Gynecologic Oncology 133 (2014) 401404

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Gynecologic Oncology

j ourna l homepage: www.e lsev ie r .com/ locate /ygynoClinical Commentary2014 FIGO staging for ovarian, fallopian tube and peritoneal cancerCancer staging is a core principle in understanding the severity of pa-tients' clinical condition, predicting the outcome, and planning ade-quate treatment. Staging is necessary for explaining epidemiologicchanges, defining the disease at presentation, and evaluating the overallimpact of new therapies. In essence, it assigns patients to prognosticgroups that require specific treatments. The steps of staging typicallybegin by establishing the histopathologic diagnosis, according to thetumor cell type, and assessing prognosis based on extent of diseaseand other known prognostic parameters. Recently, the presence of var-iousmolecular genetic alterations has been used in the establishment ofprognosis and even staging classification in some tumors but gyneco-logic cancers have continued to rely on physical, radiographic and surgi-cal findings.

This editorial is written to make the readership aware of the recentchanges that have been made by the International Federation of Gyne-cology and Obstetrics (FIGO) in the staging classification of ovarian can-cer and the reasoning behind those changes [1]. Even if the FIGOCommittee on Gynecologic Oncology utilized the best evidence current-ly available, this is always a somewhat subjective process. Furthermore,one needs to be aware that FIGO is an international organization thatmust take into account the needs of women with gynecologic cancersthroughout the world, and not just those from countries that are re-source rich. The first FIGO ovarian cancer staging was published in1973 in Volume 15 of the FIGO Annual Report. Since that time therehave been two other changes including this one in 1988 and 2013.

Ovarian cancer is not one disease. Several distinct tumors withunique clinical andpathological featuresmay arise in the ovary. Approx-imately 90% of ovarian cancers are carcinomas (malignant epithelial tu-mors) and, based on histopathology, immunohistochemistry, andmolecular genetic analysis, at least 5 main types are currently distin-guished: high-grade serous carcinoma (HGSC [70%]); endometrioid car-cinoma (EC [10%]); clear-cell carcinoma (CCC [10%]); mucinouscarcinoma (MC [3%]); and low-grade serous carcinoma (LGSC [lessthan 5%] [2]). These tumor types (which account for 98% of ovarian car-cinomas) can be reproducibly diagnosed by lightmicroscopy and are es-sentially different diseases, as indicated by differences in epidemiologicand genetic risk factors; precursor lesions; ways of spread; andmolecu-lar changes during oncogenesis, response to chemotherapy, and out-come [3] Much less frequent are malignant germ cell tumors(dysgerminomas, yolk sac tumors, and immature teratomas [3% of ovar-ian cancers]) and potentially malignant sex cord-stromal tumors (1%2%, mainly granulosa cell tumors). The biomarker expression profilewithin a given histotype is consistent across stages. In short, ovariancancers differ primarily based on histotype.

Primary fallopian tube cancer and primary peritoneal cancer are raremalignancies but share many clinical andmorphologic similarities withhttp://dx.doi.org/10.1016/j.ygyno.2014.04.0130090-8258/ 2014 Elsevier Inc. All rights reserved.HGSC; i.e., the most common type of ovarian cancer (in the past, re-ferred to as papillary serous carcinoma) and the prototype tumor oc-curring in women with BRCA1 or BRCA2 germline mutations. In thesepatients, compelling evidence for a tubal derivation of their tumors,mainly those encountered at early stage, has accumulated over thepast decade [46]. Evidence of a tubal origin is weaker in the far morecommon sporadic HGSCs, and a multicentric origin of these tumors(i.e. arising from ovarian surface mesothelial invaginations or corticalinclusion cysts, implantation of tubal-type epithelium into the ovary[endosalpingiosis], or the pelvic peritoneum [the so-called secondarymllerian system]) cannot be ruled out. Recently, it has been hypothe-sized that cytokeratin7-positive embryonic/stem cells would be capableof mullerian differentiation in cortical inclusion cysts resulting fromovarian surface epithelium (mesothelium) invaginations. Thus, embry-onic progenitorswould give rise to immunophenotypically distinct neo-plastic progeny [7] which would support the old concept of mullerianneometaplasia. On the other hand, it has been demonstrated that thevast majority of ECs and CCCs arise in the ovary from endometriosis.

