Advertisement

Uterine sarcomas and rare uterine mesenchymal tumors with malignant potential. Diagnostic guidelines of the French Sarcoma Group and the Rare Gynecological Tumors Group

Published:September 13, 2022DOI:https://doi.org/10.1016/j.ygyno.2022.07.031

      Highlights

      • Uterine sarcomas are divided into complex and simple genomic sarcomas.
      • Leiomyosarcoma and pleomorphic undifferentiated sarcoma belong to the first group.
      • Endometrial stromal sarcomas, NTRK, and COL1A1 fused sarcomas belong to the second.
      • sarcomas with NTRK, ALK, COL1A1-PDGFB fusions can benefit from targeted therapy.
      • Integration of molecular results with histology improve diagnosis and treatment.

      Abstract

      The landscape of uterine sarcomas is becoming increasingly complex with the description of new entities associated with recurrent molecular alterations. Uterine sarcomas, as well as soft tissue sarcomas, can be distinguished into complex genomic sarcomas and simple genomic sarcomas. Leiomyosarcoma and pleomorphic type undifferentiated uterine sarcoma belong to the first group. Low-grade and high-grade endometrial stromal sarcomas, NTRK, COL1A1::PDGFB, ALK, RET, ROS1 associated sarcomas, and SMARCA4 deficient uterine sarcoma belong to the second group. Leiomyosarcoma is the most common uterine sarcoma followed by endometrial stromal sarcomas. Three different histologic subtypes of leiomyosarcomas are recognized with distinct diagnostic criteria and different clinical outcomes, the myxoid and epithelioid leiomyosarcomas being even more aggressive than the fusiform type. The distinction between low-grade and high-grade endometrial stromal sarcoma is based first on morphology and immunohistochemistry. The detection of fusion transcripts helps in the diagnosis. Definitely recognized as a separate entity, uterine PEComa is a rare tumor whose diagnostic criteria are being recently defined. Uterine PEComa has a specific algorithm stratifying the tumors into uncertain malignant potential and malignant tumors. Embryonal rhabdomyosarcomas of the uterine cervix are not restricted to children but can also be observed in adult women and are almost always DICER1 mutated, unlike embryonal rhabdomyosarcoma of the vagina which are DICER1wild-type, and adenosarcoma which can be DICER1 mutated but with less frequency. As sarcomas associated with fusion transcripts involving the NTRK, ALK, COL1A1::PDGFB genes can benefit from targeted therapy, systematic detection are now relevant especially for patients with high risk of relapse or in recurrent setting. The integration of molecular data with dedicated expert pathology review for histology and clinical data allows better identification of uterine sarcomas in order to better treat them.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Gynecologic Oncology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Momeni-Boroujeni A.
        • Mohammad N.
        • Wolber R.
        • et al.
        Targeted RNA expression profiling identifies high-grade endometrial stromal sarcoma as a clinically relevant molecular subtype of uterine sarcoma.
        Mod. Pathol. 2021; 34: 1008-1016
        • Selenica P.
        • Conlon N.
        • Gonzalez C.
        • et al.
        Genomic profiling aids classification of diagnostically challenging uterine mesenchymal tumors with myomelanocytic differentiation.
        Am. J. Surg. Pathol. 2021; 45: 77-92
        • Shushkevich A.
        • Thaker P.H.
        • Littell R.D.
        • et al.
        State of the science: uterine sarcomas: from pathology to practice.
        Gynecol. Oncol. 2020; 159: 3-7
        • Brooks S.E.
        • Zhan M.
        • Cote T.
        • et al.
        Surveillance, epidemiology, and end results analysis of 2677 cases of uterine sarcoma 1989–1999.
        Gynecol. Oncol. 2004; 93: 204-208
        • Toro J.R.
        • Travis L.B.
        • Wu H.J.
        • et al.
        Incidence patterns of soft tissue sarcomas, regardless of primary site, in the surveillance, epidemiology and end results program, 1978-2001: an analysis of 26,758 cases.
