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Pathology of Endometrial Carcinoma

  • Sigurd F. Lax
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 943)

Abstract

On a clinicopathological and molecular level, two distinctive types of endometrial carcinoma, type I and type II, can be distinguished. Endometrioid carcinoma, the typical type I carcinoma, seems to develop through an estrogen-driven “adenoma carcinoma” pathway from atypical endometrial hyperplasia/endometrioid intraepithelial neoplasia (AEH/EIN). It is associated with elevated serum estrogen and high body mass index and expresses estrogen and progesterone receptors. They are mostly low grade and show a favorable prognosis. A subset progresses into high-grade carcinoma which is accompanied by loss of receptor expression and accumulation of TP53 mutations and behaves poorly. Other frequently altered genes in type I carcinomas are K-Ras, PTEN, and ß-catenin. Another frequent feature of type I carcinomas is microsatellite instability mainly caused by methylation of the MLH1 promoter. In contrast, the typical type II carcinoma, serous carcinoma, is not estrogen related since it usually occurs in a small uterus with atrophic endometrium. It is often associated with a flat putative precursor lesion called serous endometrial intraepithelial carcinoma (SEIC). The molecular pathogenesis of serous carcinoma seems to be driven by TP53 mutations, which are present in SEIC. Other molecular changes in serous carcinoma detectable by immunohistochemistry involve cyclin E and p16. Since many of the aforementioned molecular changes can be demonstrated by immunohistochemistry, they are useful ancillary diagnostic tools and may further contribute to a future molecular classification of endometrial carcinoma as recently suggested based on The Cancer Genome Atlas (TCGA) data.

Keywords

Endometrial carcinoma Histopathology Molecular pathways Prognosis Grading Typing 

References

  1. 1.
    Jemal A, et al. Cancer statistics, 2008. CA Cancer J Clin. 2008;58(2):71–96.PubMedGoogle Scholar
  2. 2.
    Parazzini F, et al. The epidemiology of endometrial cancer. Gynecol Oncol. 1991;41(1):1–16.PubMedGoogle Scholar
  3. 3.
    Allard JE, Maxwell GL. Race disparities between black and white women in the incidence, treatment, and prognosis of endometrial cancer. Cancer Control. 2009;16(1):53–6.PubMedGoogle Scholar
  4. 4.
    Voskuil DW, et al. Physical activity and endometrial cancer risk, a systematic review of current evidence. Cancer Epidemiol Biomarkers Prev. 2007;16(4):639–48.PubMedGoogle Scholar
  5. 5.
    Enriori CL, Reforzo-Membrives J. Peripheral aromatization as a risk factor for breast and endometrial cancer in postmenopausal women: a review. Gynecol Oncol. 1984;17(1):1–21.PubMedGoogle Scholar
  6. 6.
    Potischman N, et al. Case-control study of endogenous steroid hormones and endometrial cancer. J Natl Cancer Inst. 1996;88(16):1127–35.PubMedGoogle Scholar
  7. 7.
    Carcangiu ML, et al. editors. Tumors of the female reproductive organs. In Kleihues P, Sobin LH, editors. WHO classification of tumours. IARCPress: Lyon; 2014.Google Scholar
  8. 8.
    Bokhman JV. Two pathogenetic types of endometrial carcinoma. Gynecol Oncol. 1983;15(1):10–7.PubMedGoogle Scholar
  9. 9.
    Lax SF. Molecular genetic pathways in various types of endometrial carcinoma: from a phenotypical to a molecular-based classification. Virchows Arch. 2004;444(3):213–23.PubMedGoogle Scholar
  10. 10.
    Sherman ME. Theories of endometrial carcinogenesis: a multidisciplinary approach. Mod Pathol. 2000;13(3):295–308.PubMedGoogle Scholar
  11. 11.
    Yeramian A, et al. Endometrial carcinoma: molecular alterations involved in tumor development and progression. Oncogene. 2013;32(4):403–13.PubMedGoogle Scholar
  12. 12.
