Pathogenesis of ovarian clear cell adenofibroma, atypical proliferative (borderline) tumor, and carcinoma: Clinicopathologic features of tumors with endometriosis or adenofibromatous components support two related pathways of tumor development

Journal of Cancer

Volumn 2, Issue 1, 2011, Pages 94-106

  Zhao, Chengquan ^a,b   Wu, Lee Shu Fune ^c   Barner, Ross ^b,d  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b ARMED FORCES INSTITUTE OF PATHOLOGY   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

^d WALTER REED ARMY MEDICAL CENTER   (United States)

Author keywords

Adenofibromatous; Clear cell carcinoma; Endometriosis; Ovary; Pathogenesis

Indexed keywords

ADULT; ADVANCED CANCER; AGED; ARTICLE; ATYPICAL PROLIFERATIVE TUMOR; CANCER CLASSIFICATION; CANCER LOCALIZATION; CANCER PATIENT; CLINICAL FEATURE; CONTROLLED STUDY; DISEASE SEVERITY; ENDOMETRIOSIS; ENDOMETRIUM CELL; FEMALE; FIBROMA; HISTOPATHOLOGY; HUMAN; MAJOR CLINICAL STUDY; OVARIAN CLEAR CELL ADENOFIBROMA; OVARIAN EPITHELIAL CLEAR CELL NEOPLASM; OVARY CANCER; OVARY CARCINOMA; OVARY CYST; OVARY TUMOR; PATHOPHYSIOLOGY; RISK FACTOR; TUMOR GROWTH; TUMOR VOLUME;

EID: 80051548300     PISSN: None     EISSN: 18379664     Source Type: Journal    
DOI: 10.7150/jca.2.94     Document Type: Article

References (77)