        Int. J. Cancer. 2006; 119: 2922-2930
        • Ip P.
        Smooth muscle tumour of uncertain malignant potential.
        in: O. E. Female Genital Tumours. IARC, Lyon2020
        • Chapel D.B.
        • Nucci M.R.
        • Quade B.J.
        • et al.
        Epithelioid leiomyosarcoma of the uterus: modern outcome-based appraisal of diagnostic criteria in a large institutional series.
        Am. J. Surg. Pathol. 2022; 46: 464-475
        • Croce S.
        • Ribeiro A.
        • Brulard C.
        • et al.
        Uterine smooth muscle tumor analysis by comparative genomic hybridization: a useful diagnostic tool in challenging lesions.
        Mod. Pathol. 2015; 28: 1001-1010
        • Croce S.
        • Ducoulombier A.
        • Ribeiro A.
        • et al.
        Genome profiling is an efficient tool to avoid the STUMP classification of uterine smooth muscle lesions: a comprehensive array-genomic hybridization analysis of 77 tumors.
        Mod. Pathol. 2018; 31: 816-828https://doi.org/10.1038/modpathol.2017.185
        • Croce S.
        • Chibon F.
        Molecular prognostication of uterine smooth muscle neoplasms: from CGH array to CINSARC signature and beyond.
        Genes Chromosom. Cancer. 2021; 60: 129-137
        • Longacre T.
        Uterine leiomyosarcoma.
        in: Oliva E.L.A. Female Genital Tumours. IARC, Lyon2020
        • Pautier P.
        • Genestie C.
        • Rey A.
        • et al.
        Analysis of clinicopathologic prognostic factors for 157 uterine sarcomas and evaluation of a grading score validated for soft tissue sarcoma.
        Cancer. 2000; 88: 1425-1431
        • Chapel D.B.
        • Nucci M.R.
        • Quade B.J.
        • et al.
        Epithelioid leiomyosarcoma of the uterus: modern outcome-based appraisal of diagnostic criteria in a large institutional series.
        Am. J. Surg. Pathol. 2021; 46: 464-475https://doi.org/10.1097/PAS.0000000000001795
        • Davidson B.
        • Kjaereng M.L.
        • Forsund M.
        • et al.
        Progesterone receptor expression is an independent prognosticator in FIGO stage I uterine leiomyosarcoma.
        Am. J. Clin. Pathol. 2016; 145: 449-458
        • Chiang S.
        Recent advances in smooth muscle tumors with PGR and PLAG1 gene fusions and myofibroblastic uterine neoplasms.
        Genes Chromosom. Cancer. 2021; 60: 138-146
        • Thiryayi S.A.
        • Turashvili G.
        • Latta E.K.
        • et al.
        PLAG1-rearrangment in a uterine leiomyosarcoma with myxoid stroma and heterologous differentiation.
        Genes Chromosom. Cancer. 2021; 60: 713-717
        • Croce S.
        • Lesluyes T.
        • Valle C.
        • et al.
        The nanocind signature is an independent prognosticator of recurrence and death in uterine leiomyosarcomas.
        Clin. Cancer Res. 2019; 26: 855-861https://doi.org/10.1158/1078-0432.CCR-19-2891
        • Lee C.-H.
        • Sarah Chiang
        Low-grade endometrial stromal sarcoma.
        in: Wcote Board Female Genital Tumors. IARC Lyon, 2020
        • Lee C.H.
        • Nucci M.R.
        Endometrial stromal sarcoma—the new genetic paradigm.
        Histopathology. 2015; 67: 1-19
        • Hoang L.
        • Chiang S.
        • Lee C.H.
        Endometrial stromal sarcomas and related neoplasms: new developments and diagnostic considerations.
        Pathology. 2018; 50: 162-177
        • Moore M.
        • McCluggage W.G.
        Uterine endometrial stromal tumors with limited infiltration: first report of a case series indicating potential for malignant behavior.
        Int. J. Gynecol. Pathol. 2020; 39: 221-226
        • Busca A.
        • Gulavita P.