Based on the putative tubal or peritoneal origin of a number ofBRCA+ HGSCs, and the fact that they aremanaged clinically in a similarmanner regardless their ovarian, tubal, or peritoneal derivation, mostFIGO Committee members felt that FIGO staging of ovarian, peritoneal,and fallopian tube cancers should be considered collectively [8]. The pri-mary site (i.e. ovary, fallopian tube, or peritoneum) should be designat-ed where possible. In some cases, it might not be possible to delineatethe primary site clearly; such cases should be listed as undesignated.

The process of updating the staging classification of ovarian,fallopian tube, and primary peritoneal cancer started 4 years ago witha proposal that was sent to all relevant gynecology oncology organiza-tions and societies throughout the world and input was collated, evalu-ated, and formulated into the staging that is presented below. Allsuggestions are based on the best available evidence. The committee ac-knowledged that there are areas that are not supported by strong evi-dence and has been careful to ensure that changes are not madewithout quality evidence when available. The new staging below wasreached by consensus of all participating in the FIGO meeting held inRome, Italy, on October 7th, 2012, some of whom were representativesof their organizations. The new stagingwas presented to the FIGO Exec-utive Board on October 12, 2012, and approved two weeks later.

Ovarian cancer remains largely a surgically staged disease. The prog-nosis is based on histologic type, radiographic, and operative extent ofthe disease. The proposed staging system is noted below (Table 1).(See Tables 2 and 3).

Precise histopathologic diagnosis ismandatory for successful catego-rization and treatment of ovarian cancers, as different histologic typesrespond differently to treatment. To be practical, the FIGO committee

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Table 12014 FIGO ovarian, fallopian tube, and peritoneal cancer staging system and corresponding TNM.

I Tumor confined to ovaries or fallopian tube(s) T1

IA Tumor limited to one ovary (capsule intact) or fallopian tube, No tumor on ovarian or fallopian tube surfaceNomalignant cells in the ascites or peritonealwashings

T1a

IB Tumor limited to both ovaries (capsules intact) or fallopian tubesNo tumor on ovarian or fallopian tube surfaceNo malignant cells in the ascites or peritoneal washings

T1b

IC Tumor limited to one or both ovaries or fallopian tubes, with any of the following:IC1 Surgical spill intraoperativelyIC2 Capsule ruptured before surgery or tumor on ovarian or fallopian tube surfaceIC3 Malignant cells present in the ascites or peritoneal washings

T1c

II Tumor involves one or both ovaries or fallopian tubes with pelvic extension (below pelvic brim) or peritoneal cancer (Tp) T2IIA Extension and/or implants on the uterus and/or fallopian tubes/and/or ovaries T2aIIB Extension to other pelvic intraperitoneal tissues T2b

III Tumor involves one or both ovaries, or fallopian tubes, or primary peritoneal cancer, with cytologically or histologically confirmed spread to theperitoneum outside the pelvis and/or metastasis to the retroperitoneal lymph nodes T3

IIIA Metastasis to the retroperitoneal lymph nodes with or without microscopic peritoneal involvement beyond the pelvis T1,T2,T3aN1IIIA1 Positive retroperitoneal lymph nodes only (cytologically or histologically proven)IIIA1(i) Metastasis 10 mm in greatest dimension (note this is tumor dimension and not lymph node dimension) T3a/T3aN1IIIA1(ii) Metastasis N 10 mm in greatest dimension

IIIA 2 Microscopic extrapelvic (above the pelvic brim) peritoneal involvement with or without positive retroperitoneal lymph nodes T3a/T3aN1IIIB Macroscopic peritonealmetastases beyond the pelvic brim 2 cm in greatest dimension,with orwithoutmetastasis to the retroperitoneal lymphnodes T3b/T3bN1III C Macroscopic peritoneal metastases beyond the pelvic brim N 2 cm in greatest dimension, with or without metastases to the retroperitoneal nodes (Note 1) T3c/T3cN1

IV Distant metastasis excluding peritoneal metastasesStage IV A: Pleural effusion with positive cytologyStage IV B: Metastases to extra-abdominal organs (including inguinal lymph nodes and lymph nodes outside of abdominal cavity) (Note 2)

Any T, Any N,M1

(Note 1: includes extension of tumor to capsule of liver and spleen without parenchymal involvement of either organ)(Note 2: Parenchymal metastases are Stage IV B)

T3c/T3cN1)

Notes:1. Includes extension of tumor to capsule of liver and spleen without parenchymal involvement of either organ.2. Parenchymal metastases are Stage IV B.

