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• W4387086931 abstract "The International Federation of Gynecology and Obstetrics (FIGO) presented recently, 14 years after FIGO 2009, its new 2023 staging system for endometrial cancers (Table 1) [[1]Berek J.S. Matias-Guiu X. Creutzberg C. Fotopoulou C. Gaffney D. Kehoe S. et al.Endometrial Cancer Staging Subcommittee, FIGO Women's Cancer CommitteeFIGO staging of endometrial cancer: 2023.Int J Gynaecol Obstet. 2023; 162: 383-394https://doi.org/10.1002/ijgo.14923Google Scholar]. The changes incorporate not only a number of new prognostic pathological variables but also new molecular classifiers. FIGO should be applauded for incorporating these new variables in a consistent and well documented way and for introducing a molecular classification based on whole genome sequencing findings in endometrial carcinoma of The Cancer Genome Atlas (TCGA) [[2]Kandoth C. Schultz N. Cherniack A.D. Akbani R. Liu Y. Shen H. et al.Cancer Genome Atlas Research NetworkIntegrated genomic characterization of endometrial carcinoma.Nature. 2013; 497: 67-73https://doi.org/10.1038/nature12113Google Scholar]. TCGA classifies endometrial carcinomas into: (1) DNA polymerase epsilon mutated (POLEm); (2) microsatellite instability-high or mismatch repair deficiency (MMRd); (3) copy-number alteration high/serous TP53 abnormal (somatic copy number alteration-high (SCNA-high)) and (4) SCNA-low. Later, several studies of which ProMisE (Proactive Molecular risk classifier for Endometrial cancer) is the best known, presented a similar but more easily available classification based on immunohistochemistry for tumour protein p53 and for mismatch repair protein, combined with sequencing for POLE exonuclease domain mutations [[3]Talhouk A. McConechy M.K. Leung S. Yang W. Lum A. Senz J. et al.Confirmation of ProMisE: a simple, genomics-based clinical classifier for endometrial cancer.Cancer. 2017; 123: 802-813https://doi.org/10.1002/cncr.30496Google Scholar]. In 2021, the European Society of Gynaecological Oncology (ESGO) – the European Society for Radiotherapy and Oncology (ESTRO), and the European Society of Pathology (ESP) encouraged molecular classification in all endometrial carcinomas, especially in high-grade tumours [[4]Concin N. Matias-Guiu X. Vergote I. Cibula D. Mirza M.R. Marnitz S. et al.ESGO/ESTRO/ESP guidelines for the management of patients with endometrial carcinoma.Int J Gynecol Cancer. 2021; 31: 12-39https://doi.org/10.1136/ijgc-2020-002230Google Scholar]. In addition, the ESGO-ESTRO-ESP consensus presented a new prognostic group classification based on molecular classifiers including recommendations for adjuvant therapy. Patients with POLEm tumours have an excellent prognosis, while the prognosis is unfavourable in patients with abnormal p53 expression (p53abn). Furthermore, it has been shown that patients with multiple classifiers such as MMRd-p53abn should be classified as MMRd and POLEm-p53abn as POLEm [[5]León-Castillo A. Gilvazquez E. Nout R. Smit V.T. McAlpine J.N. McConechy M. et al.Clinicopathological and molecular characterisation of 'multiple-classifier' endometrial carcinomas.J Pathol. 2020; 250: 312-322https://doi.org/10.1002/path.5373Google Scholar].Table 12023 The International Federation of Gynecology and Obstetrics (FIGO) Staging of cancers of the endometriumaEndometrial cancer is surgically staged and pathologically examined., bIn early endometrial cancer, the standard surgery is a total hysterectomy with bilateral salpingo-oophorectomy via a minimally invasive laparoscopic approach. Lymph node staging should be performed in patients with intermediate-high/high-risk patients. Sentinel lymph node (SLN) biopsy is an adequate alternative to systematic lymphadenectomy for staging proposes. SLN biopsy can also be considered in low−/low-intermediate-risk patients to rule out occult lymph node metastases and to identify disease truly confined to the uterus. [1]Berek J.S. Matias-Guiu X. Creutzberg C. Fotopoulou C. Gaffney D. Kehoe S. et al.Endometrial Cancer Staging Subcommittee, FIGO Women's Cancer CommitteeFIGO staging of endometrial cancer: 2023.Int J Gynaecol Obstet. 