        • Parra-Herran C.
        • et al.
        IFITM1 outperforms CD10 in differentiating low-grade endometrial stromal sarcomas from smooth muscle neoplasms of the uterus.
        Int. J. Gynecol. Pathol. 2018; 37: 372-378
        • Le Page C.
        • Almadani N.
        • Turashvili G.
        • et al.
        SATB2 expression in uterine sarcoma: a multicenter retrospective study.
        Int. J. Gynecol. Pathol. 2021; 40: 487-494
        • Micci F.
        • Heim S.
        • Panagopoulos I.
        Molecular pathogenesis and prognostication of “low-grade” and “high-grade” endometrial stromal sarcoma.
        Genes Chromosom. Cancer. 2021; 60: 160-167
        • Chiang S.
        High-grade endometrial stromal sarcoma.
        in: Wcote Board Female Genital Tumours. 2020
        • Lee C.H.
        • Marino-Enriquez A.
        • Ou W.
        • et al.
        The clinicopathologic features of YWHAE-FAM22 endometrial stromal sarcomas: a histologically high-grade and clinically aggressive tumor.
        Am. J. Surg. Pathol. 2012; 36: 641-653
        • Lee C.H.
        • Ou W.B.
        • Marino-Enriquez A.
        • et al.
        14-3-3 fusion oncogenes in high-grade endometrial stromal sarcoma.
        Proc. Natl. Acad. Sci. U. S. A. 2012; 109: 929-934
        • Marino-Enriquez A.
        • Lauria A.
        • Przybyl J.
        • et al.
        BCOR internal tandem duplication in high-grade uterine sarcomas.
        Am. J. Surg. Pathol. 2018; 42: 335-341
        • Brahmi M.
        • Franceschi T.
        • Treilleux I.
        • et al.
        Molecular classification of endometrial stromal sarcomas using RNA sequencing defines nosological and prognostic subgroups with different natural history.
        Cancers. 2020; 12
        • Croce S.
        • Hostein I.
        • Ribeiro A.
        • et al.
        YWHAE rearrangement identified by FISH and RT-PCR in endometrial stromal sarcomas: genetic and pathological correlations.
        Mod. Pathol. 2013; 26: 1390-1400
        • Hoang L.N.
        • Aneja A.
        • Conlon N.
        • et al.
        Novel high-grade endometrial stromal sarcoma: a morphologic mimicker of myxoid leiomyosarcoma.
        Am. J. Surg. Pathol. 2017; 41: 12-24
        • Lee C.H.
        • Ali R.H.
        • 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
        • Lee C.H.
        • Hoang L.N.
        • Yip S.
        • et al.
        Frequent expression of KIT in endometrial stromal sarcoma with YWHAE genetic rearrangement.
        Mod. Pathol. 2014; 27: 751-757
        • Chiang S.
        • Lee C.H.
        • Stewart C.J.R.
        • et al.
        BCOR is a robust diagnostic immunohistochemical marker of genetically diverse high-grade endometrial stromal sarcoma, including tumors exhibiting variant morphology.
        Mod. Pathol. 2017; 30: 1251-1261https://doi.org/10.1038/modpathol.2017.42
        • Lewis N.
        • Soslow R.A.
        • Delair D.F.
        • et al.
        ZC3H7B-BCOR high-grade endometrial stromal sarcomas: a report of 17 cases of a newly defined entity.
        Mod. Pathol. 2018; 31: 674-684
        • Kommoss F.K.
        • Chang K.T.
        • Stichel D.
        • et al.
        Endometrial stromal sarcomas with BCOR-rearrangement harbor MDM2 amplifications.
        J. Pathol. Clin. Res. 2020; 6: 178-184
        • Schoolmeester J.K.
        • Sciallis A.P.
        • Greipp P.T.
        • et al.
        Analysis of MDM2 amplification in 43 endometrial stromal tumors: a potential diagnostic pitfall.
        Int. J. Gynecol. Pathol. 2015; 34: 576-583
        • Sciallis A.P.
        • Bedroske P.P.
