Strategies for distinguishing low-grade endometrioid and serous carcinomas of endometrium

Advances in Anatomic Pathology

Volumn 19, Issue 1, 2012, Pages 1-10

  Garg, Karuna ^a   Soslow, Robert A ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

endometrioid carcinomas; endometrium; morphologically ambiguous carcinomas; serous carcinomas

Indexed keywords

TAMOXIFEN;

ADULT; CANCER MORPHOLOGY; CONTROLLED STUDY; DIFFERENTIAL DIAGNOSIS; ENDOMETRIOID CARCINOMA; ENDOMETRIUM CARCINOMA; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; PATHOLOGIST; PRIORITY JOURNAL; REVIEW; SEROUS CARCINOMA;

CARCINOMA, ENDOMETRIOID; CYSTADENOCARCINOMA, SEROUS; DIAGNOSIS, DIFFERENTIAL; ENDOMETRIAL NEOPLASMS; FEMALE; HUMANS; NEOPLASM GRADING;

EID: 83755188596     PISSN: 10724109     EISSN: 15334031     Source Type: Journal    
DOI: 10.1097/PAP.0b013e318234ab36     Document Type: Review

References (84)

1. Bokhman JV. Two pathogenetic types of endometrial carcinoma. Gynecol Oncol. 1983;15:10-17. (Pubitemid 13194678)
2. Hayes MP, Wang H, Espinal-Witter R, et al. PIK3CA and PTEN mutations in uterine endometrioid carcinoma and complex atypical hyperplasia. Clin Cancer Res. 2006; 12 (20 Pt 1):5932-5935. (Pubitemid 44703751)
3. Velasco A, Bussaglia E, Pallares J, et al. PIK3CA gene mutations in endometrial carcinoma: correlation with PTEN and K-RAS alterations. Hum Pathol. 2006;37:1465-1472. (Pubitemid 44584324)
4. Oda K, Stokoe D, Taketani Y, et al. High frequency of coexistent mutations of PIK3CA and PTEN genes in endometrial carcinoma. Cancer Res. 2005;65:10669-10673. (Pubitemid 41713332)
5. Irving JA, Catasus L, Gallardo A, et al. Synchronous endometrioid carcinomas of the uterine corpus and ovary: alterations in the beta-catenin (CTNNB1) pathway are associated with independent primary tumors and favorable prognosis. Hum Pathol. 2005;36:605-619. (Pubitemid 40922566)
6. Scholten AN, Creutzberg CL, van den Broek LJ, et al. Nuclear beta-catenin is a molecular feature of type I endometrial carcinoma. J Pathol. 2003;201:460-465. (Pubitemid 37408267)
7. Moreno-Bueno G, Hardisson D, Sanchez C, et al. Abnormalities of the APC/beta-catenin pathway in endometrial cancer. Oncogene. 2002;21:7981-7990. (Pubitemid 35430609)
8. Tashiro H, Blazes MS, Wu R, et al. Mutations in PTEN are frequent in endometrial carcinoma but rare in other common gynecological malignancies. Cancer Res. 1997;57:3935-3940. (Pubitemid 27427679)
9. Levine RL, Cargile CB, Blazes MS, et al. PTEN mutations and microsatellite instability in complex atypical hyperplasia, a precursor lesion to uterine endometrioid carcinoma. Cancer Res. 1998;58:3254-3258. (Pubitemid 28371061)
10. Esteller M, Levine R, Baylin SB, et al. MLH1 promoter hypermethylation is associated with the microsatellite instability phenotype in sporadic endometrial carcinomas. Oncogene. 1998;17:2413-2417. (Pubitemid 28515395)
11. Gurin CC, Federici MG, Kang L, et al. Causes and consequences of microsatellite instability in endometrial carcinoma. Cancer Res. 1999;59:462-466. (Pubitemid 29048884)
12. Catasus L, D'Angelo E, Pons C, et al. Expression profiling of 22 genes involved in the PI3K-AKT pathway identifies two subgroups of high-grade endometrial carcinomas with different molecular alterations. Mod Pathol. 2010;23:694-702.
13. Hayes MP, Douglas W, Ellenson LH. Molecular alterations of EGFR and PIK3CA in uterine serous carcinoma. Gynecol Oncol. 2009;113:370-373.
14. Catasus L, Gallardo A, Cuatrecasas M, et al. Concomitant PI3K-AKT and p53 alterations in endometrial carcinomas are associated with poor prognosis. Mod Pathol. 2009;22:522-529.