    Matias-Guiu X, Prat J. Molecular pathology of endometrial carcinoma. Histopathology. 2013;62(1):111–23.PubMedGoogle Scholar
  13. 13.
    Djordjevic B, et al. Relationship between PTEN, DNA mismatch repair, and tumor histotype in endometrial carcinoma: retained positive expression of PTEN preferentially identifies sporadic non-endometrioid carcinomas. Mod Pathol. 2013;26(10):1401–12.PubMedPubMedCentralGoogle Scholar
  14. 14.
    Lax SF, 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(4):814–24.PubMedGoogle Scholar
  15. 15.
    Tashiro H, et al. Mutations in PTEN are frequent in endometrial carcinoma but rare in other common gynecological malignancies. Cancer Res. 1997;57(18):3935–40.PubMedGoogle Scholar
  16. 16.
    Guan B, et al. Mutation and loss of expression of ARID1A in uterine low-grade endometrioid carcinoma. Am J Surg Pathol. 2011;35(5):625–32.PubMedPubMedCentralGoogle Scholar
  17. 17.
    Kuhn E, et al. Identification of molecular pathway aberrations in uterine serous carcinoma by genome-wide analyses. J Natl Cancer Inst. 2012;104(19):1503–13.PubMedPubMedCentralGoogle Scholar
  18. 18.
    Catasus L, et al. BAX somatic frameshift mutations in endometrioid adenocarcinomas of the endometrium: evidence for a tumor progression role in endometrial carcinomas with microsatellite instability. Lab Invest. 1998;78(11):1439–44.PubMedGoogle Scholar
  19. 19.
    Oda K, et al. High frequency of coexistent mutations of PIK3CA and PTEN genes in endometrial carcinoma. Cancer Res. 2005;65(23):10669–73.PubMedGoogle Scholar
  20. 20.
    Bashir S, et al. Molecular alterations of PIK3CA in uterine carcinosarcoma, clear cell, and serous tumors. Int J Gynecol Cancer. 2014;24(7):1262–7.PubMedGoogle Scholar
  21. 21.
    Rudd ML, et al. A unique spectrum of somatic PIK3CA (p110alpha) mutations within primary endometrial carcinomas. Clin Cancer Res. 2011;17(6):1331–40.PubMedPubMedCentralGoogle Scholar
  22. 22.
    Cancer Genome Atlas Research Network, et al. Integrated genomic characterization of endometrial carcinoma. Nature. 2013;497(7447):67–73.Google Scholar
  23. 23.
    Hussein YR, et al. Clinicopathological analysis of endometrial carcinomas harboring somatic POLE exonuclease domain mutations. Mod Pathol. 2015;28(4):505–14.PubMedGoogle Scholar
  24. 24.
    Talhouk A, et al. A clinically applicable molecular-based classification for endometrial cancers. Br J Cancer. 2015;113(2):299–310.PubMedPubMedCentralGoogle Scholar
  25. 25.
    Wiegand KC, et al. Loss of BAF250a (ARID1A) is frequent in high-grade endometrial carcinomas. J Pathol. 2011;224(3):328–33.PubMedGoogle Scholar
  26. 26.
    An HJ, et al. Molecular characterization of uterine clear cell carcinoma. Mod Pathol. 2004;17(5):530–7.PubMedGoogle Scholar
  27. 27.
    Hoang LN, et al. Targeted mutation analysis of endometrial clear cell carcinoma. Histopathology. 2015;66(5):664–74.PubMedGoogle Scholar
  28. 28.
    Guan B, Wang TL, Shih Ie M. ARID1A, a factor that promotes formation of SWI/SNF-mediated chromatin remodeling, is a tumor suppressor in gynecologic cancers. Cancer Res. 2011;71(21):6718–27.PubMedPubMedCentralGoogle Scholar
  29. 29.