        • Schoolmeester J.K.
        • et al.
        High-grade endometrial stromal sarcomas: a clinicopathologic study of a group of tumors with heterogenous morphologic and genetic features.
        Am. J. Surg. Pathol. 2014; 38: 1161-1172
        • Zou Y.
        • Turashvili G.
        • Soslow R.A.
        • et al.
        High-grade transformation of low-grade endometrial stromal sarcomas lacking YWHAE and BCOR genetic abnormalities.
        Mod. Pathol. 2020; 33: 1861-1870
        • Chiang Sarah C.J.W.
        • Shuichi Kurihara
        Undifferentiated uterine sarcoma.
        in: Wcote Board Female Genital Tumours. IARC Lyon, 2020
        • 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
        • Cotzia P.
        • Benayed R.
        • Mullaney K.
        • et al.
        Undifferentiated uterine sarcomas represent under-recognized high-grade endometrial stromal sarcomas.
        Am. J. Surg. Pathol. 2019; 43: 662-669
        • Howitt Brooke E.Q.B.J.
        • Carlson Joseph W.
        Adenosarcoma of uterine corpus.
        in: Wcote Board Female Genital Tumours. IARC Lyon, 2020
        • Amin M.B.
        • Greene F.L.
        • Edge S.B.
        • et al.
        The eighth edition AJCC cancer staging manual: continuing to build a bridge from a population-based to a more “personalized” approach to cancer staging.
        CA Cancer J. Clin. 2017; 67: 93-99
        • Bennett Jennifer A.S.J.K.
        Perivascular epithelioid cell tumour (PEComa).
        in: Wcote Board Female Genital Tumours. IARC Lyon, 2020
        • Bennett J.A.
        • Braga A.C.
        • Pinto A.
        • et al.
        Uterine PEComas: a morphologic, immunohistochemical, and molecular analysis of 32 tumors.
        Am. J. Surg. Pathol. 2018; 42: 1370-1383
        • Benvenuto G.
        • Li S.
        • Brown S.J.
        • et al.
        The tuberous sclerosis-1 (TSC1) gene product hamartin suppresses cell growth and augments the expression of the TSC2 product tuberin by inhibiting its ubiquitination.
        Oncogene. 2000; 19: 6306-6316
        • Tsuda M.
        • Davis I.J.
        • Argani P.
        • et al.
        TFE3 fusions activate MET signaling by transcriptional up-regulation, defining another class of tumors as candidates for therapeutic MET inhibition.
        Cancer Res. 2007; 67: 919-929
        • Bourgmayer A.
        • Nannini S.
        • Bonjean P.
        • et al.
        Natural history and treatment strategies of advanced PEComas: a systematic review.
        Cancers. 2021; 13
        • Bennett J.A.
        • Ordulu Z.
        • Pinto A.
        • et al.
        Uterine PEComas: correlation between melanocytic marker expression and TSC alterations/TFE3 fusions.
        Mod. Pathol. 2021; 35: 515-523https://doi.org/10.1038/s41379-021-00855-1
        • Howitt B.E.
        • Folpe A.L.
        Update on SWI/SNF-related gynecologic mesenchymal neoplasms: SMARCA4-deficient uterine sarcoma and SMARCB1-deficient vulvar neoplasms.
        Genes Chromosom. Cancer. 2021; 60: 190-209
        • Kolin D.L.
        • Quick C.M.
        • Dong F.
        • et al.
        SMARCA4-deficient uterine sarcoma and undifferentiated endometrial carcinoma are distinct clinicopathologic entities.
        Am. J. Surg. Pathol. 2020; 44: 263-270
        • Barr Frederic G.B.S.D.
        • Soslow Robert A.
        • Howitt Brooke E.
        Rhabdomyosarcoma.
        in: WCote Board Female Genital Tumours. IARC Lyon, 2020
        • Dehner L.P.
        • Jarzembowski J.A.
        • Hill D.A.
        Embryonal rhabdomyosarcoma of the uterine cervix: a report of 14 cases and a discussion of its unusual clinicopathological associations.