15. Tashiro H, Isacson C, Levine R, et al. p53 gene mutations are common in uterine serous carcinoma and occur early in their pathogenesis. Am J Pathol. 1997;150:177-185. (Pubitemid 27027108)
16. Lax SF, Kendall B, Tashiro H, et al. The frequency of p53, K-ras mutations, and microsatellite instability differs in uterine endometrioid and serous carcinoma: evidence of distinct molecular genetic pathways. Cancer. 2000;88:814-824. (Pubitemid 30091101)
17. Shih Ie, M, Wang TL. Mutation of PPP2R1A: a new clue in unveiling the pathogenesis of uterine serous carcinoma. J Pathol. 2011;224:1-4.
18. Carcangiu ML, Chambers JT. Uterine papillary serous carcinoma: a study on 108 cases with emphasis on the prognostic significance of associated endometrioid carcinoma, absence of invasion, and concomitant ovarian carcinoma. Gynecol Oncol. 1992;47:298-305. (Pubitemid 23011408)
19. Soslow RA, Bissonnette JP, Wilton A, et al. Clinicopathologic analysis of 187 high-grade endometrial carcinomas of different histologic subtypes: similar outcomes belie distinctive biologic differences. Am J Surg Pathol. 2007;31:979-987. (Pubitemid 47012293)
20. Creasman WT, Morrow CP, Bundy BN, et al. Surgical Pathologic Spread Patterns of Endometrial Cancer. A Gynecologic Oncology Group Study. Cancer. 60. 1987;8 Suppl:2035-2041.
21. Faratian D, Stillie A, Busby-Earle RM, et al. A review of the pathology and management of uterine papillary serous carcinoma and correlation with outcome. Int J Gynecol Cancer. 2006;16:972-978. (Pubitemid 43886712)
22. Tay EH, Ward BG. The treatment of uterine papillary serous carcinoma (UPSC): are we doing the right thing? Int J Gynecol Cancer. 1999;9:463-469. (Pubitemid 30027549)
23. Slomovitz BM, Burke TW, Eifel PJ, et al. Uterine papillary serous carcinoma (UPSC): a single institution review of 129 cases. Gynecol Oncol. 2003;91:463-469. (Pubitemid 38388137)
24. Boruta DM 2nd, Gehrig PA, Fader AN, et al. Management of women with uterine papillary serous cancer: a Society of Gynecologic Oncology (SGO) review. Gynecol Oncol. 2009;115:142-153.
25. Zaino RJ, Kurman RJ, Diana KL, et al. The utility of the revised International Federation of Gynecology and Obstetrics histologic grading of endometrial adenocarcinoma using a defined nuclear grading system. A Gynecologic Oncology Group study. Cancer. 1995;75:81-86.
26. Lomo L, Nucci MR, Lee KR, et al. Histologic and immunohistochemical decision-making in endometrial adenocarcinoma. Mod Pathol. 2008;21:937-942.
27. Garg K, Leitao MM Jr., Wynveen CA, et al. p53 overexpression in morphologically ambiguous endometrial carcinomas correlates with adverse clinical outcomes. Mod Pathol. 2010;23:80-92.
28. Bristow RE, Asrari F, Trimble EL, et al. Extended surgical staging for uterine papillary serous carcinoma: survival outcome of locoregional (Stage I-III) disease. Gynecol Oncol. 2001;81:279-286. (Pubitemid 32424175)
29. Ferguson SE, Tornos C, Hummer A, et al. Prognostic features of surgical stage I uterine carcinosarcoma. Am J Surg Pathol. 2007;31:1653-1661. (Pubitemid 350287563)
30. Garg K, Leitao MM Jr., Kauff ND, et al. Selection of endometrial carcinomas for DNA mismatch repair protein immunohistochemistry using patient age and tumor morphology enhances detection of mismatch repair abnormalities. Am J Surg Pathol. 2009;33:925-933.
31. Carcangiu ML, Radice P, Casalini P, et al. Lynch syndromerelated endometrial carcinomas show a high frequency of nonendometrioid types and of high FIGO grade endometrioid types. Int J Surg Pathol. 2010;18:21-26.