    Sherman ME, et al. Uterine serous carcinoma. A morphologically diverse neoplasm with unifying clinicopathologic features. Am J Surg Pathol. 1992;16(6):600–10.PubMedGoogle Scholar
  30. 30.
    Tashiro H, et al. p53 gene mutations are common in uterine serous carcinoma and occur early in their pathogenesis. Am J Pathol. 1997;150(1):177–85.PubMedPubMedCentralGoogle Scholar
  31. 31.
    Kuhn E, Bahadirli-Talbott A, Shih Ie M. Frequent CCNE1 amplification in endometrial intraepithelial carcinoma and uterine serous carcinoma. Mod Pathol. 2014;27(7):1014–9.PubMedGoogle Scholar
  32. 32.
    Tan MH, et al. Lifetime cancer risks in individuals with germline PTEN mutations. Clin Cancer Res. 2012;18(2):400–7.PubMedPubMedCentralGoogle Scholar
  33. 33.
    Bonadona V, et al. Cancer risks associated with germline mutations in MLH1, MSH2, and MSH6 genes in Lynch syndrome. JAMA. 2011;305(22):2304–10.PubMedGoogle Scholar
  34. 34.
    Hampel H, et al. Screening for Lynch syndrome (hereditary nonpolyposis colorectal cancer) among endometrial cancer patients. Cancer Res. 2006;66(15):7810–7.PubMedGoogle Scholar
  35. 35.
    Mills AM, et al. Lynch syndrome screening should be considered for all patients with newly diagnosed endometrial cancer. Am J Surg Pathol. 2014;38(11):1501–9.PubMedPubMedCentralGoogle Scholar
  36. 36.
    Ferlay J, et al. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer. 2010;127(12):2893–917.PubMedGoogle Scholar
  37. 37.
    Abeler VM, Kjorstad KE. Endometrial adenocarcinoma in Norway. A study of a total population. Cancer. 1991;67(12):3093–103.PubMedGoogle Scholar
  38. 38.
    Han G, et al. Histological features associated with occult lymph node metastasis in FIGO clinical stage I, grade I endometrioid carcinoma. Histopathology. 2014;64(3):389–98.PubMedGoogle Scholar
  39. 39.
    Mai KT, et al. Endometrioid carcinoma of the endometrium with an invasive component of minimal deviation carcinoma. Hum Pathol. 2002;33(8):856–8.PubMedGoogle Scholar
  40. 40.
    Ali A, Black D, Soslow RA. Difficulties in assessing the depth of myometrial invasion in endometrial carcinoma. Int J Gynecol Pathol. 2007;26(2):115–23.PubMedGoogle Scholar
  41. 41.
    Zaino RJ, et al. The significance of squamous differentiation in endometrial carcinoma. Data from a Gynecologic Oncology Group study. Cancer. 1991;68(10):2293–302.PubMedGoogle Scholar
  42. 42.
    Abeler VM, Kjorstad KE. Endometrial adenocarcinoma with squamous cell differentiation. Cancer. 1992;69(2):488–95.PubMedGoogle Scholar
  43. 43.
    Zaino RJ, Kurman RJ. Squamous differentiation in carcinoma of the endometrium: a critical appraisal of adenoacanthoma and adenosquamous carcinoma. Semin Diagn Pathol. 1988;5(2):154–71.PubMedGoogle Scholar
  44. 44.
    Kim KR, Scully RE. Peritoneal keratin granulomas with carcinomas of endometrium and ovary and atypical polypoid adenomyoma of endometrium. A clinicopathological analysis of 22 cases. Am J Surg Pathol. 1990;14(10):925–32.PubMedGoogle Scholar
  45. 45.
    Zaino RJ, et al. Villoglandular adenocarcinoma of the endometrium: a clinicopathologic study of 61 cases: a gynecologic oncology group study. Am J Surg Pathol. 1998;22(11):1379–85.PubMedGoogle Scholar
  46. 46.