Table 2Carcinoma of the ovaryfallopian tubeperitoneum stage grouping.

FIGO UICC

(Designate primary: Tov, Tft, Tp or Tx)Stage T N MIA T1a N0 M0IB T1b N0 M0IC T1c N0 M0IIA T2a N0 M0IIB T2b N0 M0IIIA T3a N0 M0

T3a N1 M0IIIB T3b N0 M0

T3b N1 M0IIIC T3c N01 M0

T3c N1 M0IV Any T Any N M1Regional nodes (N)Nx Regional lymph nodes cannot be assessedN0 No regional lymph node metastasisN1 Regional lymph node metastasisDistant metastasis (M)Mx Distant metastasis cannot be assessedM0 No distant metastasisM1 Distant metastasis (excluding peritoneal metastasis)

Notes:1. The primary site i.e. ovary, fallopian tube or peritoneum should be designatedwherepossible. In some cases, it may not be possible to clearly delineate the primary site, andthese should be listed as undesignated.2. The histologic type of should be recorded.3. The staging includes a revision of the stage III patients and allotment to stage IIIA1 isbased on spread to the retroperitoneal lymph nodes without intraperitoneal dissemina-tion, because an analysis of these patients indicates that their survival is significantly bet-ter than those who have intraperitoneal dissemination.4. Involvement of retroperitoneal lymph nodes must be proven cytologically orhistologically.5. Extension of tumor from omentum to spleen or liver (Stage III C) should be differentiat-ed from isolated parenchymal splenic or liver metastases (Stage IVB).

402 Clinical Commentarychose a staging classification system that takes into account the mostrelevant prognostic parameters shared by all tumor types. However, itwas agreed on by all that histologic type should be designated at thetime of diagnosis and staging. The five agreed upon epithelial histologictypes, aswell asmuch less commonmalignant germ cell and potentiallymalignant sex cord-stromal tumors, are listed below.

Histologic types:

Carcinomas (by order of frequency)High-grade serous carcinoma (HGSC)Endometrioid carcinoma (EC)Clear-cell carcinoma (CCC)Mucinous carcinoma (MC)Low-grade serous carcinoma (LGSC).

Note: Transitional cell carcinoma is currently interpreted as a mor-phologic variant of HGSC; malignant Brenner tumor is considered alow-grade carcinoma which is extremely rare.

Malignant germ cell tumors (dysgerminomas, yolk sac tumors, andimmature teratomas) Potentially malignant sex cord-stromal tumors(mainly rare cases of granulosa cell tumors and SertoliLeydig cell tu-mors with heterologous sarcomatous elements).

The issues discussed and concluded by the FIGO committee will betaken one stage at a time, controversial issues raised, and the availabledata cited as appropriate.

Staging should be considered fluid. As more prognostic features be-come available these should be used to further predict outcomes anddetermine treatment. The world is getting smaller in the sense thatstaging systems must be applicable universally and including resourcerich as well as resource poor regions. Toward this end, three membersof FIGO will now be on the AJCC staging committee and there is repre-sentation of the UICC on the AJCC. The International Gynecologic CancerSociety and the Society of Gynecologic Oncology now have nonvotingrepresentation on the FIGO committee as well. We need to continue togain consensus internationally by having cross representation on our

Table 3Explantation of the Staging Changes

Stage IDisease confined to the ovary after comprehensive staging T1N0M0Stages IA and IB are unchanged from the 1988 staging. T1aN0M0IA remains tumor limited to oneovary (capsule intact) or fallopian tube. There can be nodisease on the ovary or fallopian tube surface. There are nomalignant cells inthe ascites or peritoneal washings. Primary peritoneal has no Stage IA.

1B is unchanged and remains tumor limited to both ovaries with capsule intact or fallopian tubes; and there can be no malignant cells on ovarian or fallopian tubesurfaces. There are no malignant cells in the ascites or peritoneal washings.

T1bN0M0

IC represents a change for the 1988 staging system. It still designates positive cytology but, if possible, must designate the reason for malignant cells being present;hence, this substage is divided into three groups.

