Endometrial stromal tumors: The new who classification

Advances in Anatomic Pathology

Volumn 21, Issue 6, 2014, Pages 383-393

  Conklin, Christopher M J ^a   Longacre, Teri A ^b  

^a SURREY MEMORIAL HOSPITAL   (Canada)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

High grade endometrial stromal sarcoma; Immunohistochemistry; Low grade endometrial stromal sarcoma; Molecular genetics; Undifferentiated uterine sarcoma

Indexed keywords

JAZF1 PROTEIN, HUMAN; ONCOPROTEIN; POLYCOMB REPRESSIVE COMPLEX 2; SUZ12 PROTEIN, HUMAN; TUMOR MARKER; TUMOR PROTEIN; YWHAE-FAM22 FUSION PROTEIN, HUMAN;

BIOPSY; CANCER GRADING; CELL DIFFERENTIATION; CHEMISTRY; CLASSIFICATION; DIFFERENTIAL DIAGNOSIS; ENDOMETRIAL STROMAL TUMOR; ENDOMETRIUM SARCOMA; ENDOMETRIUM TUMOR; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE FUSION; GENE TRANSLOCATION; GENETIC PREDISPOSITION; GENETICS; HUMAN; IMMUNOHISTOCHEMISTRY; NOMENCLATURE; PATHOLOGY; PHENOTYPE; PREDICTIVE VALUE;

BIOPSY; CELL DIFFERENTIATION; DIAGNOSIS, DIFFERENTIAL; ENDOMETRIAL NEOPLASMS; ENDOMETRIAL STROMAL TUMORS; FEMALE; GENE FUSION; GENETIC PREDISPOSITION TO DISEASE; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION, FLUORESCENCE; NEOPLASM GRADING; NEOPLASM PROTEINS; ONCOGENE PROTEINS, FUSION; PHENOTYPE; POLYCOMB REPRESSIVE COMPLEX 2; PREDICTIVE VALUE OF TESTS; SARCOMA, ENDOMETRIAL STROMAL; TERMINOLOGY AS TOPIC; TRANSLOCATION, GENETIC; TUMOR MARKERS, BIOLOGICAL;

EID: 84914144760     PISSN: 10724109     EISSN: 15334031     Source Type: Journal    
DOI: 10.1097/PAP.0000000000000046     Document Type: Review

References (94)