        Mod. Pathol. 2012; 25: 602-614
        • Li R.F.
        • Gupta M.
        • McCluggage W.G.
        • et al.
        Embryonal rhabdomyosarcoma (botryoid type) of the uterine corpus and cervix in adult women: report of a case series and review of the literature.
        Am. J. Surg. Pathol. 2013; 37: 344-355
        • Ferguson S.E.
        • Gerald W.
        • Barakat R.R.
        • et al.
        Clinicopathologic features of rhabdomyosarcoma of gynecologic origin in adults.
        Am. J. Surg. Pathol. 2007; 31: 382-389
        • de Kock L.
        • Yoon J.Y.
        • Apellaniz-Ruiz M.
        • et al.
        Significantly greater prevalence of DICER1 alterations in uterine embryonal rhabdomyosarcoma compared to adenosarcoma.
        Mod. Pathol. 2020; 33: 1207-1219
        • Apellaniz-Ruiz M.
        • McCluggage W.G.
        • Foulkes W.D.
        DICER1-associated embryonal rhabdomyosarcoma and adenosarcoma of the gynecologic tract: pathology, molecular genetics, and indications for molecular testing.
        Genes Chromosom. Cancer. 2021; 60: 217-233
        • Kommoss F.K.F.
        • Stichel D.
        • Mora J.
        • et al.
        Clinicopathologic and molecular analysis of embryonal rhabdomyosarcoma of the genitourinary tract: evidence for a distinct DICER1-associated subgroup.
        Mod. Pathol. 2021; 34: 1558-1569
        • Bennett J.A.
        • Ordulu Z.
        • Young R.H.
        • et al.
        Embryonal rhabdomyosarcoma of the uterine corpus: a clinicopathological and molecular analysis of 21 cases highlighting a frequent association with DICER1 mutations.
        Mod. Pathol. 2021; 34: 1750-1762
        • de Kock L.
        • Wu M.K.
        • Foulkes W.D.
        Ten years of DICER1 mutations: provenance, distribution, and associated phenotypes.
        Hum. Mutat. 2019; 40: 1939-1953
        • LT A.
        NTRK-rearranged spindle cell neoplasm (emerging).
        in: WHO Female Genital Tumours. IARC Lyon, 2020
        • Croce S.
        • Hostein I.
        • Longacre T.A.
        • et al.
        Uterine and vaginal sarcomas resembling fibrosarcoma: a clinicopathological and molecular analysis of 13 cases showing common NTRK-rearrangements and the description of a COL1A1-PDGFB fusion novel to uterine neoplasms.
        Mod. Pathol. 2019; 32: 1008-1022
        • Croce S.
        • Hostein I.
        • McCluggage W.G.
        NTRK and other recently described kinase fusion positive uterine sarcomas: a review of a group of rare neoplasms.
        Genes Chromosom. Cancer. 2021; 60: 147-159
        • Goulding E.A.
        • Morreau P.
        • De Silva M.
        • et al.
        Case report: NTRK1-rearranged cervical sarcoma with fibrosarcoma like morphology presenting in a 13-year-old managed with a neo-adjuvant TRK-inhibitor and surgical excision.
        Gynecol. Oncol. Rep. 2021; 37100845
        • Chiang S.
        • Cotzia P.
        • Hyman D.M.
        • et al.
        NTRK fusions define a novel uterine sarcoma subtype with features of fibrosarcoma.
        Am. J. Surg. Pathol. 2018; 42: 791-798https://doi.org/10.1097/PAS.0000000000001055
        • Rabban J.T.
        • Devine W.P.
        • Sangoi A.R.
        • et al.
        NTRK fusion cervical sarcoma: a report of three cases, emphasising morphological and immunohistochemical distinction from other uterine sarcomas, including adenosarcoma.
        Histopathology. 2020; 77: 100-111
        • Grindstaff S.L.
        • DiSilvestro P.
        • Quddus M.R.
        COL1A1-PDGFB fusion uterine sarcoma and its response to Imatinib therapy.