T1cN0M0

1C1 represents disease confined to one or both ovaries with capsule rupture during surgery1C2 represents rupture before surgery or tumor excrescences on the surface of the tube or ovary.1C3 represents malignant cells in the peritoneal cavity regardless of cause.CommentsSpecific issues surrounding stage I tumors need to be consideredwhen evaluating Stage I patients surgically and pathologically. Bilateral tumors that are large on oneside andmultiple or small on the other could representmetastases up to one third of the time [9,10]. The significance of positive cytology is poorly understood andis one of the reasons that the committee elected to divide it into three categories. Some studies have found that intraoperative rupture portends aworse prognosisthan if the capsule is unruptured. In one multivariate analysis, both capsule rupture and positive cytology were independent predictors of worse disease freesurvival [11]. Surface involvement of the ovary or fallopian tube should be considered present only when excrescences have cancer cells in direct contact with theperitoneal cavity, breaking through the surface of the ovarian capsule. Tumors with a smooth surface usually don't show an exposed layer of neoplastic cells.Histologic grade influences survival and is given with the histotype except for endometrioid carcinoma andmucinous cancers which should be graded. Practicallyall clear cell carcinomas are high grade.

Stage IIStage II ovarian cancer includes disease confined to the pelvis (below the pelvic brim). It involves one or both ovaries or fallopian tubes with pelvic extension orprimary peritoneal cancer.

T2N0M0

IIA Extension and/or implants on the uterus and/or fallopian tubes and/or ovaries T2aN0M0IIB Extension to other pelvic intraperitoneal tissues/organs T2bN0M0Comments:Stage II ovarian cancer remains controversial and ill defined. It comprises a small group of ovarian cancer patients that have direct extension of their tumors to otherpelvic organs without evidence of metastatic disease. However, it also includes a group of patients that has metastases to the pelvic peritoneum. In this secondgroup of patients, disease is similar to that of stage III patients. Disease invading through the bowel wall and into the mucosa increases the stage to IVB.

Stage IIIStage III Cancer involves 1 or both ovaries, fallopian tubes, or is primarily from the peritoneum with histologically confirmed spread outside of the pelvis and/ormetastases to the retroperitoneal nodes.

T1/T2N1MO

IIIA1 Positive retroperitoneal nodes only. This can be confirmed histologically or cytologically.lllA(i) Metastases up to and including 10 mm in greatest dimensionIIIA(ii) Metastases more than 10 mm in greatest dimensionStage IIIA2: Microscopic extrapelvic (above the boney pelvic brim) peritoneal involvement with or without metastases to the retroperitoneal lymph nodes T3a2N0/N1

M0IIIB: Macroscopic peritoneal metastases beyond the pelvis up to and including 2 cm in greatest dimension, with or withoutmetastases to the retroperitoneal lymphnodes.

T3bN0/N1M0

IIIC:Macroscopic peritoneal disease beyond the pelvismore than 2 cm ingreatest diameter, with orwithoutmetastases to the retroperitoneal lymphnodes (includestumor extension to the capsule of the liver and spleen but no parenchymal metastases).

CommentsApproximately, 85% of ovarian cancers present as stage III tumors and the vast majority are high-grade serous carcinomas [12]. A little less than 10% of patients withovarian cancer that appear to have stage I disease will have isolated lymph nodemetastases. The likelihood of having nodal metastasis in other stages are: III, 55%and IV, 88% [13]. There is some evidence that exclusive retroperitoneal disease portends a better prognosis and for this reason the new staging system addressesthis issue in the IIIA category [1419]. It should be noted that the size separating the IIIA tumors applies to the tumor size and not the lymph node size.

Stage IV: Distant metastases excluding peritoneal or retroperitoneal nodal disease below the diaphragm.IVA: Pleural effusion with positive cytologyIVB: Metastases to extra abdominal sites including inguinal lymph nodes and parenchymal involvement of visceral organs including liver and spleen. Transmuralinvolvement of a visceral structure also represents stage IVB disease.

403Clinical Commentaryentire representative staging committees. This will help us standardizecare and staging systems throughout the world. In the future it ishoped that organizations such as UICC, AJCC, and FIGO will continue towork together to achieve this goal.

Conflict of interest statement

The authors declare that there are no conflicts of interest.

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Jaime PratDepartment of Pathology, Hospital de la Santa Creu i Sant Pau, Autonomous

University of Barcelona, Sant Quinti, 87-89, 08041 Barcelona, Spain

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2014 FIGO staging for ovarian, fallopian tube and peritoneal cancerConflict of interest statementReferences