    Christopherson WM, Alberhasky RC, Connelly PJ. Carcinoma of the endometrium: I. A clinicopathologic study of clear-cell carcinoma and secretory carcinoma. Cancer. 1982;49(8):1511–23.PubMedGoogle Scholar
  47. 47.
    Tobon H, Watkins GJ. Secretory adenocarcinoma of the endometrium. Int J Gynecol Pathol. 1985;4(4):328–35.PubMedGoogle Scholar
  48. 48.
    Hendrickson MR, Kempson RL. Ciliated carcinoma--a variant of endometrial adenocarcinoma: a report of 10 cases. Int J Gynecol Pathol. 1983;2(1):1–12.PubMedGoogle Scholar
  49. 49.
    Longacre TA, et al. Proposed criteria for the diagnosis of well-differentiated endometrial carcinoma. A diagnostic test for myoinvasion. Am J Surg Pathol. 1995;19(4):371–406.PubMedGoogle Scholar
  50. 50.
    Kurman RJ, Norris HJ. Evaluation of criteria for distinguishing atypical endometrial hyperplasia from well-differentiated carcinoma. Cancer. 1982;49(12):2547–59.PubMedGoogle Scholar
  51. 51.
    Heatley MK. Atypical polypoid adenomyoma: a systematic review of the English literature. Histopathology. 2006;48(5):609–10.PubMedGoogle Scholar
  52. 52.
    Soslow RA, et al. Atypical polypoid adenomyofibroma (APA) versus well-differentiated endometrial carcinoma with prominent stromal matrix: an immunohistochemical study. Int J Gynecol Pathol. 1996;15(3):209–16.PubMedGoogle Scholar
  53. 53.
    Monte NM, et al. Joint loss of PAX2 and PTEN expression in endometrial precancers and cancer. Cancer Res. 2010;70(15):6225–32.PubMedPubMedCentralGoogle Scholar
  54. 54.
    Moreno-Bueno G, et al. Abnormalities of E- and P-cadherin and catenin (beta-, gamma-catenin, and p120ctn) expression in endometrial cancer and endometrial atypical hyperplasia. J Pathol. 2003;199(4):471–8.PubMedGoogle Scholar
  55. 55.
    Ansari-Lari MA, et al. Distinction of endocervical and endometrial adenocarcinomas: immunohistochemical p16 expression correlated with human papillomavirus (HPV) DNA detection. Am J Surg Pathol. 2004;28(2):160–7.PubMedGoogle Scholar
  56. 56.
    Lax SF, et al. Clear cell carcinoma of the endometrium is characterized by a distinctive profile of p53, Ki-67, estrogen, and progesterone receptor expression. Hum Pathol. 1998;29(6):551–8.PubMedGoogle Scholar
  57. 57.
    Lax SF, et al. Comparison of estrogen and progesterone receptor, Ki-67, and p53 immunoreactivity in uterine endometrioid carcinoma and endometrioid carcinoma with squamous, mucinous, secretory, and ciliated cell differentiation. Hum Pathol. 1998;29(9):924–31.PubMedGoogle Scholar
  58. 58.
    Ross JC, et al. Primary mucinous adenocarcinoma of the endometrium. A clinicopathologic and histochemical study. Am J Surg Pathol. 1983;7(8):715–29.PubMedGoogle Scholar
  59. 59.
    Staebler A, et al. Hormone receptor immunohistochemistry and human papillomavirus in situ hybridization are useful for distinguishing endocervical and endometrial adenocarcinomas. Am J Surg Pathol. 2002;26(8):998–1006.PubMedGoogle Scholar
  60. 60.
    Chekmareva M, Ellenson LH, Pirog EC. Immunohistochemical differences between mucinous and microglandular adenocarcinomas of the endometrium and benign endocervical epithelium. Int J Gynecol Pathol. 2008;27(4):547–54.PubMedGoogle Scholar
  61. 61.
    Hendrickson M, et al. Uterine papillary serous carcinoma: a highly malignant form of endometrial adenocarcinoma. Am J Surg Pathol. 1982;6(2):93–108.PubMedGoogle Scholar
  62. 62.