1. Akahane T, Sekizawa A, Purwosunu Y, et al. The role of p53 mutation in the carcinomas arising from endometriosis. Int J Gynecol Pathol. 2007;26:345-351.
2. Ali-Fehmi R, Khalifeh I, Bandyopadhyay S, et al. 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. 2006;25:223-229.
3. Ballouk F, Ross JS, Wolf BC. Ovarian endometriotic cysts. An analysis of cytologic atypia and DNA ploidy patterns. Am J Clin Pathol. 1994;102:415-419.
4. Bell DA, Scully RE. Benign and borderline clear cell adenofibromas of the ovary. Cancer. 1985;56:2922-2931.
5. Borgfeldt C, Andolf E. Cancer risk after hospital discharge diagnosis of benign ovarian cysts and endometriosis. Acta Obstet Gynecol Scand. 2004;83:395-400.
6. Brescia RJ, Dubin N, Demopoulos RI. Endometrioid and clear cell carcinoma of the ovary. Factors affecting survival. Int J Gynecol Pathol. 1989;8:132-138.
7. Brinton LA, Gridley G, Persson I, et al. Cancer risk after a hospital discharge diagnosis of endometriosis. Am J Obstet Gynecol. 1997;176:572-579.
8. Chan JK, Teoh D, Hu JM, et al. Do clear cell ovarian carcinomas have poorer prognosis compared to other epithelial cell types? A study of 1411 clear cell ovarian cancers. Gynecol Oncol. 2008;109:370-376.
9. Cho K, Shih I. Ovarian cancer. Annu Rev Pathol Mech Dis. 2009;4:287-313.
10. Crozier MA, Copeland LJ, Silva EG, et al. Clear cell carcinoma of the ovary: a study of 59 cases. Gynecol Oncol. 1989;35:199-203.
11. Cuatrecasas M, Catasus L, Palacios J, et al. Transitional cell tumors of the ovary: a comparative clinicopathologic, immunohistochemical, and molecular genetic analysis of Brenner tumors and transitional cell carcinomas. Am J Surg Pathol. 2009;33:556-567.
12. Czernobilsky B, Silverman BB, Enterline HT. Clear-cell carcinoma of the ovary. A clinicopathologic analysis of pure and mixed forms and comparison with endometrioid carcinoma. Cancer. 1970;25:762-772.
13. Delair D, Oliva E, Kobel M, et al. Morphologic spectrum of immunohistochemically characterized clear cell carcinoma of the ovary: a study of 155 cases. Am J Surg Pathol. 2011;35:36-44.
14. Dent J, Hall GD, Wilkinson N, et al. Cytogenetic alterations in ovarian clear cell carcinoma detected by comparative genomic hybridisation. Br J Cancer. 2003;88:1578-1583.
15. Erzen M, Rakar S, Klancnik B, et al. Endometriosis-associated ovarian carcinoma (EAOC): an entity distinct from other ovarian carcinomas as suggested by a nested case-control study. Gynecol Oncol. 2001;83:100-108.
16. Fujita M, Enomoto T, Inoue M, et al. Alteration of the p53 tumor suppressor gene occurs independently of K-ras activation and more frequently in serous adenocarcinomas than in other common epithelial tumors of the human ovary. Jpn J Cancer Res. 1994;85:1247-1256.
17. Fukunaga M, Nomura K, Ishikawa E, et al. Ovarian atypical endometriosis: its close association with malignant epithelial tumours. Histopathology. 1997;30:249-255.
18. Geyer JT, Lopez-Garcia MA, Sanchez-Estevez C, et al. Pathogenetic pathways in ovarian endometrioid adenocarcinoma: a molecular study of 29 cases. Am J Surg Pathol. 2009;33:1157-1163.
19. Gilks CB, Ionescu DN, Kalloger SE, et al. Tumor cell type can be reproducibly diagnosed and is of independent prognostic significance in patients with maximally debulked ovarian carcinoma. Hum Pathol. 2008;39:1239-1251.
20. Goff BA, Sainz de la Cuesta R, Muntz HG, et al. 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. 1996;60:412-417.
21. Goumenou AG, Arvanitis DA, Matalliotakis IM, et al. Microsatellite DNA assays reveal an allelic imbalance in p16(Ink4), GALT, p53, and APOA2 loci in patients with endometriosis. Fertil Steril. 2001;75:160-165.
22. Ho ES, Lai CR, Hsieh YT, et al. p53 mutation is infrequent in clear cell carcinoma of the ovary. Gynecol Oncol. 2001;80:189-193.
23. Horiuchi A, Itoh K, Shimizu M, et al. Toward understanding the natural history of ovarian carcinoma development: a clinicopathological approach. Gynecol Oncol. 2003;88:309-317.
24. Itamochi H, Kigawa J, Sugiyama T, et al. Low proliferation activity may be associated with chemoresistance in clear cell carcinoma of the ovary. Obstet Gynecol. 2002;100:281-287.
25. Jenison EL, Montag AG, Griffiths CT, et al. Clear cell adenocarcinoma of the ovary: a clinical analysis and comparison with serous carcinoma. Gynecol Oncol. 1989;32:65-71.
26. Jiang X, Hitchcock A, Bryan EJ, et al. Microsatellite analysis of endometriosis reveals loss of heterozygosity at candidate ovarian tumor suppressor gene loci. Cancer Res. 1996;56:3534-3539.
