappaB may contribute to the onset of labor through inhibition of PR function. Mol Endocrinol, 20, 764-75. https://doi.org/10.1210/me.2005-0242
  21. D'Angelo E, Spagnoli LG, Prat J (2009). Comparative clinicopathologic and immunohistochemical analysis of uterine sarcomas diagnosed using the World Health Organization classification system. Hum Pathol, 40, 1571-85. https://doi.org/10.1016/j.humpath.2009.03.018
  22. Dhingra S, Rodriguez ME, Shen Q, et al (2010 ). Constitutive activation with overexpression of the mTORC2-phospholipase D1 pathway in uterine leiomyosarcoma and STUMP: morphoproteomic analysis with therapeutic implications. Int J Clin Exp Pathol, 4, 134-46.
  23. Du YB, Gao MZ, Shi Y, Sun ZG, Wang J (2013). Endocrine and inflammatory factors and endometriosis-associated infertility in assisted reproduction techniques. Arch Gynecol Obstet, 287, 123-30. https://doi.org/10.1007/s00404-012-2567-0
  24. Finn OJ, Gantt KR, Lepisto AJ, et al (2011). Importance of MUC1 and spontaneous mouse tumor models for understanding the immunobiology of human adenocarcinomas. Immunol Res, 50, 261-8. https://doi.org/10.1007/s12026-011-8214-1
  25. Fortuny J, Sima C, Bayuga S, et al (2009). Risk of endometrial cancer in relation to medical conditions and medication use. Cancer Epidemiol Biomarkers Prev, 18, 1448-56. https://doi.org/10.1158/1055-9965.EPI-08-0936
  26. Fuseya C, Horiuchi A, Hayashi A, et al (2012). Involvement of pelvic inflammation-related mismatch repair abnormalities and microsatellite instability in the malignant transformation of ovarian endometriosis. Hum Pathol, 43, 1964-72. https://doi.org/10.1016/j.humpath.2012.02.005
  27. Gadducci A, Guerrieri ME, Genazzani AR (2012). New insights on the pathogenesis of ovarian carcinoma: molecular basis and clinical implications. Gynecol Endocrinol, 28, 582-6. https://doi.org/10.3109/09513590.2011.649595
  28. Gonzalez-Ramos R, Van Langendonckt A, Defrere S, et al (2010). Involvement of the nuclear factor-${\kappa}B$ pathway in the pathogenesis of endometriosis. Fertil Steril, 94, 1985-94. https://doi.org/10.1016/j.fertnstert.2010.01.013
  29. Gounaris I, Charnock-Jones DS, Brenton JD (2011). Ovarian clear cell carcinoma--bad endometriosis or bad endometrium? J Pathol, 225, 157-60. https://doi.org/10.1002/path.2970
  30. Graca-Souza AV, Arruda MA, de Freitas MS, Barja-Fidalgo C, Oliveira PL (2002). Neutrophil activation by heme: implications for inflammatory processes. Blood, 99, 4160-5. https://doi.org/10.1182/blood.V99.11.4160
  31. Gupta S, Joshi K, Wig JD, Arora SK (2009). High frequency of loss of allelic integrity at Wilms' tumor suppressor gene-1 locus in advanced breast tumors associated with aggressiveness of the tumor. Indian J Cancer, 46, 303-10. https://doi.org/10.4103/0019-509X.55550
  32. Harris HA, Bruner-Tran KL, Zhang X, Osteen KG, Lyttle CR (2005). A selective estrogen receptor-beta agonist causes lesion regression in an experimentally induced model of endometriosis. Hum Reprod, 20, 936-41.
