The Impact of the 2023 FIGO Staging Update of Endometrial Carcinoma on the Content of Pathological Diagnosis

doi:10.12280/gjfckx.20240166

Abstract

Abstract:

Endometrial carcinoma is the most common malignancy of the female reproductive system. Recent years have witnessed pivotal developments in the diagnosis and treatment, including the quantitative assessment of lymphovascular space invasion, the ultrastaging of sentinel lymph nodes, and the molecular stratification of endometrial carcinoma, all progressively integrated into clinical practice. These new insights have been incorporated into the 2023 version of the staging system by the International Federation of Gynecology and Obstetrics (FIGO), heralding a new era of clinical adoption. The importance of precise pathological evaluation cannot be overstated, serving as a linchpin for prognosticating patient outcomes and steering the course of adjuvant therapies. Through the lens of the updated 2023 FIGO staging for endometrial carcinoma, this discourse aims to elevate the paradigm of pathological diagnosis, promoting a benchmark of standardization and precision for pathologists, thereby empowering clinicians with a deeper and more accurate application of the staging system.

Key words: Endometrial neoplasms, Neoplasm invasiveness, Lymphatic metastasis, Sentinel lymph node, Molecular typing, International Federation of Gynecology and Obstetrics

SI Jing-wen, YU Xiu-jie, SHEN Yan. The Impact of the 2023 FIGO Staging Update of Endometrial Carcinoma on the Content of Pathological Diagnosis[J]. Journal of International Obstetrics and Gynecology, 2024, 51(3): 241-246.