1. Oliva E, Clement PB, Young RH. Endometrial stromal tumors: An update on a group of tumors with a protean phenotype. Adv Anat Pathol. 2000;7:257-281
2. Chiang S, Oliva E. Recent developments in uterine mesenchymal neoplasms. Histopathology. 2013;62:124-137
3. D'Angelo E, Prat J. Uterine sarcomas: A review. Gynecol Oncol. 2010;116:131-139
4. Rauh-Hain JA, del CarmenMG. Endometrial stromal sarcoma: A systematic review. Obstet Gynecol. 2013;122:676-683
5. Norris HJ, Taylor HB. Mesenchymal tumors of the uterus. I. A clinical and pathological study of 53 endometrial stromal tumors. Cancer. 1966;19:755-766
6. Kurman RJ, Carcangiu ML, Herrington CS, et al. WHO Classification of Tumors of Female Reproductive Organs. 4th ed. Lyon, France: IARC Press; 2014:307
7. Lee C-H, Mariño-Enriquez A, Ou W, et al. The clinicopathologic features of YWHAE-FAM22 endometrial stromal sarcomas: A histologically high-grade and clinically aggressive tumor. Test Site. 2012;36:641-653
8. Dionigi A, Oliva E, Clement PB, et al. Endometrial stromal nodules and endometrial stromal tumors with limited infiltration: A clinicopathologic study of 50 cases. Am J Surg Pathol. 2002;26:567-581
9. Tavassoli FA, Norris HJ. Mesenchymal tumours of the uterus. VII. A clinicopathological study of 60 endometrial stromal nodules.∗. Histopathology. 1981;5:1-10
10. Chang KL, Crabtree GS, Lim-Tan SK, et al. Primary uterine endometrial stromal neoplasms: A clinicopathologic study of 117 cases. Am J Surg Pathol. 1990;14:415-438
11. Evans HL. Endometrial stromal sarcoma and poorly differentiated endometrial sarcoma. Cancer. 1982;50:2170-2182
12. Stadsvold JL, Molpus KL, Baker JJ, et al. Conservative management of a myxoid endometrial stromal sarcoma in a 16- year-old nulliparous woman. Gynecol Oncol. 2005;99:243-245
13. Young RH, Prat J, Scully RE. Endometrioid stromal sarcomas of the ovary. A clinicopathologic analysis of 23 cases. Cancer. 1984;53:1143-1155
14. Young RH, Scully RE. Sarcomas metastatic to the ovary: A report of 21 cases. Int J Gynecol Pathol. 1990;9:231-252
15. Aubry M-C, Myers JL, Colby TV, et al. Endometrial stromal sarcoma metastatic to the lung: A detailed analysis of 16 patients. Am J Surg Pathol. 2002;26:440-449
16. Riopel J, Plante M, Renaud M-C, et al. Lymph node metastases in low-grade endometrial stromal sarcoma. Gynecol Oncol. 2005;96:402-406
17. Beer TW, Buchanan R, Buckley CH. Uterine stromal sarcoma following tamoxifen treatment. J Clin Pathol. 1995;48:596
18. Meredith RF, Eisert DR, Kaka Z, et al. An excess of uterine sarcomas after pelvic irradiation. Cancer. 1986;58:2003-2007
19. Fekete PS, Vellios F. The clinical and histologic spectrum of endometrial stromal neoplasms: A report of 41 cases. Int J Gynecol Pathol. 1984;3:198-212
20. Oliva E, Young RH, Clement PB, et al. Myxoid and fibrous endometrial stromal tumors of the uterus: A report of 10 cases. Int J Gynecol Pathol. 1999;18:310-319
21. Oliva E, Clement PB, Young RH, et al. Mixed endometrial stromal and smooth muscle tumors of the uterus: A clinicopathologic study of 15 cases. Am J Surg Pathol. 1998;22: 997-1005
22. McCluggage WG, Bharucha H, Toner PG. Endometrial stromal sarcoma with sex cord-like areas and focal rhabdoid differentiation. Histopathology. 1996;29:369-374
23. Clement PB, Scully RE. Endometrial stromal sarcomas of the uterus with extensive endometrioid glandular differentiation: A report of three cases that caused problems in differential diagnosis. Int J Gynecol Pathol. 1992;11:163-137
24. Leath CA III, Huh WK, Hyde J Jr, et al. A multi-institutional review of outcomes of endometrial stromal sarcoma. Gynecol Oncol. 2007;105:630-634
25. Gadducci A, Cosio S, Romanini A, et al. The management of patients with uterine sarcoma: A debated clinical challenge. Crit Rev Oncol Hematol. 2008;65:129-142
26. Weitmann HD, Knocke TH, Kucera H, et al. Radiation therapy in the treatment of endometrial stromal sarcoma. Int J Radiat Oncol Biol Phys. 2001;49:739-748