  33. Ismiil N, Rasty G, Ghorab Z, et al (2007a). Adenomyosis involved by endometrial adenocarcinoma is a significant risk factor for deep myometrial invasion. Ann Diagn Pathol, 11, 252-7. https://doi.org/10.1016/j.anndiagpath.2006.08.011
  34. Herrmann Lavoie C, Fraser D, Therriault MJ, Akoum A (2007). Interleukin-1 stimulates macrophage migration inhibitory factor secretion in ectopic endometrial cells of women with endometriosis. Am J Reprod Immunol, 58, 505-13. https://doi.org/10.1111/j.1600-0897.2007.00471.x
  35. Hodge JC, Morton CC (2007). Genetic heterogeneity among uterine leiomyomata: insights into malignant progression. Hum Mol Genet, 16, 7-13. https://doi.org/10.1093/hmg/ddm043
  36. Ip PP, Cheung AN (2011). Pathology of uterine leiomyosarcomas and smooth muscle tumours of uncertain malignant potential. Best Pract Res Clin Obstet Gynaecol, 25, 691-704. https://doi.org/10.1016/j.bpobgyn.2011.07.003
  37. Ip PP, Cheung AN, Clement PB (2009). Uterine smooth muscle tumors of uncertain malignant potential (STUMP): a clinicopathologic analysis of 16 cases. Am J Surg Pathol, 33, 992-1005. https://doi.org/10.1097/PAS.0b013e3181a02d1c
  38. Ismiil ND, Rasty G, Ghorab Z, et al (2007b). Adenomyosis is associated with myometrial invasion by FIGO 1 endometrial adenocarcinoma. Int J Gynecol Pathol, 26, 278-83. https://doi.org/10.1097/01.pgp.0000235064.93182.ec
  39. Jiang X, Morland SJ, Hitchcock A, Thomas EJ, Campbell IG (1998). Allelotyping of endometriosis with adjacent ovarian carcinoma reveals evidence of a common lineage. Cancer Res, 58, 1707-12.
  40. Kajihara H, Yamada Y, Kanayama S, et al (2011). New insights into the pathophysiology of endometriosis: from chronic inflammation to danger signal. Gynecol Endocrinol, 27, 73-9. https://doi.org/10.3109/09513590.2010.507292
  41. Kao YC, Lin MC, Lin WC, Jeng YM, Mao TL (2012). Utility of hepatocyte nuclear factor-$1{\beta}$ as a diagnostic marker in ovarian carcinomas with clear cells. Histopathol, 61, 760-8. https://doi.org/10.1111/j.1365-2559.2012.04267.x
  42. Kobayashi H, Kajihara H, Yamada Y, et al (2011). Risk of carcinoma in women with ovarian endometrioma. Front Biosci (Elite Ed), 3, 529-39. https://doi.org/10.2741/e267
  43. Kim JH, Choi YJ, Kim DC, Lee SJ (2010). Leiomyosarcoma arising in a patient with prior mitotically active leiomyoma. J Obstet Gynaecol Res, 36, 187-90. https://doi.org/10.1111/j.1447-0756.2009.01117.x
  44. Kim JJ, Kurita T, Bulun SE (2013). Progesterone action in endometrial cancer, endometriosis, uterine fibroids, and breast cancer. Endocr Rev, 34, 130-62. https://doi.org/10.1210/er.2012-1043
  45. Kim KH, Jo MS, Suh DS, et al (2012). Expression and significance of the TLR4/MyD88 signaling pathway in ovarian epithelial cancers. World J Surg Oncol, 10, 193. https://doi.org/10.1186/1477-7819-10-193
  46. Kobayashi H, Kajiwara H, Kanayama S, et al (2009). Molecular pathogenesis of endometriosis-associated clear cell carcinoma of the ovary (review). Oncol Rep, 22, 233-40.
  47. Kobayashi H, Sumimoto K, Moniwa N, et al (2007). Risk of developing ovarian cancer among women with ovarian endometrioma: a cohort study in Shizuoka, Japan. Int J Gynecol Cancer, 17, 37-43. https://doi.org/10.1111/j.1525-1438.2006.00754.x
  48. Kowalewska M, Bakula-Zalewska E, Chechlinska M, et al (2013). microRNAs in uterine sarcomas and mixed epithelial-mesenchymal uterine tumors: a preliminary report. Tumour Biol, 34, 2153-60. https://doi.org/10.1007/s13277-013-0748-5
  49. Kucera E, Hejda V, Dankovcik R, et al (2011). Malignant changes in adenomyosis in patients with endometrioid adenocarcinoma. Eur J Gynaecol Oncol, 32, 182-4.