        Gynecol. Oncol. Rep. 2020; 34100653
        • Staat Paul N.M.W.G.
        • Irving Julie A.
        Uterine tumour resembling ovarian sex cord tumour.
        in: Wcote Board Female Genital Tumours. IARC Lyon, 2020
        • Moore M.
        • McCluggage W.G.
        Uterine tumour resembling ovarian sex cord tumour (UTROSCT): first report of a large series with follow-up.
        Histopathology. 2017; 71: 751-759https://doi.org/10.1111/his.13296
        • Clement P.B.
        • Scully R.E.
        Uterine tumors resembling ovarian sex-cord tumors. A clinicopathologic analysis of fourteen cases.
        Am. J. Clin. Pathol. 1976; 66: 512-525
        • Lee C.H.
        • Kao Y.C.
        • Lee W.R.
        • et al.
        Clinicopathologic characterization of GREB1-rearranged uterine sarcomas with variable sex-cord differentiation.
        Am. J. Surg. Pathol. 2019; 43: 928-942
        • Bennett J.A.
        • Lastra R.R.
        • Barroeta J.E.
        • et al.
        Uterine tumor resembling ovarian sex cord stromal tumor (UTROSCT): a series of 3 cases with extensive rhabdoid differentiation, malignant behavior, and ESR1-NCOA2 fusions.
        Am. J. Surg. Pathol. 2020; 44: 1563-1572
        • Croce S.
        • de Kock L.
        • Boshari T.
        • et al.
        Uterine tumor resembling ovarian sex cord tumor (UTROSCT) commonly exhibits positivity with sex cord markers FOXL2 and SF-1 but lacks FOXL2 and DICER1 mutations.
        Int. J. Gynecol. Pathol. 2015; 35: 301-308https://doi.org/10.1097/PGP.0000000000000240
        • Chiang S.
        • Staats P.N.
        • Senz J.
        • et al.
        FOXL2 mutation is absent in uterine tumors resembling ovarian sex cord tumors.
        Am. J. Surg. Pathol. 2015; 39: 618-623
        • Kao Y.C.
        • Lee J.C.
        An update of molecular findings in uterine tumor resembling ovarian sex cord tumor and GREB1-rearranged uterine sarcoma with variable sex-cord differentiation.
        Genes Chromosom. Cancer. 2021; 60: 180-189
        • Croce S.
        • Lesluyes T.
        • Delespaul L.
        • et al.
        GREB1-CTNNB1 fusion transcript detected by RNA-sequencing in a uterine tumor resembling ovarian sex cord tumor (UTROSCT): a novel CTNNB1 rearrangement.
        Genes Chromosom. Cancer. 2019; 58: 155-163
        • Dickson B.C.
        • Childs T.J.
        • Colgan T.J.
        • et al.
        Uterine tumor resembling ovarian sex cord tumor: a distinct entity characterized by recurrent NCOA2/3 gene fusions.
        Am. J. Surg. Pathol. 2019; 43: 178-186
        • Goebel E.A.
        • Hernandez Bonilla S.
        • Dong F.
        • et al.
        Uterine tumor resembling ovarian sex cord tumor (UTROSCT): a morphologic and molecular study of 26 cases confirms recurrent NCOA1-3 rearrangement.
        Am. J. Surg. Pathol. 2020; 44: 30-42
        • Parra-Herran Carlos L.C.-H.
        • Rabban Joseph T.
        • Bennett Jennifer A.
        Inflammatory myofibroblastic tumours.
        in: Wcote Board Female Genital Tumours. IARC Lyon, 2020
        • Parra-Herran C.
        • Quick C.M.
        • Howitt B.E.
        • et al.
        Inflammatory myofibroblastic tumor of the uterus: clinical and pathologic review of 10 cases including a subset with aggressive clinical course.
        Am. J. Surg. Pathol. 2015; 39: 157-168
        • Bennett J.A.
        • Nardi V.
        • Rouzbahman M.
        • et al.