2023; 162: 383-394https://doi.org/10.1002/ijgo.14923Google Scholar.StageDescriptionStage IConfined to the uterine corpus and ovarycLow-grade EECs involving both the endometrium and the ovary are considered to have a good prognosis, and no adjuvant treatment is recommended if all the below criteria are met. Disease limited to low-grade endometrioid carcinomas involving the endometrium and ovaries (Stage IA3) must be distinguished from the extensive spread of the endometrial carcinoma to the ovary (Stage IIIA1), by the following criteria: (1) no more than superficial myometrial invasion is present (<50%); (2) absence of extensive/substantial LVSI; (3) absence of additional metastases; and (4) the ovarian tumour is unilateral, limited to the ovary, without capsule invasion/rupture (equivalent to pT1a). IADisease limited to the endometrium OR non-aggressive histological type i.e. low-grade endometrioid, with invasion of less than half of myometrium with no or focal lymphovascular space involvement (LVSI) OR good prognosis diseaseIA1 Non-aggressive histological type limited to an endometrial polyp OR confined to the endometriumIA2 Non-aggressive histological types involving less than half of the myometrium with no or focal LVSIIA3 Low-grade endometrioid carcinomas limited to the uterus and ovarycLow-grade EECs involving both the endometrium and the ovary are considered to have a good prognosis, and no adjuvant treatment is recommended if all the below criteria are met. Disease limited to low-grade endometrioid carcinomas involving the endometrium and ovaries (Stage IA3) must be distinguished from the extensive spread of the endometrial carcinoma to the ovary (Stage IIIA1), by the following criteria: (1) no more than superficial myometrial invasion is present (<50%); (2) absence of extensive/substantial LVSI; (3) absence of additional metastases; and (4) the ovarian tumour is unilateral, limited to the ovary, without capsule invasion/rupture (equivalent to pT1a). IBNon-aggressive histological types with invasion of half or more of the myometrium, and with no or focal LVSIdLVSI: extensive/substantial, ≥5 vessels involved. ICAggressive histological typeseGrade and histological type: Serous adenocarcinomas, clear cell adenocarcinomas, mesonephric-like carcinomas, gastrointestinal-type mucinous endometrial carcinoma, undifferentiated carcinomas, and carcinosarcomas are considered high-grade by definition. Non-aggressive histological types are composed of low-grade (grade 1 and 2) EECs. Aggressive histological types are composed of high-grade EECs (grade 3), serous, clear cell, undifferentiated, mixed, mesonephric-like, gastrointestinal mucinous type carcinomas, and carcinosarcomas. limited to a polyp or confined to the endometriumStage IIInvasion of cervical stroma without extrauterine extension OR with substantial LVSI OR aggressive histological types with myometrial invasion IIAInvasion of the cervical stroma of non-aggressive histological types IIBSubstantial LVSIdLVSI: extensive/substantial, ≥5 vessels involved. of non-aggressive histological types IICAggressive histological typeseGrade and histological type: Serous adenocarcinomas, clear cell adenocarcinomas, mesonephric-like carcinomas, gastrointestinal-type mucinous endometrial carcinoma, undifferentiated carcinomas, and carcinosarcomas are considered high-grade by definition. Non-aggressive histological types are composed of low-grade (grade 1 and 2) EECs. Aggressive histological types are composed of high-grade EECs (grade 3), serous, clear cell, undifferentiated, mixed, mesonephric-like, gastrointestinal mucinous type carcinomas, and carcinosarcomas. with any myometrial