1460

Dnternational Federation of Gynecology

and Obstetrics Staging of Endometrial
Cancer 1988
John J. Mikuta, M.D.

In 1988,the International Federation of Gynecology and

Obstetrics (FIGO)Cancer Committee changed the staging
of endometrial carcinoma from a clinical one to a surgicopathologic one. The emphasis in the new FIGO system
was changed to the pathologic findings in the uterus, cervix, adnexa, and pelvic and/or periaortic nodes, and peritoneal cytologic findings. The major changes in this staging system were (1)the use of the depth of myometrial
invasion and (2) the identification of tumor cells in peritoneal cytologic examination and of invasion in the retroperitoneal lymph nodes. Preoperative endocervical curettage was no longer necessary. Currently, the high level of
operability of patients with endometrial carcinoma
makes this staging system a viable one, which will provide information about the need for additional treatment.
The use of the grading system for the tumor also was
refined to upgrade nuclear changes that were inappropriate for the architectural grade. In serous adenocarcinomas, clear cell adenocarcinomas, and squamous cell
carcinomas, nuclear grading took precedence. Adenocarcinomas with squamous differentiation were graded according to the nuclear grade of the glandular component.
Cancer 1993: 71:1460-3.
Key words: cancer, cancer staging, endometrial cancer,
cancer surgery.
Endometrial cancer is the most common invasive gynecologic malignancy, with an estimated 33,000 new
cases diagnosed in 1990 with 4500 deaths. Despite the
overall appearance of a favorable prognosis in this malignancy (survival rate range, 80-90% when the disease
is confined to the uterine corpus), recently, a new look
Presented at the National Conference on Gynecologic Cancers,
Orlando, Floris, April 2-4,1992.
From the University of Pennsylvania School of Medicine, Hospital of the University of Pennsylvania, Philadelphia, Pennsylvania.
Address for reprints: John 1. Mikuta, M.D., the University of
Pennsylvania School of Medicine, Hospital of the University of
Pennsylvania, 1000 Courtyard, 3400 Spruce Street, Philadelphia, PA
19104.
Accepted for publication September 2, 1992.

at the relatively low cure rates in Stage I disease was

taken. Various prognostic factors were identified. These
include the tumor grade, the depth of myometrial invasion, cervical involvement, lymph node metastases,
and peritoneal cytologic findings. These prognostic factors were used to define a surgicopathologic staging
system for endometrial carcinoma that was adopted by
the International Federation of Gynecology and Obstetrics (FIGO) Cancer Committee on Oncology in 1988.
The incorporation of these factors into the new
staging system has provided, as it did with ovarian
cancer, the most accurate means of identifying the degree of spread of the tumor into the uterine muscle itself, into adjacent structures, and to distant areas. As in
any system that recently has been proposed, there are
bound to be discrepancies, inadequacies, and inconsistencies that must be corrected with time.
History of Endometrial Cancer Staging
The early FIGO staging for endometrial cancer was
adopted in 1950 and was used from approximately
1951-1961. It was a simple system based on two criteria. The major staging was done after a determination of
whether the cancer was confined to the corpus or had
spread beyond the corpus. Stage I included tumor confined to the corpus, and Stage I1 indicated spread
beyond the uterus. These stages then were subdivided
into whether the patient was medically operable or not.
The spread of the tumor was defined by clinical examination and included the findings at the time of a diagnostic dilatation and curettage with endocervical curettage (Fig. l).' It should be noted that the reason for
using medical operability in this early staging system
was related to the association between endometrial
cancer and obesity, hypertension, and diabetes. The
early framers did not have the advantages of modern
medical advances that are available currently. In addition, the quality of anesthesia, blood availability, and
gynecologic surgeons with the expertise to do more ex-

FIGO Staging of Endometrial CancerlMikuta

stage 0.
Cases which the pathologist considers most likely to be of a
carcinomatous nature though it is impossible to arrive at a
definite microscopic diagnosis.
Stage I.
The growth is confir.ed to the uterus
Group 1.

Operation advisable.

Group 2.

Bad operative risks.

Stage 11.
The growth has spread outside the uterus.

Figure 1. FIG0 staging for endometrial cancer 1950-1961. Stage 0,

cases that the pathologist considers most likely to be of a
carcinomatous nature although it is impossible to arrive at a definite
microscopic diagnosis. Stage I, growth is confined to the uterus.
Group 1, operation advisable. Group 2, bad operative risks. Stage
II, growth has spread outside the uterus.

tensive dissections in such high-risk patients added to

the operability problems.
In 1961, the FIGO Committee on Cancer revised
the staging of endometrial carcinoma. It added a special
stage for cervical involvement and one for extrauterine
spread that was confined to the pelvis. Stage IV was
added to include bladder and rectal mucosal involvement or spread outside the pelvis (Fig. 2).1
By 1971, it was evident that other factors were significant in the prognosis and natural history of endometrial cancer. It was emphasized repeatedly that three
parameters of "virulence" should be added to the staging.2 These were: the size of the uterine cavity, the lack
of differentiation of the tumor, and clinical involvement of the cervix. The FIGO Committee on Cancer in

1461

1971 changed the corpus cancer staging as follows.