27. Reich O, Regauer S. Hormonal therapy of endometrial stromal sarcoma. Curr Opin Oncol. 2007;19:347-352
28. Silverberg SG, Kurman RJ. Endometrial stromal tumors. Atlas of Tumor Pathology Tumors of the Uterine Corpus and Gestational Trophoblastic Disease Third Series, Fascicle 3. Armed Forces Intitute of Pathology 1992:91-112
29. Kurihara S, Oda Y, Ohishi Y, et al. Endometrial stromal sarcomas and related high-grade sarcomas: immunohistochemical and molecular genetic study of 31 cases. Am J Surg Pathol. 2008;32:1228-1238
30. Cheung AN, Ng WF, Chung LP, et al. Mixed low grade and high grade endometrial stromal sarcoma of uterus: differences on immunohistochemistry and chromosome in situ hybridisation. J Clin Pathol. 1996;49:604-607
31. Amant F, Woestenborghs H, Vandenbroucke V, et al. Transition of endometrial stromal sarcoma into high-grade sarcoma. Gynecol Oncol. 2006;103:1137-1140
32. Ohta Y, Suzuki T, Omatsu M, et al. Transition from low-grade endometrial stromal sarcoma to high-grade endometrial stromal sarcoma. Int J Gynecol Pathol. 2010;29:374-377
33. Soslow RA, Longacre TA. Endometrial Stromal Tumors. Uterine Pathology. Cambridge, England: Cambridge University Press; 2012:251-263
34. Kurman RJ, Ellenson LH, Ronnett BM. Mesenchymal Tumors of the Uterus. Blaustein's Pathology of the Female Genital Tract. Sixth. New York: Springer; 2011:453-527
35. Silverberg SG, Kurman RJ. Atlas of Tumor Pathology. Tumors of the Uterine Corpus and Gestational Trophoblastic Disease. Third Series, Fascicle 3. Armed Forces Institute of Pathology; Washington, D.C., 1992
36. Chew I, Oliva E. Endometrial stromal sarcomas: A review of potential prognostic factors. Adv Anat Pathol. 2010;17:113-120
37. Baker RJ, Hildebrandt RH, Rouse RV, et al. Inhibin and CD99 (MIC2) expression in uterine stromal neoplasms with sex-cord-like elements. Hum Pathol. 1999;30:671-679
38. Gadducci A, Sartori E, Landoni F, et al. Endometrial stromal sarcoma: Analysis of treatment failures and survival. Gynecol Oncol. 1996;63:247-253
39. Blom R, Malmström H, Guerrieri C. Endometrial stromal sarcoma of the uterus: A clinicopathologic, DNA flow cytometric, p53, and mdm-2 analysis of 17 cases. Int J Gynecol Cancer. 1999;9:98-104
40. Chu P, Arber DA. Paraffin-section detection of CD10 in 505 nonhematopoietic neoplasms frequent expression in renal cell carcinoma and endometrial stromal sarcoma. Am J Clin Pathol. 2000;113:374-382
41. Chu PG, Arber DA, Weiss LM, et al. Utility of CD10 in distinguishing between endometrial stromal sarcoma and uterine smooth muscle tumors: An immunohistochemical comparison of 34 cases. Mod Pathol. 2001;14:465-471
42. McCluggage WG, Sumathi VP, Maxwell P. CD10 is a sensitive and diagnostically useful immunohistochemical marker of normal endometrial stroma and of endometrial stromal neoplasms. Histopathology. 2001;39:273-278
43. Toki T, Shimizu M, Takagi Y, et al. CD10 is a marker for normal and neoplastic endometrial stromal cells. Int J Gynecol Pathol. 2002;21:41-47
44. Oliva E, Young RH, Amin MB, et al. An immunohistochemical analysis of endometrial stromal and smooth muscle tumors of the guterus: A study of 54 cases emphasizing the importance of using a panel because of overlap in immunoreactivity for individual antibodies. Am J Surg Pathol. 2002;26:403-412
45. Irving JA, Carinelli S, Prat J. Uterine tumors resembling ovarian sex cord tumors are polyphenotypic neoplasms with true sex cord differentiation. Mod Pathol. 2006;19:17-24
46. De Leval L, Waltregny D, Boniver J, et al. Use of histone deacetylase 8 (HDAC8), a new marker of smooth muscle differentiation, in the classification of mesenchymal tumors of the uterus. Am J Surg Pathol. 2006;30:319-327
47. Devaney K, Tavassoli FA. Immunohistochemistry as a diagnostic aid in the interpretation of unusual mesenchymal tumors of the uterus. Mod Pathol Off J U S Can Acad Pathol Inc. 1991;4:225-231
48. Farhood AI, Abrams J. Immunohistochemistry of endometrial stromal sarcoma. Hum Pathol. 1991;22:224-230