involvementStage IIILocal and/or regional spread of the tumour of any histological subtype IIIAInvasion of uterine serosa, adnexa, or both by direct extension or metastasisIIIA1 Spread to ovary or fallopian tube (except when meeting stage IA3 criteria)cLow-grade EECs involving both the endometrium and the ovary are considered to have a good prognosis, and no adjuvant treatment is recommended if all the below criteria are met. Disease limited to low-grade endometrioid carcinomas involving the endometrium and ovaries (Stage IA3) must be distinguished from the extensive spread of the endometrial carcinoma to the ovary (Stage IIIA1), by the following criteria: (1) no more than superficial myometrial invasion is present (<50%); (2) absence of extensive/substantial LVSI; (3) absence of additional metastases; and (4) the ovarian tumour is unilateral, limited to the ovary, without capsule invasion/rupture (equivalent to pT1a).IIIA2 Involvement of uterine subserosa or spread through the uterine serosa IIIBMetastasis or direct spread to the vagina and/or to the parametria or pelvic peritoneumIIIB1 Metastasis or direct spread to the vagina and/or the parametriaIIIB2 Metastasis to the pelvic peritoneum IIICMetastasis to the pelvic or para-aortic lymph nodes or bothfMicrometastases are considered to be metastatic involvement (pN1 (mi)). The prognostic significance of isolated tumour cells (ITCs) is unclear. The presence of ITCs should be documented and is regarded as pN0(i+). Macrometastases are >2 mm in size, micrometastases are 0.2–2 mm and/or >200 cells, and isolated tumour cells are ≥0.2 mm and ≤200 cells.IIIC1 Metastasis to the pelvic lymph nodesIIIC1i MicrometastasisIIICii MacrometastasisIIIC2 Metastasis to para-aortic lymph nodes up to the renal vessels, with or without metastasis to the pelvic lymph nodesIIIC2i MicrometastasisIIIC2ii MacrometastasisStage IVSpread to the bladder mucosa and/or intestinal mucosa and/or distance metastasis IVAInvasion of the bladder mucosa and/or the intestinal/bowel mucosa IVBAbdominal peritoneal metastasis beyond the pelvis IVCDistant metastasis, including metastasis to any extra-or intra-abdominal lymph nodes above the renal vessels, lungs, liver, brain, or boneFIGO endometrial cancer stage with molecular classificationStage descriptionMolecular findings in patients with early endometrial cancer (Stages I and II after surgical staging)Stage IAmPOLEmPOLEm endometrial carcinoma, confined to the uterine corpus or with cervical extension, regardless of the degree of LVSI or histological typeStage IICmp53abnp53abn endometrial carcinoma confined to the uterine corpus with any myometrial invasion, with or without cervical invasion, and regardless of the degree of LVSI or histological typeAdapted from [1]Berek J.S. Matias-Guiu X. Creutzberg C. Fotopoulou C. Gaffney D. Kehoe S. et al.Endometrial Cancer Staging Subcommittee, FIGO Women's Cancer CommitteeFIGO staging of endometrial cancer: 2023.Int J Gynaecol Obstet. 2023; 162: 383-394https://doi.org/10.1002/ijgo.14923Google ScholarAbbreviations: EEC, endometrioid carcinoma; LVSI, lymphovascular space involvement; abn, abnormal; POLEm, polymerase epsilon mutated.a Endometrial cancer is surgically staged and pathologically examined.b In early endometrial cancer, the standard surgery is a total hysterectomy with bilateral salpingo-oophorectomy via a minimally invasive laparoscopic approach. Lymph node staging should be performed in patients with intermediate-high/high-risk patients. Sentinel lymph node (SLN) biopsy is an adequate alternative to systematic lymphadenectomy for staging proposes. SLN biopsy can also be considered in low−/low-intermediate-risk patients to rule out occult lymph node metastases and to identify disease truly confined to the uterus.c Low-grade EECs involving both the endometrium and the ovary are considered to have a good prognosis, and no adjuvant treatment is recommended if