        Inflammatory myofibroblastic tumor of the uterus: a clinicopathological, immunohistochemical, and molecular analysis of 13 cases highlighting their broad morphologic spectrum.
        Mod. Pathol. 2017; 30: 1489-1503
        • Pickett J.L.
        • Chou A.
        • Andrici J.A.
        • et al.
        Inflammatory myofibroblastic tumors of the female genital tract are under-recognized: a low threshold for ALK immunohistochemistry is required.
        Am. J. Surg. Pathol. 2017; 41: 1433-1442
        • Makhdoum S.
        • Nardi V.
        • Devereaux K.A.
        • et al.
        Inflammatory myofibroblastic tumors associated with the placenta: a series of 9 cases.
        Hum. Pathol. 2020; 106: 62-73
        • Devereaux K.A.
        • Fitzpatrick M.B.
        • Hartinger S.
        • et al.
        Pregnancy-associated inflammatory myofibroblastic tumors of the uterus are clinically distinct and highly enriched for TIMP3-ALK and THBS1-ALK fusions.
        Am. J. Surg. Pathol. 2020; 44: 970-981
        • Butrynski J.E.
        • D’Adamo D.R.
        • Hornick J.L.
        • et al.
        Crizotinib in ALK-rearranged inflammatory myofibroblastic tumor.
        N. Engl. J. Med. 2010; 363: 1727-1733
        • Collins K.
        • Ramalingam P.
        • Euscher E.D.
        • et al.
        Uterine inflammatory myofibroblastic neoplasms with aggressive behavior, including an epithelioid inflammatory myofibroblastic sarcoma: a clinicopathologic study of 9 cases.
        Am. J. Surg. Pathol. 2022; 46: 105-117
        • Marino-Enriquez A.
        • Wang W.L.
        • Roy A.
        • et al.
        Epithelioid inflammatory myofibroblastic sarcoma: an aggressive intra-abdominal variant of inflammatory myofibroblastic tumor with nuclear membrane or perinuclear ALK.
        Am. J. Surg. Pathol. 2011; 35: 135-144
        • Bennett J.A.
        • Wang P.
        • Wanjari P.
        • et al.
        Uterine inflammatory myofibroblastic tumor: first report of a ROS1 fusion.
        Genes Chromosom. Cancer. 2021; 60: 822-826
        • Cheek E.H.
        • Fadra N.
        • Jackson R.A.
        • et al.
        Uterine inflammatory myofibroblastic tumors in pregnant women with and without involvement of the placenta: a study of 6 cases with identification of a novel TIMP3-RET fusion.
        Hum. Pathol. 2020; 97: 29-39
        • Perrier L.
        • Rascle P.
        • Morelle M.
        • et al.
        The cost-saving effect of centralized histological reviews with soft tissue and visceral sarcomas, GIST, and desmoid tumors: the experiences of the pathologists of the French Sarcoma Group.
        PLoS One. 2018; 13e0193330
        • Ray-Coquard I.
        • Montesco M.C.
        • Coindre J.M.
        • et al.
        Sarcoma: concordance between initial diagnosis and centralized expert review in a population-based study within three European regions.
        Ann. Oncol. 2012; 23: 2442-2449
        • Henno S.
        • Jeanne C.
        • Rouge T.M.
        • et al.
        Potential histological discordance revealed by second review in the national rare gynecological cancer network (TMRG).
        Gynecol. Oncol. 2022; 165: 637-641https://doi.org/10.1016/j.ygyno.2022.03.019
        • Costigan C, D
        • et al.
        NTRK-Rearranged Uterine Sarcomas: Clinicopathologic Features of 15 Cases, Literature Review, and Risk Stratification.
        American journal of surgical pathology. 2022; https://doi.org/10.1097/PAS.0000000000001929
        • Bean R, G
        • et al.
        DICER1 mutations are frequent in müllerian adenosarcomas and are independent of rhabdomyosarcomatous differentiation.
        American journal of surgical pathology. 2019; 32: 280-289https://doi.org/10.1038/s41379-018-0132-5