49. Franquemont DW, Frierson HF Jr, Mills SE. An immunohistochemical study of normal endometrial stroma and endometrial stromal neoplasms: evidence for smooth muscle differentiation. Am J Surg Pathol. 1991;15:861-870
50. Lillemoe TJ, Perrone T, Norris HJ, et al. Myogenous phenotype of epithelial-like areas in endometrial stromal sarcomas. Arch Pathol Lab Med. 1991;115:215-219
51. Nucci MR, O'Connell JT, Huettner PC, et al. h-Caldesmon expression effectively distinguishes endometrial stromal tumors from uterine smooth muscle tumors. Am J Surg Pathol. 2001;25:455-463
52. Lee C-H, Ali RH, Rouzbahman M, et al. Cyclin D1 as a diagnostic immunomarker for endometrial stromal sarcoma with YWHAE-FAM22 rearrangement. Am J Surg Pathol. 2012;36:1562-1570
53. Balleine RL, Earls PJ, Webster LR, et al. Expression of progesterone receptor A and B isoforms in low-grade endometrial stromal sarcoma. Int J Gynecol Pathol. 2004;23:138-144
54. Chu MC,Mor G, Lim C, et al. Low-grade endometrial stromal sarcoma: hormonal aspects.∗. Gynecol Oncol. 2003;90:170-176
55. Jakate K, Azimi F, Ali RH, et al. Endometrial sarcomas: An immunohistochemical and JAZF1 re-arrangement study in low-grade and undifferentiated tumors. Mod Pathol. 2013;26:95-105
56. Reich O, Regauer S, Urdl W, et al. Expression of oestrogen and progesterone receptors in low-grade endometrial stromal sarcomas. Br J Cancer. 2000;82:1030-1034
57. Bhargava R, Shia J, Hummer AJ, et al. Distinction of endometrial stromal sarcomas from "hemangiopericytomatous" tumors using a panel of immunohistochemical stains. Mod Pathol. 2005;18:40-47
58. Fukunaga M, Miyazawa Y, Ushigome S. Endometrial lowgrade stromal sarcoma with ovarian sex cord-like differentiation: report of two cases with an immunohistochemical and flow cytometric study. Pathol Int. 1997;47:412-415
59. Ohta Y, Suzuki T, Kojima M, et al. Low-grade endometrial stromal sarcoma with an extensive epithelial-like element. Pathol Int. 2003;53:246-251
60. Sumathi VP, Al-Hussaini M, Connolly LE, et al. Endometrial stromal neoplasms are immunoreactive with WT-1 antibody. Int J Gynecol Pathol. 2004;23:241-247
61. Zámečnćkl M, Michal M. Endometrial stromal nodule with retiform sex-cord-like differentiation. Pathol Res Pract. 1998;194:449-453
62. Kurihara S, Oda Y, Ohishi Y, et al. Coincident expression of bcatenin and cyclin D1 in endometrial stromal tumors and related high-grade sarcomas. Mod Pathol. 2010;23:225-234
63. Ng TL, Gown AM, Barry TS, et al. Nuclear beta-catenin in mesenchymal tumors. Mod Pathol. 2005;18:68-74
64. Jung C-K, Jung J-H, Lee A, et al. Diagnostic use of nuclear bcatenin expression for the assessment of endometrial stromal tumors. Mod Pathol. 2008;21:756-763
65. Moinfar F, Regitnig P, Tabrizi AD, et al. Expression of androgen receptors in benign and malignant endometrial stromal neoplasms. Virchows Arch. 2004;444:410-414
66. Reich O, Regauer S. Aromatase expression in low-grade endometrial stromal sarcomas: An immunohistochemical study. Mod Pathol. 2004;17:104-108
67. Park J-Y, Kim K-R, Nam J-H. Immunohistochemical analysis for therapeutic targets and prognostic markers in low-grade endometrial stromal sarcoma. Int J Gynecol Cancer. 2013; 23:81-89
68. Caudell JJ, Deavers MT, Slomovitz BM, et al. Imatinib mesylate (gleevec)-targeted kinases are expressed in uterine sarcomas. Appl Immunohistochem Mol Morphol. 2005;13: 167-170
69. Sardinha R, Herná ndez T, Fraile S, et al. Endometrial stromal tumors: immunohistochemical and molecular analysis of potential targets of tyrosine kinase inhibitors. Clin Sarcoma Res. 2013;3:3-13
70. Lee C-H, Hoang LN, Yip S, et al. Frequent expression of KIT in endometrial stromal sarcoma with YWHAE genetic rearrangement. Mod Pathol. 2014;27:751-757
71. Cheng X, Yang G, Schmeler KM, et al. Recurrence patterns and prognosis of endometrial stromal sarcoma and the potential of tyrosine kinase-inhibiting therapy. Gynecol Oncol. 2011;121:323-327
72. Rushing RS, Shajahan S, Chendil D, et al. Uterine sarcomas express KIT protein but lack mutation (s) in exon 11 or 17 of cKIT. Gynecol Oncol. 2003;91:9-14