  50. Lam EW, Shah K, Brosens JJ (2012). The diversity of sex steroid action: the role of micro-RNAs and FOXO transcription factors in cycling endometrium and cancer. J Endocrinol, 212, 13-25. https://doi.org/10.1530/JOE-10-0480
  51. Lee CH, Turbin DA, Sung YC, et al (2009). A panel of antibodies to determine site of origin and malignancy in smooth muscle tumors. Mod Pathol, 22, 1519-31. https://doi.org/10.1038/modpathol.2009.122
  52. Makinen N, Mehine M, Tolvanen J, et al (2011). MED12, the mediator complex subunit 12 gene, is mutated at high frequency in uterine leiomyomas. Science, 334, 252-5. https://doi.org/10.1126/science.1208930
  53. Lee JY, Myung SK, Song YS (2013). Prognostic role of cyclooxygenase-2 in epithelial ovarian cancer: a meta-analysis of observational studies. Gynecol Oncol, 129, 613-9. https://doi.org/10.1016/j.ygyno.2013.02.011
  54. Lin SC, Wang CC, Wu MH, et al (2012). Hypoxia-induced microRNA-20a expression increases ERK phosphorylation and angiogenic gene expression in endometriotic stromal cells. J Clin Endocrinol Metab, 97, 1515-23. https://doi.org/10.1210/jc.2012-1450
  55. Maeda D, Shih IeM (2013). Pathogenesis and the role of ARID1A mutation in endometriosis-related ovarian neoplasms. Adv Anat Pathol, 20, 45-52. https://doi.org/10.1097/PAP.0b013e31827bc24d
  56. 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, 383-91. https://doi.org/10.1007/s10147-009-0935-y
  57. Mangili G, Bergamini A, Taccagni G, et al (2012). Unraveling the two entities of endometrioid ovarian cancer: a single center clinical experience. Gynecol Oncol, 126, 403-7. https://doi.org/10.1016/j.ygyno.2012.05.007
  58. Matsumura N, Mandai M, Miyanishi M, et al (2006). Oncogenic property of acrogranin in human uterine leiomyosarcoma: direct evidence of genetic contribution in in vivo tumorigenesis. Clin Cancer Res, 12, 1402-11. https://doi.org/10.1158/1078-0432.CCR-05-2003
  59. McDonald AG, Dal Cin P, Ganguly A, et al (2011). Liposarcoma arising in uterine lipoleiomyoma: a report of 3 cases and review of the literature. Am J Surg Pathol, 35, 221-7. https://doi.org/10.1097/PAS.0b013e31820414f7
  60. McGuire MM, Yatsenko A, Hoffner L, et al (2012). Whole exome sequencing in a random sample of North American women with leiomyomas identifies MED12 mutations in majority of uterine leiomyomas. PLoS One, 7, 33251. https://doi.org/10.1371/journal.pone.0033251
  61. Mittal KR, Chen F, Wei JJ, et al (2009). Molecular and immunohistochemical evidence for the origin of uterine leiomyosarcomas from associated leiomyoma and symplastic leiomyoma-like areas. Mod Pathol, 22, 1303-11. https://doi.org/10.1038/modpathol.2009.96
  62. Melin A, Sparen P, Persson I, Bergqvist A (2006). Endometriosis and the risk of cancer with special emphasis on ovarian cancer. Hum Reprod, 21, 1237-42. https://doi.org/10.1093/humrep/dei462
  63. Mittal K, Joutovsky A (2007). Areas with benign morphologic and immunohistochemical features are associated with some uterine leiomyosarcomas. Gynecol Oncol, 104, 362-5. https://doi.org/10.1016/j.ygyno.2006.08.034
  64. Mittal KR, Barwick KW (1993). Endometrial adenocarcinoma involving adenomyosis without true myometrial invasion is characterized by frequent preceding estrogen therapy, low histologic grades, and excellent prognosis. Gynecol Oncol, 49, 197-201. https://doi.org/10.1006/gyno.1993.1107
  65. Modugno F, Ness RB, Allen GO, et al (2004). Oral contraceptive use, reproductive history, and risk of epithelial ovarian cancer in women with and without endometriosis. Am J Obstet Gynecol, 191, 733-40. https://doi.org/10.1016/j.ajog.2004.03.035
  66. Munksgaard PS, Blaakaer J (2012). The association between endometriosis and ovarian cancer: a review of histological, genetic and molecular alterations. Gynecol Oncol, 124, 164-9. https://doi.org/10.1016/j.ygyno.2011.10.001
  67. Murphy MA, Wentzensen N (2011). Frequency of mismatch repair deficiency in ovarian cancer: a systematic review This article is a US Government work and, as such, is in the public domain of the United States of America. Int J Cancer, 129, 1914-22. https://doi.org/10.1002/ijc.25835
  68. Musa F, Frey MK, Im HB, et al (2012). Does the presence of adenomyosis and lymphovascular space invasion affect lymph node status in patients with endometrioid adenocarcinoma of the endometrium? Am J Obstet Gynecol, 207, 417.