    Ambros RA, et al. Endometrial intraepithelial carcinoma: a distinctive lesion specifically associated with tumors displaying serous differentiation. Hum Pathol. 1995;26(11):1260–7.PubMedGoogle Scholar
  63. 63.
    Wheeler DT, et al. Minimal uterine serous carcinoma: diagnosis and clinicopathologic correlation. Am J Surg Pathol. 2000;24(6):797–806.PubMedGoogle Scholar
  64. 64.
    Al-Hussaini M, et al. WT-1 assists in distinguishing ovarian from uterine serous carcinoma and in distinguishing between serous and endometrioid ovarian carcinoma. Histopathology. 2004;44(2):109–15.PubMedGoogle Scholar
  65. 65.
    Goldstein NS, Uzieblo A. WT1 immunoreactivity in uterine papillary serous carcinomas is different from ovarian serous carcinomas. Am J Clin Pathol. 2002;117(4):541–5.PubMedGoogle Scholar
  66. 66.
    Hirschowitz L, Ganesan R, McCluggage WG. WT1, p53 and hormone receptor expression in uterine serous carcinoma. Histopathology. 2009;55(4):478–82.PubMedGoogle Scholar
  67. 67.
    Giuntoli 2nd RL, et al. Stage I noninvasive and minimally invasive uterine serous carcinoma: comprehensive staging associated with improved survival. Int J Gynecol Cancer. 2012;22(2):273–9.PubMedGoogle Scholar
  68. 68.
    Seward S, et al. Outcomes of patients with uterine serous carcinoma using the revised FIGO staging system. Int J Gynecol Cancer. 2012;22(3):452–6.PubMedGoogle Scholar
  69. 69.
    Kurman RJ, Scully RE. Clear cell carcinoma of the endometrium: an analysis of 21 cases. Cancer. 1976;37(2):872–82.PubMedGoogle Scholar
  70. 70.
    Fadare O, et al. Frequent expression of napsin A in clear cell carcinoma of the endometrium: potential diagnostic utility. Am J Surg Pathol. 2014;38(2):189–96.PubMedGoogle Scholar
  71. 71.
    Fadare O, et al. Utility of alpha-methylacyl-coenzyme-A racemase (p504s) immunohistochemistry in distinguishing endometrial clear cell carcinomas from serous and endometrioid carcinomas. Hum Pathol. 2013;44(12):2814–21.PubMedGoogle Scholar
  72. 72.
    Hoang LN, et al. Immunohistochemical characterization of prototypical endometrial clear cell carcinoma--diagnostic utility of HNF-1beta and oestrogen receptor. Histopathology. 2014;64(4):585–96.PubMedGoogle Scholar
  73. 73.
    Abeler VM, Kjorstad KE. Clear cell carcinoma of the endometrium: a histopathological and clinical study of 97 cases. Gynecol Oncol. 1991;40(3):207–17.PubMedGoogle Scholar
  74. 74.
    Webb GA, Lagios MD. Clear cell carcinoma of the endometrium. Am J Obstet Gynecol. 1987;156(6):1486–91.PubMedGoogle Scholar
  75. 75.
    Carcangiu ML, Chambers JT. Early pathologic stage clear cell carcinoma and uterine papillary serous carcinoma of the endometrium: comparison of clinicopathologic features and survival. Int J Gynecol Pathol. 1995;14(1):30–8.PubMedGoogle Scholar
  76. 76.
    Alkushi A, et al. High-grade endometrial carcinoma: serous and grade 3 endometrioid carcinomas have different immunophenotypes and outcomes. Int J Gynecol Pathol. 2010;29(4):343–50.PubMedGoogle Scholar
  77. 77.
    Quddus MR, et al. Minor serous and clear cell components adversely affect prognosis in “mixed-type” endometrial carcinomas: a clinicopathologic study of 36 stage-I cases. Reprod Sci. 2010;17(7):673–8.PubMedGoogle Scholar
  78. 78.