all the below criteria are met. Disease limited to low-grade endometrioid carcinomas involving the endometrium and ovaries (Stage IA3) must be distinguished from the extensive spread of the endometrial carcinoma to the ovary (Stage IIIA1), by the following criteria: (1) no more than superficial myometrial invasion is present (<50%); (2) absence of extensive/substantial LVSI; (3) absence of additional metastases; and (4) the ovarian tumour is unilateral, limited to the ovary, without capsule invasion/rupture (equivalent to pT1a).d LVSI: extensive/substantial, ≥5 vessels involved.e Grade and histological type: Serous adenocarcinomas, clear cell adenocarcinomas, mesonephric-like carcinomas, gastrointestinal-type mucinous endometrial carcinoma, undifferentiated carcinomas, and carcinosarcomas are considered high-grade by definition. Non-aggressive histological types are composed of low-grade (grade 1 and 2) EECs. Aggressive histological types are composed of high-grade EECs (grade 3), serous, clear cell, undifferentiated, mixed, mesonephric-like, gastrointestinal mucinous type carcinomas, and carcinosarcomas.f Micrometastases are considered to be metastatic involvement (pN1 (mi)). The prognostic significance of isolated tumour cells (ITCs) is unclear. The presence of ITCs should be documented and is regarded as pN0(i+). Macrometastases are >2 mm in size, micrometastases are 0.2–2 mm and/or >200 cells, and isolated tumour cells are ≥0.2 mm and ≤200 cells. Open table in a new tab Adapted from [1]Berek J.S. Matias-Guiu X. Creutzberg C. Fotopoulou C. Gaffney D. Kehoe S. et al.Endometrial Cancer Staging Subcommittee, FIGO Women's Cancer CommitteeFIGO staging of endometrial cancer: 2023.Int J Gynaecol Obstet. 2023; 162: 383-394https://doi.org/10.1002/ijgo.14923Google Scholar Abbreviations: EEC, endometrioid carcinoma; LVSI, lymphovascular space involvement; abn, abnormal; POLEm, polymerase epsilon mutated. Integrating all currently available evidence, FIGO has taken the position that, when feasible, the addition of molecular subtype evaluation to the staging criteria should be performed as it allows a better prediction of prognosis in a staging scheme (Table 1) [[1]Berek J.S. Matias-Guiu X. Creutzberg C. Fotopoulou C. Gaffney D. Kehoe S. et al.Endometrial Cancer Staging Subcommittee, FIGO Women's Cancer CommitteeFIGO staging of endometrial cancer: 2023.Int J Gynaecol Obstet. 2023; 162: 383-394https://doi.org/10.1002/ijgo.14923Google Scholar]. In addition, FIGO added a number of other important variables in the staging system such as histological type and grade (classifying tumours as aggressive or non-aggressive types), lymphovascular space invasion (LVSI) extension and type of adnexal involvement, micro- or macrometastases in pelvic and/or para-aortic lymph nodes, peritoneal metastases in the pelvis or extrapelvic area. These substantial changes increased the number of (sub)stages from 10 to 23, their incidence and precise prognostic value remains however unsure. Hence, validation of the new FIGO 2023 staging system is of utmost importance. In this issue of the European Journal of Cancer, 2 studies investigated this new FIGO 2023 staging system for endometrial cancer [6Schwameis R, et al. EJC-D-23-01694.Google Scholar, 7Matsuo K, et al. EJC-D-23-01414.Google Scholar]. In the study of Schwameis et al [[6]Schwameis R, et al. EJC-D-23-01694.Google Scholar], 519 endometrial cancer patients with molecular characterisation treated at 3 ESGO accredited centres were categorised according to the FIGO 2009 and FIGO 2023 staging systems. As expected (sub)stage shift occurred in a high number of patients (27.6%), of which the majority were upstaged (23.6%) and the authors concluded that the new FIGO classification resulted in a higher prognostic precision compared with the former one. Upstaging was mainly because all endometrial carcinomas of the aggressive types with any myometrial