  69. Newman AC, Hughes CC (2012). Macrophages and angiogenesis: a role for Wnt signaling. Vasc Cell, 4, 13. https://doi.org/10.1186/2045-824X-4-13
  70. Nagle CM, Olsen CM, Webb PM, et al (2008). Endometrioid and clear cell ovarian cancers: a comparative analysis of risk factors. Eur J Cancer, 44, 2477-84. https://doi.org/10.1016/j.ejca.2008.07.009
  71. Ness RB, Cramer DW, GoodmanMT, et al (2002). Infertility, fertility drugs, and ovarian cancer: a pooled analysis of case-control studies. Am J Epidemiol, 155, 217-24. https://doi.org/10.1093/aje/155.3.217
  72. Ness RB, Grisso JA, Cottreau C, et al (2000). Factors related to inflammation of the ovarian epithelium and risk of ovarian cancer. Epidemiol, 11, 111-7. https://doi.org/10.1097/00001648-200003000-00006
  73. Nezhat F, Datta MS, Hanson V, et al (2008). The relationship of endometriosis and ovarian malignancy: a review. Fertil Steril, 90, 1559-70. https://doi.org/10.1016/j.fertnstert.2008.08.007
  74. O'Donnell AJ, Macleod KG, Burns DJ, Smyth JF, Langdon SP (2005). Estrogen receptor alpha mediates gene expression changes and growth response in ovarian cancer cells exposed to estrogen. Endocr Relat Cancer, 12, 851-66. https://doi.org/10.1677/erc.1.01039
  75. O'Neill CJ, McBride HA, Connolly LE, McCluggage WG (2007). Uterine leiomyosarcomas are characterized by high p16, p53 and MIB1 expression in comparison with usual leiomyomas, leiomyoma variants and smooth muscle tumours of uncertain malignant potential. Histopathol, 50, 851-8. https://doi.org/10.1111/j.1365-2559.2007.02699.x
  76. Obeid E, Nanda R, Fu YX, Olopade OI (2013). The role of tumor-associated macrophages in breast cancer progression (review). Int J Oncol, 43, 5-12.
  77. Olson JE, Cerhan JR, Janney CA, et al (2002). Postmenopausal cancer risk after self-reported endometriosis diagnosis in the Iowa women's health study. Cancer, 94, 1612-8. https://doi.org/10.1002/cncr.10370
  78. Pellegrini C, Gori I, Achtari C, et al (2012). The expression of estrogen receptors as well as GREB1, c-MYC, and cyclin D1, estrogen-regulated genes implicated in proliferation, is increased in peritoneal endometriosis. Fertil Steril, 98, 1200-8. https://doi.org/10.1016/j.fertnstert.2012.06.056
  79. Otsuka J, Okuda T, Sekizawa A, et al (2004). K-ras mutation may promote carcinogenesis of endometriosis leading to ovarian clear cell carcinoma. Med Electron Microsc, 37, 188-92.