Stage I was still defined as tumor confined to the corpus, using clinical criteria and including fractional curettage and pelvic examination. Stage I was subdivided
into Ia and Ib based on the depth of the uterine cavity.
A measurement or sounding from the external cervical
0s to the top of the interior portion of the uterus that
was less than 8 cm was Stage Ia. If it were greater than 8
cm, it was defined as Stage Ib. Also, the grading of the
tumor was included in the staging and was based primarily on the degree of glandular versus nonglandular
components (Fig. 3).*f3
In 1970, a series of patients with endometrial
cancer was reported who were treated with radical hysterectomy and pelvic lymphadene~tomy.~
In this series,
11.4% of patients had pelvic lymph node metastases.
This highlighted two issues. First, endometrial cancers
confined to the corpus did metastasize to the pelvic and
paraaortic nodes. This finding differed from the conventional teaching of many years. Second, the treatment of
endometrial cancer for three decades consisted of preoperative intrauterine radium placement by various techniques (e.g., tandem, Crossen, and Heyman) followed
in 6 weeks by hysterectomy and bilateral salpingo-ooStage 0.
Carcinoma in-situ.

Histological findings auspicious of

malignancy.
Stage I.
The carcinoma is confined to the corpus.
Stage Ia.
The length Of the uterine cavity is 8 cm. or less.
Stage Ib,

Stage 0.
The length of the uterine cavity is greater than 8 cm.
Histological findings suspicious of malignancy but not
It is desirable that Stage I cases be subgrouped with regard
proven.
Stage I.
The carcinoma is confined to the corpus.

G1.

Highly differentiated adenomatous carcinoma.

GZ.

Differentiated adenomatous carcinoma with partly solid

Stage 11.
The carcinoma has involved the corpus and the cervix.
Stage 111.
The carcinoma has extended outside the uterus but not
outside the true pelvis.
Stage IV.
The carcinoma has extended outside the true pelvis or has
obviously involved the mucosa of the bladder or rectun.

Figure 2. FIGO staging for endometrial cancer 1962-1971. Stage 0,

histologic findings suggesting malignancy but not proved. Stage I,
the carcinoma is confined to the corpus. Stage 11, the carcinoma has
involved the corpus and the cervix. Stage 111, the carcinoma has
extended outside the uterus but not outside the true pelvis. Stage
IV, the carcinoma has extended outside the true pelvis or has
involved the mucosa of the bladder or rectum obviously.

tp

the histological type of the adenocarcinoma as follows:

area.
G3.

Predominantly solid or entirely undifferentiated

carcinoma

Stage 11, I11 and IV.

Essentially unchanged from 1962.

Figure 3. FIGO staging for endometrial cancer 1971-1988. Stage 0,

carcinoma in situ, histologic findings suggesting malignancy. Stage
I, the carcinoma is confined to the corpus. Stage la, the length of the
uterine cavity is 8 cm or less. Stage Ib, the length of the uterine
cavity is greater than 8 cm. It is desirable that Stage I cases be
subgrouped with regard to the histologic type of the
adenocarcinoma as follows: G1, highly differentiated adenomatous
carcinoma; C2, differentiated adenomatous carcinoma with partly
solid area; and G3, predominantly solid or entirely undifferentiated
carcinoma. Stages 11,111, and IV, essentially unchanged from 1962
staging system.

1462

CANCER Supplement February 25, 2993, Volume 71, No. 4

phorectomy. It is obvious that no significant amount of

radiation was delivered to the pelvic nodes by this
method, although external pelvic radiation was being
administered routinely to patients with Stage Ib cervical
cancers, a situation with a comparable risk for nodal
metastases. At this time, the nodal metastatic potential,
especially in the pelvis, was virtually ignored.
In 1975, Boronow5 published an article entitled
"Endometrial Cancer: Not a Benign Disease." This
acted among other things, as a turning point in reassessing our knowledge concerning this lesion. In this
article, four "myths" relating to endometrial cancer
were described as follows.
1, Endometrial cancer is a benign disease.
2. The best way to treat endometrial cancer has been
defined.
3. The prognostic factors have been defined sufficiently.
4. Pelvic and aortic nodes are of little or no consequence in endometrial cancer.