invasion are classified in the FIGO 2023 as Stage IIC. This seems to be a correct decision as the patients with stage IIC had a similar 5-year progression-free survival (79.3%) as the other stage II patients (overall 74.8%) in the FIGO 2023 staging system. This resulted in a better 5-year progression-free survival in Stage I with the FIGO 2023 (95.1%) compared with the FIGO 2009 (89.6%) staging system. The study also confirmed the excellent prognosis of patients with POLEm (100% 5-year progression-free survival) and the unfavourable prognosis of patients with abnormal p53 protein expression (59.8%). Moreover, the molecular-defined prognostic risk groups in FIGO 2023 Stage I and II endometrial carcinoma (Stage IAmPOLEm and Stage IICmp53abn) are much less complicated than the ESGO-ESTRO-ESP classification [[4]Concin N. Matias-Guiu X. Vergote I. Cibula D. Mirza M.R. Marnitz S. et al.ESGO/ESTRO/ESP guidelines for the management of patients with endometrial carcinoma.Int J Gynecol Cancer. 2021; 31: 12-39https://doi.org/10.1136/ijgc-2020-002230Google Scholar]. Therefore, we believe that for molecular-based risk group allocation and planning of adjuvant therapy, the FIGO 2023 molecular staging system is more straightforward than the ESGO-ESTRO-ESP classification. However, in the study of Schwameis et al, only 232 out of the 519 patients had an adequate follow-up, making further validation of their findings necessary in larger series with longer follow-ups. In a second paper in this issue, Matsuo et al [[7]Matsuo K, et al. EJC-D-23-01414.Google Scholar] compared the FIGO 2009 with FIGO 2023 staging system in 5473 patients with advanced (Stage III-IV) endometrial cancer of the National Cancer Institute’s Surveillance, Epidemiology and End Results (SEER) Programme. According to FIGO 2023, the 5-year endometrial cancer-specific mortality rate in the new downstaged IA3 group (with low risk ovarian metastases) was 11%, and this was significantly lower than in the new IIIA1 group (with high-risk spread to the ovary or fallopian tube) (31.8%). Furthermore, it is important to note that in this study patients with macrometastases in lymph nodes had a higher endometrial cancer-specific mortality than patients with micrometastases, reinforcing the introduction of micro- versus macrometastases in regional lymph nodes in the FIGO 2023 classification. Surprisingly, the prognosis of patients with pelvic versus para-aortic micrometastases was similar. In addition, it is noteworthy that this study showed that abdominal peritoneal metastasis beyond the pelvis (FIGO 2023 stage IVB) and pelvic peritoneal metastasis (IIIB2) had a distinct outcome (5-year endometrial cancer-specific mortality rates for new IVB versus IIIB2, 42.0% versus 62.7%, respectively). These findings support the new FIGO 2023 staging system in advanced endometrial cancer. However, this study also had some drawbacks: the SEER database has no recurrence data; the authors had to select cohorts from different time periods for the various (sub)stages; and the median follow-up in the group of patients with metastatic lymph nodes (Stage IIIC, 10 months) was much shorter than in the stage IIIA-IIIB and IV cohorts (respectively 77 and 72 months). Additionally, no molecular classification was available in the SEER database and consequently, Stages I and II were excluded. Current molecular classifiers are not only prognostic markers but also have predictive value. In Stage I-II POLEm tumours adjuvant therapy can be de-escalated, while in patients with abnormal p53wt expression the benefit from the addition of chemotherapy to radiotherapy was highest [[8]León-Castillo A. de Boer S.M. Powell M.E. Mileshkin L.R. Mackay H.J. Leary A. et al.TransPORTEC consortiumMolecular classification of the PORTEC-3 trial for high-risk endometrial cancer: impact on prognosis and benefit from adjuvant therapy.J Clin Oncol. 