    McConechy MK, et al. Use of mutation profiles to refine the classification of endometrial carcinomas. J Pathol. 2012;228(1):20–30.PubMedPubMedCentralGoogle Scholar
  79. 79.
    Tafe LJ, et al. Endometrial and ovarian carcinomas with undifferentiated components: clinically aggressive and frequently underrecognized neoplasms. Mod Pathol. 2010;23(6):781–9.PubMedGoogle Scholar
  80. 80.
    Silva EG, et al. Association of low-grade endometrioid carcinoma of the uterus and ovary with undifferentiated carcinoma: a new type of dedifferentiated carcinoma? Int J Gynecol Pathol. 2006;25(1):52–8.PubMedGoogle Scholar
  81. 81.
    Altrabulsi B, et al. Undifferentiated carcinoma of the endometrium. Am J Surg Pathol. 2005;29(10):1316–21.PubMedGoogle Scholar
  82. 82.
    Seidman JD, Chauhan S. Evaluation of the relationship between adenosarcoma and carcinosarcoma and a hypothesis of the histogenesis of uterine sarcomas. Int J Gynecol Pathol. 2003;22(1):75–82.PubMedGoogle Scholar
  83. 83.
    Nordal RR, et al. An evaluation of prognostic factors in uterine carcinosarcoma. Gynecol Oncol. 1997;67(3):316–21.PubMedGoogle Scholar
  84. 84.
    de Brito PA, Silverberg SG, Orenstein JM. Carcinosarcoma (malignant mixed mullerian (mesodermal) tumor) of the female genital tract: immunohistochemical and ultrastructural analysis of 28 cases. Hum Pathol. 1993;24(2):132–42.PubMedGoogle Scholar
  85. 85.
    Silverberg SG, et al. Carcinosarcoma (malignant mixed mesodermal tumor) of the uterus. A Gynecologic Oncology Group pathologic study of 203 cases. Int J Gynecol Pathol. 1990;9(1):1–19.PubMedGoogle Scholar
  86. 86.
    Gonzalez-Bosquet E, et al. Carcinoid tumor of the uterine corpus. A case report. J Reprod Med. 1998;43(9):844–6.PubMedGoogle Scholar
  87. 87.
    Chetty R, Clark SP, Bhathal PS. Carcinoid tumour of the uterine corpus. Virchows Arch A Pathol Anat Histopathol. 1993;422(1):93–5.PubMedGoogle Scholar
  88. 88.
    Starzynski S, Kubicka-Pertkiewicz M. Carcinoid of the uterine corpus. Patol Pol. 1978;29(2):237–40.PubMedGoogle Scholar
  89. 89.
    Huntsman DG, et al. Small-cell carcinoma of the endometrium. A clinicopathological study of sixteen cases. Am J Surg Pathol. 1994;18(4):364–75.PubMedGoogle Scholar
  90. 90.
    van Hoeven KH, et al. Small cell neuroendocrine carcinoma of the endometrium. Int J Gynecol Pathol. 1995;14(1):21–9.PubMedGoogle Scholar
  91. 91.
    Deodhar KK, et al. Large cell neuroendocrine carcinoma of the endometrium: an extremely uncommon diagnosis, but worth the efforts. J Cancer Res Ther. 2011;7(2):211–3.PubMedGoogle Scholar
  92. 92.
    Zaino RJ, et al. The prognostic value of nuclear versus architectural grading in endometrial adenocarcinoma: a Gynecologic Oncology Group study. Int J Gynecol Pathol. 1994;13(1):29–36.PubMedGoogle Scholar
  93. 93.
    Zaino RJ, 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(1):81–6.PubMedGoogle Scholar
  94. 94.
    Ayhan A, et al. The prognostic value of nuclear grading and the revised FIGO grading of endometrial adenocarcinoma. Int J Gynecol Pathol. 2003;22(1):71–4.PubMedGoogle Scholar
  95. 95.