  80. Pal T, Permuth-Wey J, Kumar A, Sellers TA (2008). Systematic review and meta-analysis of ovarian cancers: estimation of microsatellite-high frequency and characterization of mismatch repair deficient tumor histology. Clin Cancer Res, 14, 6847-54. https://doi.org/10.1158/1078-0432.CCR-08-1387
  81. Pandurangan AK (2013). Potential targets for prevention of colorectal cancer: a focus on PI3K/Akt/mTOR and Wnt pathways. Asian Pac J Cancer Prev, 14, 2201-5. https://doi.org/10.7314/APJCP.2013.14.4.2201
  82. Perez de Castro I, Malumbres M (2012). Mitotic stress and chromosomal instability in cancer: the case for TPX2. Genes Cancer, 3, 721-30. https://doi.org/10.1177/1947601912473306
  83. Perot G, Croce S, Ribeiro A, et al (2012). MED12 alterations in both human benign and malignant uterine soft tissue tumors. PLoS One, 7, 40015. https://doi.org/10.1371/journal.pone.0040015
  84. Quade BJ, Wang TY, Sornberger K, et al (2004). Molecular pathogenesis of uterine smooth muscle tumors from transcriptional profiling. Genes Chromosomes Cancer, 40, 97-108. https://doi.org/10.1002/gcc.20018
  85. 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, 1357-64. https://doi.org/10.1007/s10552-008-9207-9
  86. Rowlands IJ, Nagle CM, Spurdle AB, Webb PM (2011). Gynecological conditions and the risk of endometrial cancer. Gynecol Oncol, 123, 537-41. https://doi.org/10.1016/j.ygyno.2011.08.022
  87. Slater M, Cooper M, Murphy CR (2006). Human growth hormone and interleukin-6 are upregulated in endometriosis and endometrioid adenocarcinoma. Acta Histochem, 108, 13-8. https://doi.org/10.1016/j.acthis.2006.01.004
  88. Sacco K, Portelli M, Pollacco J, Schembri-Wismayer P, Calleja-Agius J (2012). The role of prostaglandin E2 in endometriosis. Gynecol Endocrinol, 28, 134-8. https://doi.org/10.3109/09513590.2011.588753
  89. Sato N, Tsunoda H, Nishida M, et al (2000). Loss of heterozygosity on 10q23.3 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, 7052-6.
  90. Siegel R, Naishadham D, Jemal A (2013). Cancer statistics, 2013. CA Cancer J Clin Jan, 63, 11-30. https://doi.org/10.3322/caac.21166
  91. Son Y, Kim S, Chung HT, Pae HO (2013). Reactive oxygen https://doi.org/10.1016/B978-0-12-405881-1.00002-1

Cited by

  1. miRNA-1297 Induces Cell Proliferation by Targeting Phosphatase and Tensin Homolog in Testicular Germ Cell Tumor Cells vol.15, pp.15, 2014, https://doi.org/10.7314/APJCP.2014.15.15.6243
  2. Influence of Propofol, Isoflurane and Enflurance on Levels of Serum Interleukin-8 and Interleukin-10 in Cancer Patients vol.15, pp.16, 2014, https://doi.org/10.7314/APJCP.2014.15.16.6703
  3. Rare case of endometrioid adenocarcinoma arising from cystic adenomyosis vol.41, pp.2, 2014, https://doi.org/10.1111/jog.12513
  4. No Evidence of Association of the Arg72Pro p53 Gene Polymorphism with Cancer Risk in the Saudi Population: a Meta-Analysis vol.16, pp.14, 2015, https://doi.org/10.7314/APJCP.2015.16.14.5663
  5. Lack of Influence of the ACE1 Gene I/D Polymorphism on the Formation and Growth of Benign Uterine Leiomyoma in Turkish Patients vol.16, pp.3, 2015, https://doi.org/10.7314/APJCP.2015.16.3.1123
  6. Use of enhanced T2 star-weighted angiography (ESWAN) and R2* values to distinguish ovarian cysts due to endometriosis from other causes vol.40, pp.6, 2015, https://doi.org/10.1007/s00261-014-0314-7
  7. Expression of MIF and c-erbB-2 in endometrial cancer vol.13, pp.5, 2016, https://doi.org/10.3892/mmr.2016.4992
  8. Follicle-Stimulating Hormone Receptor Expression in Endometriotic Lesions and the Associated Vasculature vol.23, pp.7, 2016, https://doi.org/10.1177/1933719115623647
  9. Risk of Endometrial Cancer in Women With Pelvic Inflammatory Disease vol.94, pp.34, 2015, https://doi.org/10.1097/MD.0000000000001278
  10. Upregulation of long noncoding RNA TUG1 by EGR1 promotes adenomyotic epithelial cell migration and invasion through recruiting EZH2 and suppressing TIMP2 vol.86, pp.2, 2019, https://doi.org/10.1002/mrd.23099