32. Broaddus RR, Lynch HT, Chen LM, et al. Pathologic features of endometrial carcinoma associated with HNPCC: a comparison with sporadic endometrial carcinoma. Cancer. 2006;106: 87-94. (Pubitemid 43032552)
33. Westin SN, Lacour RA, Urbauer DL, et al. Carcinoma of the lower uterine segment: a newly described association with Lynch syndrome. J Clin Oncol. 2008;26:5965-5971.
34. Gilks CBOE, Soslow R. Poor Interobserver reproducibility in the diagnosis of high-grade endometrial carcinoma. Mod Pathol. 2011;24:1.
35. Alkushi A, Kobel M, Kalloger SE, et al. High-grade endometrial carcinoma: serous and grade 3 endometrioid carcinomas have different immunophenotypes and outcomes. Int J Gynecol Pathol. 2010;29:343-350.
36. Sherman ME, Sturgeon S, Brinton LA, et al. Risk factors and hormone levels in patients with serous and endometrioid uterine carcinomas. Mod Pathol. 1997;10:963-968. (Pubitemid 27471115)
37. Bland AE, Calingaert B, Secord AA, et al. Relationship between tamoxifen use and high risk endometrial cancer histologic types. Gynecol Oncol. 2009;112:150-154.
38. Liang SX, Pearl M, Liang S, et al. Personal history of breast cancer as a significant risk factor for endometrial serous carcinoma in women aged 55 years old or younger. Int J Cancer. 2011;128:763-770.
39. Ferguson SE, Soslow RA, Amsterdam A, et al. Comparison of uterine malignancies that develop during and following tamoxifen therapy. Gynecol Oncol. 2006;101:322-326.
40. Pothuri B, Ramondetta L, Eifel P, et al. Radiation-associated ndometrial cancers are prognostically unfavorable tumors: a clinicopathologic comparison with 527 sporadic endometrial cancers. Gynecol Oncol. 2006;103:948-951. (Pubitemid 44821320)
41. Trahan S, Tetu B, Raymond PE. Serous papillary carcinoma of the endometrium arising from endometrial polyps: a clinical, histological, and immunohistochemical study of 13 cases. Hum Pathol. 2005;36:1316-1321. (Pubitemid 41682288)
42. Hui P, Kelly M, O'Malley DM, et al. Minimal uterine serous carcinoma: a clinicopathological study of 40 cases. Mod Pathol. 2005;18:75-82. (Pubitemid 40128098)
43. Ambros RA, Sherman ME, Zahn CM, et al. Endometrial intraepithelial carcinoma: a distinctive lesion specifically associated with tumors displaying serous differentiation. Hum Pathol. 1995;26:1260-1267.
44. Zheng W, Xiang L, Fadare O, et al. A proposed model for endometrial serous carcinogenesis. Am J Surg Pathol. 2011;35:e1-e14.
45. Zhang X, Liang SX, Jia L, et al. Molecular identification of "latent precancers" for endometrial serous carcinoma in benign-appearing endometrium. Am J Pathol. 2009;174: 2000-2006.
46. Jia L, Liu Y, Yi X, et al. Endometrial glandular dysplasia with frequent p53 gene mutation: a genetic evidence supporting its precancer nature for endometrial serous carcinoma. Clin Cancer Res. 2008;14:2263-2269. (Pubitemid 351551056)
47. Fadare O, ZhengW. Endometrial Glandular Dysplasia (EmGD): morphologically and biologically distinctive putative precursor lesions of Type II endometrial cancers. Diagn Pathol. 2008;3:6.
48. Murray SK, Young RH, Scully RE. Uterine endometrioid carcinoma with small nonvillous papillae: an analysis of 26 cases of a favorable-prognosis tumor to be distinguished from serous carcinoma. Int J Surg Pathol. 2000;8:279-289. (Pubitemid 32120690)
49. Parkash V, Carcangiu ML. Endometrioid endometrial adenocarcinoma with psammoma bodies. Am J Surg Pathol. 1997; 21:399-406. (Pubitemid 27184772)