Figures/Tables 2

References 29

[1]	Lortet-Tieulent J, Ferlay J, Bray F, et al. International Patterns and Trends in Endometrial Cancer Incidence, 1978-2013[J]. J Natl Cancer Inst, 2018, 110(4):354-361. doi: 10.1093/jnci/djx214. pmid: 29045681
[2]	Berek JS, Matias-Guiu X, Creutzberg C, et al. FIGO staging of endometrial cancer: 2023[J]. Int J Gynaecol Obstet, 2023, 162(2):383-394. doi: 10.1002/ijgo.14923.
[3]	中华医学会病理学分会女性生殖疾病学组. 子宫内膜癌病理诊断规范[J]. 中华病理学杂志, 2020, 49(3):214-219. doi: 10.3760/cma.j.issn.0529-5807.2020.03.002.
[4]	WHO Classification of Tumours Editorial Board. WHO classification of tumours. Female genital tumours[M]. 5th ed. Lyon: IARC Press, 2020.
[5]	Creasman W. Revised FIGO staging for carcinoma of the endometrium[J]. Int J Gynaecol Obstet, 2009, 105(2):109. doi:10.1016/j.ijgo.2009.02.010. pmid: 19345353
[6]	Bosse T, Peters EE, Creutzberg CL, 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[J]. Eur J Cancer, 2015, 51(13):1742-1750. doi: 10.1016/j.ejca.2015.05.015. pmid: 26049688
[7]	Peters E, Bartosch C, McCluggage WG, et al. Reproducibility of lymphovascular space invasion(LVSI) assessment in endometrial cancer[J]. Histopathology, 2019, 75(1):128-136. doi: 10.1111/his.13871. pmid: 31155736
[8]	Peters E, León-Castillo A, Smit V, et al. Defining Substantial Lymphovascular Space Invasion in Endometrial Cancer[J]. Int J Gynecol Pathol, 2022, 41(3):220-226. doi: 10.1097/PGP.0000000000000806.
[9]	中国研究型医院学会妇产科专业委员会. 子宫内膜癌前哨淋巴结切除临床应用专家共识[J]. 中国妇产科临床杂志, 2020, 21(4):438-440. doi: 10.13390/j.issn.1672-1861.2020.04.033.
[10]	Abu-Rustum N, Yashar C, Arend R, et al. Uterine Neoplasms, Version 1.2023, NCCN Clinical Practice Guidelines in Oncology[J]. J Natl Compr Canc Netw, 2023, 21(2):181-209. doi: 10.6004/jnccn.2023.0006.
[11]	Salman L, Cusimano MC, Marchocki Z, et al. Sentinel Lymph Node Mapping in High-Grade Endometrial Cancer[J]. Curr Oncol, 2022, 29(2):1123-1135. doi: 10.3390/curroncol29020096. pmid: 35200595
[12]	Burg LC, Hengeveld EM, In′t Hout J, et al. Ultrastaging methods of sentinel lymph nodes in endometrial cancer - a systematic review[J]. Int J Gynecol Cancer, 2021, 31(5):744-753. doi: 10.1136/ijgc-2020-001964. pmid: 33187974
[13]	中国研究型医院学会妇产科学专业委员会. 子宫颈癌前哨淋巴结活检临床应用中国专家共识[J]. 中华肿瘤杂志, 2021, 43(10):981-988. doi: 10.3760/cma.j.cn112152-20210720-00526.
[14]	Euscher E, Sui D, Soliman P, et al. Ultrastaging of Sentinel Lymph Nodes in Endometrial Carcinoma According to Use of 2 Different Methods[J]. Int J Gynecol Pathol, 2018, 37(3):242-251. doi: 10.1097/PGP.0000000000000415. pmid: 28700425
[15]	Kim CH, Soslow RA, Park KJ, et al. Pathologic ultrastaging improves micrometastasis detection in sentinel lymph nodes during endometrial cancer staging[J]. Int J Gynecol Cancer, 2013, 23(5):964-970. doi: 10.1097/IGC.0b013e3182954da8. pmid: 23694985
[16]	Cibula D, Raspollini MR, Planchamp F, et al. ESGO/ESTRO/ESP Guidelines for the management of patients with cervical cancer - Update 2023[J]. Int J Gynecol Cancer, 2023, 33(5):649-666. doi: 10.1136/ijgc-2023-004429. pmid: 37127326
[17]	Plante M, Stanleigh J, Renaud MC, et al. Isolated tumor cells identified by sentinel lymph node mapping in endometrial cancer: Does adjuvant treatment matter?[J]. Gynecol Oncol, 2017, 146(2):240-246. doi: 10.1016/j.ygyno.2017.05.024. pmid: 28577885
[18]	Turashvili G, Gómez-Hidalgo NR, Flynn J, et al. Risk-based stratification of carcinomas concurrently involving the endometrium and ovary[J]. Gynecol Oncol, 2019, 152(1):38-45. doi: 10.1016/j.ygyno.2018.10.033. pmid: 30413340
[19]	Vermij L, Smit V, Nout R, et al. Incorporation of molecular characteristics into endometrial cancer management[J]. Histopathology, 2020, 76(1):52-63. doi: 10.1111/his.14015. pmid: 31846532
[20]	李园园, 李倩, 何莲, 等. 子宫内膜癌ProMisE分子分型与淋巴结转移及其他临床特征的关系[J]. 国际妇产科学杂志, 2023, 50(4):377-381,391. doi: 10.12280/gjfckx.20230211.
[21]	Kurnit KC, Kim GN, Fellman BM, et al. CTNNB1 (beta-catenin) mutation identifies low grade, early stage endometrial cancer patients at increased risk of recurrence[J]. Mod Pathol, 2017, 30(7):1032-1041. doi: 10.1038/modpathol.2017.15.
[22]	Kim G, Kurnit KC, Djordjevic B, et al. Nuclear β-catenin localization and mutation of the CTNNB1 gene: a context-dependent association[J]. Mod Pathol, 2018, 31(10):1553-1559. doi: 10.1038/s41379-018-0080-0.
[23]	Travaglino A, Raffone A, Saccone G, et al. Immunohistochemical Nuclear Expression of β-Catenin as a Surrogate of CTNNB1 Exon 3 Mutation in Endometrial Cancer[J]. Am J Clin Pathol, 2019, 151(5):529-538. doi: 10.1093/ajcp/aqy178. pmid: 30715091
[24]	Bosse T, Nout RA, Stelloo E, et al. L1 cell adhesion molecule is a strong predictor for distant recurrence and overall survival in early stage endometrial cancer: pooled PORTEC trial results[J]. Eur J Cancer, 2014, 50(15):2602-2610. doi: 10.1016/j.ejca.2014.07.014. pmid: 25126672
[25]	Asano H, Hatanaka KC, Matsuoka R, et al. L1CAM Predicts Adverse Outcomes in Patients with Endometrial Cancer Undergoing Full Lymphadenectomy and Adjuvant Chemotherapy[J]. Ann Surg Oncol, 2020, 27(7):2159-2168. doi: 10.1245/s10434-019-08103-2. pmid: 31792716
[26]	De Brot L. L1CAM expression in endometrial cancer: Is it really a prognostic factor?[C]. United States and Canadian academy of pathology′s annual meeting, 2023.
[27]	Liu G, Xu P, Fu Z, et al. Prognostic and Clinicopathological Significance of ARID1A in Endometrium-Related Gynecological Cancers: A Meta-Analysis[J]. J Cell Biochem, 2017, 118(12):4517-4525. doi: 10.1002/jcb.26109. pmid: 28466574
[28]	Concin N, Creutzberg CL, Vergote I, et al. ESGO/ESTRO/ESP Guidelines for the management of patients with endometrial carcinoma[J]. Virchows Arch, 2021, 478(2):153-190. doi: 10.1007/s00428-020-03007-z.
[29]	Stelloo E, Nout RA, Osse EM, et al. Improved Risk Assessment by Integrating Molecular and Clinicopathological Factors in Early-stage Endometrial Cancer-Combined Analysis of the PORTEC Cohorts[J]. Clin Cancer Res, 2016, 22(16):4215-4224. doi: 10.1158/1078-0432.CCR-15-2878. pmid: 27006490