73. Koontz JI, Soreng AL, Nucci M, et al. Frequent fusion of the JAZF1 and JJAZ1 genes in endometrial stromal tumors. Proc Natl Acad Sci. 2001;98:6348-6353
74. Chiang S, Ali R, Melnyk N, et al. Frequency of known gene rearrangements in endometrial stromal tumors. Am J Surg Pathol. 2011;35:1364-1372
75. Hrzenjak A, Moinfar F, Tavassoli FA, et al. JAZF1/JJAZ1 gene fusion in endometrial stromal sarcomas: molecular analysis by reverse transcriptase-polymerase chain reaction optimized for paraffin-embedded tissue. J Mol Diagn. 2005;7:388-395
76. Nucci MR, Harburger D, Koontz J, et al. Molecular analysis of the JAZF1-JJAZ1 gene fusion by RT-PCR and fluorescence in situ hybridization in endometrial stromal neoplasms. Am J Surg Pathol. 2007;31:65-70
77. Oliva E, de Leval L, Soslow RA, et al. High frequency of JAZF1-JJAZ1 gene fusion in endometrial stromal tumors with smooth muscle differentiation by interphase FISH detection. Am J Surg Pathol. 2007;31:1277-1284
78. Lee C-H, Ou W-B, Mariño-Enriquez A, et al. 14-3-3 fusion oncogenes in high-grade endometrial stromal sarcoma. Proc Natl Acad Sci. 2012;109:929-934
79. Lax SF. Molecular genetic changes in epithelial, stromal and mixed neoplasms of the endometrium. Pathology (Phila). 2007;39:46-54
80. Micci F, Panagopoulos I, Bjerkehagen B, et al. Consistent rearrangement of chromosomal band 6p21 with generation of fusion genes JAZF1/PHF1 and EPC1/PHF1 in endometrial stromal sarcoma. Cancer Res. 2006;66:107-112
81. Panagopoulos I, Micci F, Thorsen J, et al. Novel fusion of MYST/Esa1-associated factor 6 and PHF1 in endometrial stromal sarcoma. PloS One. 2012;7:e39354
82. Sandberg AA. The cytogenetics and molecular biology of endometrial stromal sarcoma. Cytogenet Genome Res. 2007; 118:182-189
83. Chiang S, Oliva E. Cytogenetic and molecular aberrations in endometrial stromal tumors. Hum Pathol. 2011;42:609-617
84. Huang H-Y, Ladanyi M, Soslow RA. Molecular detection of JAZF1-JJAZ1 gene fusion in endometrial stromal neoplasms with classic and variant histology: evidence for genetic heterogeneity. Am J Surg Pathol. 2004;28:224-232
85. Li H, Wang J, Mor G, et al. A neoplastic gene fusion mimics trans-splicing of RNAs in normal human cells. Science. 2008;321:1357-1361
86. O'Meara E, Stack D, Lee C-H, et al. Characterization of the chromosomal translocation t (10; 17)(q22; p13) in clear cell sarcoma of kidney. J Pathol. 2012;227:72-80
87. Fehr A, Hansson MC, Kindblom L-G, et al. YWHAE- FAM22 gene fusion in clear cell sarcoma of the kidney. J Pathol. 2012;227:e5-e7
88. Goldblum JR, Clement PB, Hart WR. Adenomyosis with sparse glands. A potential mimic of low-grade endometrial stromal sarcoma. Am J Clin Pathol. 1995;103:218-223
89. Lloreta J, Prat J. Endometrial stromal nodule with smooth and skeletal muscle components simulating stromal sarcoma. Int J Gynecol Pathol. 1992;11:293-298
90. Oliva E, Young RH, Clement PB, et al. Cellular benign mesenchymal tumors of the uterus. A comparative morphologic and immunohistochemical analysis of 33 highly cellular leiomyomas and six endometrial stromal nodules, two frequently confused tumors. Am J Surg Pathol. 1995;19:757-768
91. Vang R, Kempson RL. Perivascular epithelioid cell tumor (PEComa') of the uterus: A subset of HMB-45-positive epithelioid mesenchymal neoplasms with an uncertain relationship to pure smooth muscle tumors. Am J Surg Pathol. 2002;26:1-13
92. Altrabulsi B, Malpica A, Deavers MT, et al. Undifferentiated carcinoma of the endometrium. Am J Surg Pathol. 2005;29: 1316-1321
93. Tafe LJ, Garg K, Chew I, et al. Endometrial and ovarian carcinomas with undifferentiated components: clinically aggressive and frequently underrecognized neoplasms. Mod Pathol. 2010;23:781-789
94. Hurrell DP, McCluggage WG. Uterine tumour resembling ovarian sex cord tumour is an immunohistochemically polyphenotypic neoplasm which exhibits coexpression of epithelial, myoid and sex cord markers. J Clin Pathol. 2007;60:1148-1154.