50. Murray SK, Young RH, Scully RE. Unusual epithelial and stromal changes in myoinvasive endometrioid adenocarcinoma: a study of their frequency, associated diagnostic problems, and prognostic significance. Int J Gynecol Pathol. 2003;22: 324-333. (Pubitemid 37152980)
51. Iggo R, Gatter K, Bartek J, et al. Increased expression of mutant forms of p53 oncogene in primary lung cancer. Lancet. 1990;335:675-679. (Pubitemid 20089305)
52. Soong R, Robbins PD, Dix BR, et al. Concordance between p53 protein overexpression and gene mutation in a large series of common human carcinomas. Hum Pathol. 1996;27: 1050-1055. (Pubitemid 26347060)
53. Harris CC, Hollstein M. Clinical implications of the p53 tumor-suppressor gene. N Engl J Med. 1993;329:1318-1327. (Pubitemid 23317333)
54. Geisler JP, Geisler HE, Wiemann MC, et al. p53 expression as a prognostic indicator of 5-year survival in endometrial cancer. Gynecol Oncol. 1999;74:468-471. (Pubitemid 29439892)
55. Alkushi A, Lim P, Coldman A, et al. Interpretation of p53 immunoreactivity in endometrial carcinoma: establishing a clinically relevant cut-off level. Int J Gynecol Pathol. 2004; 23:129-137. (Pubitemid 38391772)
56. Moll UM, Chalas E, Auguste M, et al. Uterine papillary serous carcinoma evolves via a p53-driven pathway. Hum Pathol. 1996;27:1295-1300. (Pubitemid 26415322)
57. Salvesen HB, Iversen OE, Akslen LA. Prognostic significance of angiogenesis and Ki-67, p53, and p21 expression: a population-based endometrial carcinoma study. J Clin Oncol. 1999;17:1382-1390. (Pubitemid 29220843)
58. Egan JA, Ionescu MC, Eapen E, et al. Differential expression of WT1 and p53 in serous and endometrioid carcinomas of the endometrium. Int J Gynecol Pathol. 2004;23:119-122. (Pubitemid 38391770)
59. Halperin R, Zehavi S, Habler L, et al. Comparative immunohistochemical study of endometrioid and serous papillary carcinoma of endometrium. Eur J Gynaecol Oncol. 2001;22:122-126. (Pubitemid 32963063)
60. Soslow RA, Shen PU, Chung MH, et al. Distinctive p53 and mdm2 immunohistochemical expression profiles suggest different pathogenetic pathways in poorly differentiated endometrial carcinoma. Int J Gynecol Pathol. 1998;17:129-134. (Pubitemid 28151011)
61. Hamel NW, Sebo TJ, Wilson TO, et al. Prognostic value of p53 and proliferating cell nuclear antigen expression in endometrial carcinoma. Gynecol Oncol. 1996;62:192-198. (Pubitemid 26274798)
62. Pisani AL, Barbuto DA, Chen D, et al. HER-2/neu, p53, and DNA analyses as prognosticators for survival in endometrial carcinoma. Obstet Gynecol. 1995;85:729-734.
63. Powell B, Soong R, Grieu F, et al. p53 protein overexpression is a prognostic indicator of poor survival in stage I endometrial carcinoma. Int J Oncol. 1999;14:175-179.
64. Athanassiadou P, Athanassiades P, Grapsa D, et al. The prognostic value of PTEN, p53, and beta-catenin in endometrial carcinoma: a prospective immunocytochemical study. Int J Gynecol Cancer. 2007;17:697-704. (Pubitemid 46744009)
65. Lukes AS, Kohler MF, Pieper CF, et al. Multivariable analysis of DNA ploidy, p53, and HER-2/neu as prognostic factors in endometrial cancer. Cancer. 1994;73:2380-2385. (Pubitemid 24129123)
66. Chiesa-Vottero AG, Malpica A, Deavers MT, et al. Immunohistochemical overexpression of p16 and p53 in uterine serous carcinoma and ovarian high-grade serous carcinoma. Int J Gynecol Pathol. 2007;26:328-333. (Pubitemid 46986071)
67. O'Neill CJ, McCluggage WG. p16 expression in the female genital tract and its value in diagnosis. Adv Anat Pathol. 2006;13:8-15. (Pubitemid 44357144)