    Sagae S, et al. The reproducibility of a binary tumor grading system for uterine endometrial endometrioid carcinoma, compared with FIGO system and nuclear grading. Oncology. 2004;67(5-6):344–50.PubMedGoogle Scholar
  96. 96.
    Lax SF, et al. A binary architectural grading system for uterine endometrial endometrioid carcinoma has superior reproducibility compared with FIGO grading and identifies subsets of advance-stage tumors with favorable and unfavorable prognosis. Am J Surg Pathol. 2000;24(9):1201–8.PubMedGoogle Scholar
  97. 97.
    Guan H, et al. Prognosis and reproducibility of new and existing binary grading systems for endometrial carcinoma compared to FIGO grading in hysterectomy specimens. Int J Gynecol Cancer. 2011;21(4):654–60.PubMedGoogle Scholar
  98. 98.
    Alkushi A, et al. Description of a novel system for grading of endometrial carcinoma and comparison with existing grading systems. Am J Surg Pathol. 2005;29(3):295–304.PubMedGoogle Scholar
  99. 99.
    Zaino RJ. FIGO staging of endometrial adenocarcinoma: a critical review and proposal. Int J Gynecol Pathol. 2009;28(1):1–9.PubMedGoogle Scholar
  100. 100.
    Abu-Rustum NR, et al. The revised 2009 FIGO staging system for endometrial cancer: should the 1988 FIGO stages IA and IB be altered? Int J Gynecol Cancer. 2011;21(3):511–6.PubMedGoogle Scholar
  101. 101.
    Haltia UM, et al. FIGO 1988 versus 2009 staging for endometrial carcinoma: a comparative study on prediction of survival and stage distribution according to histologic subtype. J Gynecol Oncol. 2014;25(1):30–5.PubMedPubMedCentralGoogle Scholar
  102. 102.
    Kim HS, et al. Lymphadenectomy increases the prognostic value of the revised 2009 FIGO staging system for endometrial cancer: a multi-center study. Eur J Surg Oncol. 2012;38(3):230–7.PubMedGoogle Scholar
  103. 103.
    Werner HM, et al. Revision of FIGO surgical staging in 2009 for endometrial cancer validates to improve risk stratification. Gynecol Oncol. 2012;125(1):103–8.PubMedGoogle Scholar
  104. 104.
    Korczynski J, et al. Comparison of FIGO 1989 and 2009 recommendations on staging of endometrial carcinoma: pathologic analysis and cervical status in 123 consecutive cases. Int J Gynecol Pathol. 2011;30(4):328–34.PubMedGoogle Scholar
  105. 105.
    Bosse T, et al. Substantial lymph-vascular space invasion (LVSI) is a significant risk factor for recurrence in endometrial cancer - a pooled analysis of PORTEC 1 and 2 trials. Eur J Cancer. 2015;51(13):1742–50.PubMedGoogle Scholar
  106. 106.
    Hachisuga T, et al. The grading of lymphovascular space invasion in endometrial carcinoma. Cancer. 1999;86(10):2090–7.PubMedGoogle Scholar
  107. 107.
    Morrow CP, et al. Relationship between surgical-pathological risk factors and outcome in clinical stage I and II carcinoma of the endometrium: a Gynecologic Oncology Group study. Gynecol Oncol. 1991;40(1):55–65.PubMedGoogle Scholar
  108. 108.
    Han KH, et al. Peritoneal cytology: a risk factor of recurrence for non-endometrioid endometrial cancer. Gynecol Oncol. 2014;134(2):293–6.PubMedGoogle Scholar
  109. 109.
    Group AES, et al. Adjuvant external beam radiotherapy in the treatment of endometrial cancer (MRC ASTEC and NCIC CTG EN.5 randomised trials): pooled trial results, systematic review, and meta-analysis. Lancet. 2009;373(9658):137–46.Google Scholar
  110. 110.