27. Jiang X, Morland SJ, Hitchcock A, et al. Allelotyping of endometriosis with adjacent ovarian carcinoma reveals evidence of a common lineage. Cancer Res. 1998;58:1707-1712.
28. Jimbo H, Hitomi Y, Yoshikawa H, et al. Evidence for monoclonal expansion of epithelial cells in ovarian endometrial cysts. Am J Pathol. 1997;150:1173-1178.
29. Jimbo H, Yoshikawa H, Onda T, et al. Prevalence of ovarian endometriosis in epithelial ovarian cancer. Int J Gynaecol Obstet. 1997;59:245-250.
30. Kennedy AW, Biscotti CV, Hart WR, et al. Ovarian clear cell adenocarcinoma. Gynecol Oncol. 1989;32:342-349.
31. Kita T, Kikuchi Y, Kudoh K, et al. Exploratory study of effective chemotherapy to clear cell carcinoma of the ovary. Oncol Rep. 2000;7:327-331.
32. Kobayashi H, Kajiwara H, Kanayama S, et al. Molecular pathogenesis of endometriosis-associated clear cell carcinoma of the ovary (review). Oncol Rep. 2009;22:233-240.
33. Kobayashi H, Sumimoto K, Kitanaka T, et al. Ovarian endometrioma--risks factors of ovarian cancer development. Eur J Obstet Gynecol Reprod Biol. 2008;138:187-193.
34. Kobayashi H, Yamada Y, Kanayama S, et al. The role of hepatocyte nuclear factor-1beta in the pathogenesis of clear cell carcinoma of the ovary. Int J Gynecol Cancer. 2009;19:471-479.
35. Komiyama S, Aoki D, Tominaga E, et al. Prognosis of Japanese patients with ovarian clear cell carcinoma associated with pelvic endometriosis: clinicopathologic evaluation. Gynecol Oncol. 1999;72:342-346.
36. Korner M, Burckhardt E, Mazzucchelli L. Higher frequency of chromosomal aberrations in ovarian endometriosis compared to extragonadal endometriosis: A possible link to endometrioid adenocarcinoma. Mod Pathol. 2006;19:1615-1623.
37. Kuo KT, Mao TL, Chen X, et al. DNA copy numbers profiles in affinity-purified ovarian clear cell carcinoma. Clin Cancer Res. 2010;16:1997-2008.
38. Kuo KT, Mao TL, Jones S, et al. Frequent activating mutations of PIK3CA in ovarian clear cell carcinoma. Am J Pathol. 2009;174:1597-1601.
39. Kurman RJ, Craig JM. Endometrioid and clear cell carcinoma of the ovary. Cancer. 1972;29:1653-1664.
40. Kurman RJ, Shih I. Pathogenesis of ovarian cancer: lessons from morphology and molecular biology and their clinical implications. Int J Gynecol Pathol. 2008;27:151-160.
41. Kurman RJ, Shih I. The origin and pathogenesis of epithelial ovarian cancer: a proposed unifying theory. Am J Surg Pathol. 2010;34:433-443.
42. LaGrenade A, Silverberg SG. Ovarian tumors associated with atypical endometriosis. Hum Pathol. 1988;19:1080-1084.
43. Mandai M, Yamaguchi K, Matsumura N, et al. Ovarian cancer in endometriosis: molecular biology, pathology, and clinical management. Int J Clin Oncol. 2009;14:383-391.
44. Mizuno M, Kikkawa F, Shibata K, et al. Long-term follow-up and prognostic factor analysis in clear cell adenocarcinoma of the ovary. J Surg Oncol. 2006;94:138-143.
45. Modesitt SC, Tortolero-Luna G, Robinson JB, et al. Ovarian and extraovarian endometriosis-associated cancer. Obstet Gynecol. 2002;100:788-795.
46. Moll UM, Chumas JC, Chalas E, et al. Ovarian carcinoma arising in atypical endometriosis. Obstet Gynecol. 1990;75:537-539.
47. Montag AG, Jenison EL, Griffiths CT, et al. Ovarian clear cell carcinoma. A clinicopathologic analysis of 44 cases. Int J Gynecol Pathol. 1989;8:85-96.
48. Nilbert M, Pejovic T, Mandahl N, et al. Monoclonal origin of endometriotic cysts. Int J Gynecol Cancer. 1995;5:61-63.
49. Norris HJ, Robinowitz M. Ovarian adenocarcinoma of mesonephric type. Cancer. 1971;28:1074-1081.
50. Ogawa S, Kaku T, Amada S, et al. Ovarian endometriosis associated with ovarian carcinoma: a clinicopathological and immunohistochemical study. Gynecol Oncol. 2000;77:298-304.
51. Okada S, Tsuda H, Takarabe T, et al. Allelotype analysis of common epithelial ovarian cancers with special reference to comparison between clear cell adenocarcinoma with other histological types. Jpn J Cancer Res. 2002;93:798-806.
52. Okuda T, Otsuka J, Sekizawa A, et al. p53 mutations and overexpression affect prognosis of ovarian endometrioid cancer but not clear cell cancer. Gynecol Oncol. 2003;88:318-325.
53. Orezzoli JP, Russell AH, Oliva E, et al. Prognostic implication of endometriosis in clear cell carcinoma of the ovary. Gynecol Oncol. 2008;110:336-344.