分期	2023版FIGO分期^[2]	2009版FIGO分期^[5]
Ⅰ期	肿瘤局限于子宫体和卵巢	肿瘤局限于子宫
ⅠA	肿瘤局限于子宫内膜，或非侵袭性组织学亚型（低级别子宫内膜样癌）侵犯肌层<1/2，无或局灶性LVSI，或预后良好	肿瘤局限于子宫内膜或侵犯肌层<1/2
	ⅠA1：非侵袭性组织学亚型局限于子宫内膜息肉，或局限于子宫内膜
	ⅠA2：非侵袭性组织学亚型侵犯肌层<1/2，无或局灶性LVSI
	ⅠA3：同时存在局限于子宫和卵巢的低级别子宫内膜样癌
ⅠB	非侵袭性组织学亚型侵犯肌层≥1/2，无或局灶性LVSI	肿瘤侵犯肌层≥1/2
ⅠC	侵袭性组织学亚型局限于息肉，或局限于子宫内膜
Ⅱ期	肿瘤侵犯宫颈间质但无子宫体外扩散，或大量LVSI，或侵袭性组织学亚型侵犯子宫肌层	肿瘤侵犯宫颈间质但仍局限于子宫
ⅡA	非侵袭性组织学亚型侵犯宫颈间质
ⅡB	非侵袭性组织学亚型伴大量LVSI
ⅡC	侵袭性组织学亚型侵犯子宫肌层
Ⅲ期	任何组织类型伴局部或区域性扩散	肿瘤局部或区域性扩散
ⅢA	肿瘤累及子宫浆膜面和（或）附件，直接扩散或转移	肿瘤累及子宫浆膜面和（或）附件
	ⅢA1：扩散至卵巢或输卵管（符合ⅠA3期标准的除外）
	ⅢA2：肿瘤侵犯子宫浆膜或通过子宫浆膜向外扩散
ⅢB	肿瘤转移或直接蔓延到阴道和（或）宫旁，或转移到盆腔腹膜	肿瘤累及阴道和（或）宫旁
	ⅢB1：肿瘤转移或直接蔓延到阴道和（或）宫旁
	ⅢB2：肿瘤转移到盆腔腹膜
ⅢC	肿瘤转移至盆腔和（或）腹主动脉旁淋巴结	肿瘤转移至盆腔和（或）腹主动脉旁淋巴结
	ⅢC1：转移到盆腔淋巴结	盆腔淋巴结阳性
	ⅢC1i：微转移（转移灶直径0.2~2.0 mm）
	ⅢC1ii：宏转移（转移灶直径>2.0 mm）
	ⅢC2：转移至肾血管下方的腹主动脉旁淋巴结，有或无盆腔淋巴结转移	腹主动脉旁淋巴结阳性和（或）盆腔淋巴结阳性
	ⅢC2i：微转移（转移灶直径0.2~2.0 mm）
	ⅢC2ii：宏转移（转移灶直径>2.0 mm）
Ⅳ期	肿瘤侵犯膀胱黏膜和（或）肠黏膜和（或）远处转移	肿瘤侵犯膀胱和（或）侵犯直肠黏膜和（或）远处转移
ⅣA	肿瘤侵犯膀胱和（或）侵犯肠黏膜	肿瘤侵犯膀胱和（或）侵犯直肠黏膜
ⅣB	肿瘤转移到盆腔外腹腔腹膜	远处转移，包括腹腔内转移和腹股沟淋巴结转移
ⅣC	远处转移，包括转移到肾血管上方的任何腹腔外或腹腔内的淋巴结、肺、肝、脑或骨转移