2020; 38: 3388-3397https://doi.org/10.1200/JCO.20.00549Google Scholar]. On the other hand, patients with TP53wt recurrent endometrial cancer appeared to have the most benefit of maintenance therapy with the exportin-1 inhibitor selinexor [[9]Vergote I. Pérez-Fidalgo J.A. Hamilton E.P. Valabrega G. Gorp T.V. Sehouli J. et al.ENGOT-EN5/GOG-3055/SIENDO InvestigatorsOral selinexor as maintenance therapy after first-line chemotherapy for advanced or recurrent endometrial cancer.J Clin Oncol. 2023; (Advance online publication)JCO2202906https://doi.org/10.1200/JCO.22.02906Google Scholar]. Moreover, in PORTEC-1 and PORTEC-2 the molecular classification predicted response to radiotherapy [[10]Horeweg N. Nout R.A. Jürgenliemk-Schulz I.M. Lutgens L.C.H.W. Jobsen J.J. Haverkort M.A.D. et al.PORTEC Study GroupMolecular classification predicts response to radiotherapy in the randomized PORTEC-1 and PORTEC-2 trials for early-stage endometrioid endometrial cancer.J Clin Oncol. 2023; (Advance online publication)JCO2300062https://doi.org/10.1200/JCO.23.00062Google Scholar]. Programmed death 1 blockade has become the standard of care in patients with MMRd in second-line treatment of recurrent endometrial cancer [[11]Le D.T. Uram J.N. Wang H. Bartlett B.R. Kemberling H. Eyring A.D. et al.PD-1 blockade in tumors with mismatch-repair deficiency.N Eng J Med. 2015; 372: 2509-2520https://doi.org/10.1056/NEJMoa1500596Google Scholar] and is in combination with chemotherapy in first-line recurrent or advanced endometrial cancer most effective in MMRd patients [[12]Mirza M.R. Chase D.M. Slomovitz B.M. dePont Christensen R. Novák Z. Black D. et al.RUBY InvestigatorsDostarlimab for primary advanced or recurrent endometrial cancer.N Eng J Med. 2023; 388: 2145-2158Google Scholar]. Besides the molecular classifiers based on TCGA, other classifiers such as HER2/neu, oestrogen receptor, L1CAM, and CTNB1 should in the future be considered as predictive factors [[13]Corr B. Cosgrove C. Spinosa D. Guntupalli S. Endometrial cancer: molecular classification and future treatments.BMJ Med. 2022; 1e000152https://doi.org/10.1136/bmjmed-2022-000152Google Scholar]. FIGO 2023 is an example of what it is expected to occur in the staging systems for other organs from now on, during the 21st century. Anatomic spread has been the major criterion for cancer staging in the past. However, tumours are heterogeneous and have complex biological features. The addition of pathologic and molecular parameters is very important to increase the prognostic value of staging systems. In fact, some authors previously suggested such incorporation in the staging of endometrial cancer [14Maheshwari A. Gupta S. Prat J. A proposal for updating the staging of endometrial cancer.Int J Gynaecol Obstet. 2019; 145: 245-252https://doi.org/10.1002/ijgo.12789Google Scholar, 15Binder P.S. Prat J. Mutch D.G. Molecular staging of gynecological cancer: what is the future?.Best Pract Res Clin Obstet Gynaecol. 2015; 29: 776-789https://doi.org/10.1016/j.bpobgyn.2015.01.008Google Scholar], and this approach has also been taken by the American Joint Committee on Cancer in breast cancer [[16]Giuliano A.E. Edge S.B. Hortobagyi G.N. Eighth edition of the AJCC cancer staging manual: breast cancer.Ann Surg Oncol. 2018; 25: 1783-1785https://doi.org/10.1245/s10434-018-6486-6Google Scholar]. In conclusion, the recent FIGO 2023 staging system for endometrial cancer was validated in 2 studies published in this issue. Further validation is still needed, but the new FIGO 2023 classification obviously is a major step forward in identifying better prognostic and predictive factors for our patients with endometrial cancer. None." @default.
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• W4387086931 title "New FIGO 2023 endometrial cancer staging validation. Welcome to the first molecular classifiers and new pathological variables!" @default.
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