68. Reid-Nicholson M, Iyengar P, Hummer AJ, et al. Immunophenotypic diversity of endometrial adenocarcinomas: implications for differential diagnosis. Mod Pathol. 2006;19:1091-1100. (Pubitemid 44106724)
69. Yemelyanova A, Ji H, Ie M Shih, et al. Utility of p16 expression for distinction of uterine serous carcinomas from endometrial endometrioid and endocervical adenocarcinomas: immunohistochemical analysis of 201 cases. Am J Surg Pathol. 2009;33:1504-1514.
70. Zhang L, Liu Y, Hao S, et al. IMP2 expression distinguishes endometrioid from serous endometrial adenocarcinomas. Am J Surg Pathol. 2011;35:868-872.
71. Zheng W, Yi X, Fadare O, et al. The oncofetal protein IMP3: a novel biomarker for endometrial serous carcinoma. Am J Surg Pathol. 2008;32:304-315. (Pubitemid 351172146)
72. Geisler JP, Geisler HE, Miller GA, et al. MIB-1 in endometrial carcinoma: prognostic significance with 5-year follow-up. Gynecol Oncol. 1999;75:432-436.
73. Al Kushi A, Lim P, Aquino-Parsons C, et al. Markers of proliferative activity are predictors of patient outcome for lowgrade endometrioid adenocarcinoma but not papillary serous carcinoma of endometrium. Mod Pathol. 2002;15:365-371. (Pubitemid 34326943)
74. Mutter GL, Lin MC, Fitzgerald JT, et al. Altered PTEN expression as a diagnostic marker for the earliest endometrial precancers. J Natl Cancer Inst. 2000;92:924-930.
75. Bussaglia E, del Rio E, Matias-Guiu X, et al. PTEN mutations in endometrial carcinomas: a molecular and clinicopathologic analysis of 38 cases. Hum Pathol. 2000;31:312-317. (Pubitemid 30161349)
76. Kimura F, Watanabe J, Hata H, et al. PTEN immunohistochemical expression is suppressed in G1 endometrioid adenocarcinoma of the uterine corpus. J Cancer Res Clin Oncol. 2004;130:161-168. (Pubitemid 38392349)
77. Lacey JV Jr., Mutter GL, Ronnett BM, et al. PTEN expression in endometrial biopsies as a marker of progression to ndometrial carcinoma. Cancer Res. 2008;68:6014-6020.
78. Darvishian F, Hummer AJ, Thaler HT, et al. Serous endometrial cancers that mimic endometrioid adenocarcinomas: a clinicopathologic and immunohistochemical study of a group of problematic cases. Am J Surg Pathol. 2004;28:1568-1578. (Pubitemid 39564961)
79. Alkushi A, Clarke BA, Akbari M, et al. Identification of prognostically relevant and reproducible subsets of endometrial adenocarcinoma based on clustering analysis of immunostaining data. Mod Pathol. 2007;20:1156-1165. (Pubitemid 47609063)
80. Pallares J, Bussaglia E, Martinez-Guitarte JL, et al. Immunohistochemical analysis of PTEN in endometrial carcinoma: a tissue microarray study with a comparison of four commercial antibodies in correlation with molecular abnormalities. Mod Pathol. 2005;18:719-727. (Pubitemid 40676385)
81. Machin P, Catasus L, Pons C, et al. CTNNB1 mutations and beta-catenin expression in endometrial carcinomas. Hum Pathol. 2002;33:206-212. (Pubitemid 34298736)
82. Schlosshauer PW, Ellenson LH, Soslow RA. Beta-catenin and E-cadherin expression patterns in high-grade endometrial carcinoma are associated with histological subtype. Mod Pathol. 2002;15:1032-1037.
83. Sasano H, Comerford J, Wilkinson DS, et al. Serous papillary adenocarcinoma of the endometrium. Analysis of protooncogene mplification, flow cytometry, estrogen and progesterone receptors, and immunohistochemistry. Cancer. 1990;65: 1545-1551. (Pubitemid 20106113)
84. Alkushi A, Abdul-Rahman ZH, Lim P, et al. Description of a novel system for grading of endometrial carcinoma and comparison with existing grading systems. Am J Surg Pathol. 2005;29:295-304. (Pubitemid 40321964)