54. Prowse AH, Manek S, Varma R, et al. Molecular genetic evidence that endometriosis is a precursor of ovarian cancer. Int J Cancer. 2006;119:556-562.
55. Roth LM, Langley FA, Fox H, et al. Ovarian clear cell adenofibromatous tumors. Benign, of low malignant potential, and associated with invasive clear cell carcinoma. Cancer. 1984;53:1156-1163.
56. Ryu SY, Park SI, Nam BH, et al. Prognostic significance of histological grade in clear-cell carcinoma of the ovary: a retrospective study of Korean Gynecologic Oncology Group. Ann Oncol. 2009;20:1032-1036.
57. Sato N, Tsunoda H, Nishida M, et al. 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. 2000;60:7052-7056.
58. Sato Y, Shimamoto T, Amada S, et al. Prognostic value of histologic grading of ovarian carcinomas. Int J Gynecol Pathol. 2003;22:52-56.
59. Shih I, Kurman RJ. Ovarian tumorigenesis: a proposed model based on morphological and molecular genetic analysis. Am J Pathol. 2004;164:1511-1518.
60. Shimizu Y, Kamoi S, Amada S, et al. Toward the development of a universal grading system for ovarian epithelial carcinoma: testing of a proposed system in a series of 461 patients with uniform treatment and follow-up. Cancer. 1998;82:893-901.
61. Silva EG, Young RH. Endometrioid neoplasms with clear cells: a report of 21 cases in which the alteration is not of typical secretory type. Am J Surg Pathol. 2007;31:1203-1208.
62. Silverberg SG. Histopathologic grading of ovarian carcinoma: a review and proposal. Int J Gynecol Pathol. 2000;19:7-15.
63. Stern RC, Dash R, Bentley RC, et al. Malignancy in endometriosis: frequency and comparison of ovarian and extraovarian types. Int J Gynecol Pathol. 2001;20:133-139.
64. Sugiyama T, Kamura T, Kigawa J, et al. Clinical characteristics of clear cell carcinoma of the ovary: a distinct histologic type with poor prognosis and resistance to platinum-based chemotherapy. Cancer. 2000;88:2584-2589.
65. Takano M, Kikuchi Y, Yaegashi N, et al. Clear cell carcinoma of the ovary: a retrospective multicentre experience of 254 patients with complete surgical staging. Br J Cancer. 2006;94:1369-1374.
66. Tammela J, Geisler JP, Eskew PN Jr, et al. Clear cell carcinoma of the ovary: poor prognosis compared to serous carcinoma. Eur J Gynaecol Oncol. 1998;19:438-440.
67. Tamura M, Fukaya T, Murakami T, et al. Analysis of clonality in human endometriotic cysts based on evaluation of X chromosome inactivation in archival formalin-fixed, paraffin-embedded tissue. Lab Invest. 1998;78:213-218.
68. Tsukahara Y, Satoh M, Kato J, et al. Clinicopathologic investigation of ovarian endometriosis: a comparative study of cystic and non-cystic types. Nippon Sanka Fujinka Gakkai Zasshi. 1985;37:751-757.
69. Varma R, Rollason T, Gupta JK, et al. Endometriosis and the neoplastic process. Reproduction. 2004;127:293-304.
70. Veras E, Mao TL, Ayhan A, et al. Cystic and adenofibromatous clear cell carcinomas of the ovary: distinctive tumors that differ in their pathogenesis and behavior: a clinicopathologic analysis of 122 cases. Am J Surg Pathol. 2009;33:844-853.
71. Willner J, Wurz K, Allison KH, et al. Alternate molecular genetic pathways in ovarian carcinomas of common histological types. Hum Pathol. 2007;38:607-613.
72. Yamamoto S, Tsuda H, Miyai K, et al. Aberrant expression of p27(Kip1)-interacting cell-cycle regulatory proteins in ovarian clear cell carcinomas and their precursors with special consideration of two distinct multistage clear cell carcinogenetic pathways. Virchows Arch. 2009;455:413-422.
73. Yamamoto S, Tsuda H, Suzuki K, et al. An allelotype analysis indicating the presence of two distinct ovarian clear-cell carcinogenic pathways: endometriosis-associated pathway vs. clear-cell adenofibroma-associated pathway. Virchows Arch. 2009;455:261-270.
74. Yamamoto S, Tsuda H, Takano M, et al. Clear-cell adenofibroma can be a clonal precursor for clear-cell adenocarcinoma of the ovary: a possible alternative ovarian clear-cell carcinogenic pathway. J Pathol. 2008;216:103-110.
75. Yamamoto S, Tsuda H, Yoshikawa T, et al. Clear cell adenocarcinoma associated with clear cell adenofibromatous components: a subgroup of ovarian clear cell adenocarcinoma with distinct clinicopathologic characteristics. Am J Surg Pathol. 2007;31:999-1006.
76. Yoonessi M, Weldon D, Satchidand SK, et al. Clear cell ovarian adenocarcinoma. J Surg Oncol. 1984;27:289-297.
77. Young RH, Scully RE. Oxyphilic clear cell carcinoma of the ovary. A report of nine cases. Am J Surg Pathol. 1987;11:661-667.