    Creutzberg CL, et al. Outcome of high-risk stage IC, grade 3, compared with stage I endometrial carcinoma patients: the Postoperative Radiation Therapy in Endometrial Carcinoma Trial. J Clin Oncol. 2004;22(7):1234–41.PubMedGoogle Scholar
  111. 111.
    Abdelazim IA, et al. Accuracy of endometrial sampling compared to conventional dilatation and curettage in women with abnormal uterine bleeding. Arch Gynecol Obstet. 2015;291(5):1121–6.PubMedGoogle Scholar
  112. 112.
    Thanachaiviwat A, et al. Accuracy of preoperative curettage in determining tumor type and grade in endometrial cancer. J Med Assoc Thai. 2011;94(7):766–71.PubMedGoogle Scholar
  113. 113.
    Wang XY, et al. Accuracy of tumor grade by preoperative curettage and associated clinicopathologic factors in clinical stage I endometriod adenocarcinoma. Chin Med J (Engl). 2009;122(16):1843–6.Google Scholar
  114. 114.
    Obermair A, et al. Endometrial cancer: accuracy of the finding of a well differentiated tumor at dilatation and curettage compared to the findings at subsequent hysterectomy. Int J Gynecol Cancer. 1999;9(5):383–6.PubMedGoogle Scholar
  115. 115.
    Egle D, et al. Validation of intraoperative risk assessment on frozen section for surgical management of endometrial carcinoma. Gynecol Oncol. 2008;110(3):286–92.PubMedGoogle Scholar
  116. 116.
    Atad J, et al. Intraoperative frozen section examination of myometrial invasion depth in patients with endometrial carcinoma. Int J Gynecol Cancer. 1994;4(5):352–5.PubMedGoogle Scholar
  117. 117.
    ASTEC study group, et al. Efficacy of systematic pelvic lymphadenectomy in endometrial cancer (MRC ASTEC trial): a randomised study. Lancet. 2009;373(9658):125–36.Google Scholar
  118. 118.
    Siufi DF, et al. Lymphadenectomy in early stage endometrial cancer: a critical review of the current literature. Tumori. 2014;100(5):477–85.PubMedGoogle Scholar
  119. 119.
    Mitamura T, et al. Lymphadenectomy can be omitted for low-risk endometrial cancer based on preoperative assessments. J Gynecol Oncol. 2014;25(4):301–5.PubMedPubMedCentralGoogle Scholar
  120. 120.
    Todo Y, et al. Tailoring lymphadenectomy according to the risk of lymph node metastasis in endometrial cancer. J Obstet Gynaecol Res. 2014;40(2):317–21.PubMedGoogle Scholar
  121. 121.
    Bogani G, et al. Role of pelvic and para-aortic lymphadenectomy in endometrial cancer: current evidence. J Obstet Gynaecol Res. 2014;40(2):301–11.PubMedPubMedCentralGoogle Scholar
  122. 122.
    Touboul C, et al. Sentinel lymph node in endometrial cancer: a review. Curr Oncol Rep. 2013;15(6):559–65.PubMedGoogle Scholar
  123. 123.
    Abu-Rustum NR. Sentinel lymph node mapping for endometrial cancer: a modern approach to surgical staging. J Natl Compr Canc Netw. 2014;12(2):288–97.PubMedGoogle Scholar
  124. 124.
    Leitao Jr MM, et al. Impact of incorporating an algorithm that utilizes sentinel lymph node mapping during minimally invasive procedures on the detection of stage IIIC endometrial cancer. Gynecol Oncol. 2013;129(1):38–41.PubMedGoogle Scholar
  125. 125.
    Pristauz G, et al. How accurate is frozen section histology of pelvic lymph nodes in patients with endometrial cancer? Gynecol Oncol. 2009;115(1):12–7.PubMedGoogle Scholar

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© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Department of PathologyHospital Graz Süd-West, Academic Teaching Hospital of the Medical University GrazGrazAustria

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