分期	2023版FIGO分期^[2]	2009版FIGO分期^[5]
Ⅰ期	肿瘤局限于子宫体和卵巢	肿瘤局限于子宫
ⅠA	肿瘤局限于子宫内膜，或非侵袭性组织学亚型（低级别子宫内膜样癌）侵犯肌层<1/2，无或局灶性LVSI，或预后良好	肿瘤局限于子宫内膜或侵犯肌层<1/2
	ⅠA1：非侵袭性组织学亚型局限于子宫内膜息肉，或局限于子宫内膜
	ⅠA2：非侵袭性组织学亚型侵犯肌层<1/2，无或局灶性LVSI
	ⅠA3：同时存在局限于子宫和卵巢的低级别子宫内膜样癌
ⅠB	非侵袭性组织学亚型侵犯肌层≥1/2，无或局灶性LVSI	肿瘤侵犯肌层≥1/2
ⅠC	侵袭性组织学亚型局限于息肉，或局限于子宫内膜
Ⅱ期	肿瘤侵犯宫颈间质但无子宫体外扩散，或大量LVSI，或侵袭性组织学亚型侵犯子宫肌层	肿瘤侵犯宫颈间质但仍局限于子宫
ⅡA	非侵袭性组织学亚型侵犯宫颈间质
ⅡB	非侵袭性组织学亚型伴大量LVSI
ⅡC	侵袭性组织学亚型侵犯子宫肌层
Ⅲ期	任何组织类型伴局部或区域性扩散	肿瘤局部或区域性扩散
ⅢA	肿瘤累及子宫浆膜面和（或）附件，直接扩散或转移	肿瘤累及子宫浆膜面和（或）附件
	ⅢA1：扩散至卵巢或输卵管（符合ⅠA3期标准的除外）
	ⅢA2：肿瘤侵犯子宫浆膜或通过子宫浆膜向外扩散
ⅢB	肿瘤转移或直接蔓延到阴道和（或）宫旁，或转移到盆腔腹膜	肿瘤累及阴道和（或）宫旁
	ⅢB1：肿瘤转移或直接蔓延到阴道和（或）宫旁
	ⅢB2：肿瘤转移到盆腔腹膜
ⅢC	肿瘤转移至盆腔和（或）腹主动脉旁淋巴结	肿瘤转移至盆腔和（或）腹主动脉旁淋巴结
	ⅢC1：转移到盆腔淋巴结	盆腔淋巴结阳性
	ⅢC1i：微转移（转移灶直径0.2~2.0 mm）
	ⅢC1ii：宏转移（转移灶直径>2.0 mm）
	ⅢC2：转移至肾血管下方的腹主动脉旁淋巴结，有或无盆腔淋巴结转移	腹主动脉旁淋巴结阳性和（或）盆腔淋巴结阳性
	ⅢC2i：微转移（转移灶直径0.2~2.0 mm）
	ⅢC2ii：宏转移（转移灶直径>2.0 mm）
Ⅳ期	肿瘤侵犯膀胱黏膜和（或）肠黏膜和（或）远处转移	肿瘤侵犯膀胱和（或）侵犯直肠黏膜和（或）远处转移
ⅣA	肿瘤侵犯膀胱和（或）侵犯肠黏膜	肿瘤侵犯膀胱和（或）侵犯直肠黏膜
ⅣB	肿瘤转移到盆腔外腹腔腹膜	远处转移，包括腹腔内转移和腹股沟淋巴结转移
ⅣC	远处转移，包括转移到肾血管上方的任何腹腔外或腹腔内的淋巴结、肺、肝、脑或骨转移

操作出处	取材方式	切片间隔厚度（μm）	水平面数量（个）	每水平面切片张数
MD Anderson Cancer Center^[14]	间隔2 mm，垂直于长轴方向取材	250	5	3张（1张HE+2张未染色）
MSKCC^[15]		50	2	2张（1张HE+1张未染色）
ESP指南^[16]		200	5	1张HE，至少2个水平附加1张未染色切片行免疫组织化学检查
中国共识^[13]		50	2	2张（1张HE+1张未染色）

操作出处	取材方式	切片间隔厚度（μm）	水平面数量（个）	每水平面切片张数
MD Anderson Cancer Center^[14]	间隔2 mm，垂直于长轴方向取材	250	5	3张（1张HE+2张未染色）
MSKCC^[15]		50	2	2张（1张HE+1张未染色）
ESP指南^[16]		200	5	1张HE，至少2个水平附加1张未染色切片行免疫组织化学检查
中国共识^[13]		50	2	2张（1张HE+1张未染色）