The evidence presented in this article reaffirmed

the information with respect to the histologic grade as it
related to survival, lymph node metastasis, and the
depth of myometrial invasion. It also showed that the
depth of myometrial invasion was related to survival
and lymph node metastasis. In 1977, the Gynecologic
Oncology Group established a pilot study directed at
evaluating in a uniform way the natural history of endometrial cancer.6
By 1984,' there was significant solidification of the
risk factors associated with endometrial cancer. This
was reaffirmed again in 1991.' These were divided into
two groups, the first being uterine risk factors and the
second, extrauterine risk factors. The intrauterine risk
factors were the following: (1) histologic grade, (2)
depth of myometrial invasion, (3) cervical extension,
and (4) vascular space invasion. The extrauterine risk
factors are: (1) pelvic node metastases, (2) aortic node
metastases, (3) adnexal metastases, (4) penetration of
uterine serosa, and (5) positive peritoneal cytologic findings.
Recognizing the advances in information with respect to the natural history of endometrial cancer and
the influence of this on survival, the FIGO Committee
on Oncology in 1988 decided to develop a staging system incorporating this new information. This resulted
in the following FIGO staging system as of January
1989.9
Stage I. Limited to corpus.
Ia. Limited to endometrium.
Ib. Invasion < */z of myometrium.
Ic. Invasion > l/z of myometrium.

Each case is also graded G1, G2, G3. Grading will

be based on nuclear/cytoplasmic abnormalities
rather than morphology alone.
Stage 11. Involvement of the cervix.
IIa. Glandular involvement only.
IIb. Cervical stromal involvement.
Each case will be graded histologically G1, G2, G3.
Stage 111. Spread outside of the uterus, confined to
pelvis (not including bladder or rectal involvement).
IIla. Involvement of uterine serosa, adnexa (ae),
positive peritoneal cytology.
IIIb. Spread to vagina.
IIIc. Spread to retroperitoneal nodes.
Each case will also be graded histologically G1,
G2, G3.
Stage IV. Spread to the bladder, rectum, distant sites.
IVa. Involvement of bladder and/or rectal mucosa.
IVb. Distant, intra-abdominal spread, inguinal
nodes.
Each case will also be graded histologically G1,
G2, G3.
This staging system, loosely called a surgical one, is
really a surgicopathologic one. It is evident that the definition of the pathologic findings would be altered by
preoperative radiation therapy, particularly by external
beam, because the delay and radiation effects between
the original diagnosis and final completion of treatment
would allow changes to occur that might modify the
appropriate delineation of the surgicopathologic findings. When intracavitary radiation is used, immediate
hysterectomy may show no significant histologic
changes. Again, a delay of some time between the application and the surgery might. This new staging system assumes that most patients will be treated by a
primary surgical approach to provide the best information for staging in addition to being therapeutic. If prior
radiation has been used, the clinical staging system of
1971 is applied.
As a result of the changes in staging, the fractional
curettage, prescribed earlier, is no longer necessary. Finally, it is recommended that the myometrium be measured so that the depth of myometrial invasion be identified in relation to the full thickness of the myometrium.
As mentioned earlier, with respect to the grading of
the tumor:
1. Significant nuclear atypia will increase the histologic grade one step.
2. In serous papillary, adenosquamous, and clear cell
carcinomas, the nuclear grade will take preference.
3. Adenocarcinoma with squamous differentiation

FIGO Staging of Endometrial CancerlMikuta

will be graded according to the nuclear grade of the

glandular component.
Note also that the designation of Stage 0, carcinoma in situ, was dropped because it was found to be of
limited value and was equated primarily with atypical
endometrial hyperplasia.

1463

and where nodal dissection or sampling should be

done.
This historically oriented review of endometrial
cancer staging was designed to show the dynamic nature of our application of scientific information to clinical issues. Things surely will change as additional information becomes available. Flexibility in the development of staging systems is vital to allow the integration
of this new information.

Discussion
References

The new surgkopathologic FIGO staging system for

endometrial cancer has several advantages. It provides
the most accurate method for defining the extent of the
disease, the desirability and need for postoperative
treatment, and a reasonable estimate of the prognosis.
All these factors are desirable features. However, objections have been voiced with respect to the placement of
high-risk findings, e.g., Grade 3 cancer into a Stage I
category and a low-risk cancer, e.g., fallopian tube extension in Stage IIIa. There has been much criticism
about the need for node sampling or dissection to define this aspect of tumor extension. In reality, the endometrial cancer staging provides the same need for
proper surgicopathologic evaluation as it does in ovarian cancer. It is therefore incumbent on the clinician
who discovers and has to treat a patient with endometrial cancer to define those cases that can be managed
readily and those that will require greater surgical expertise and training. In hospitals that can provide this
service, it is possible, by careful pathologic evaluation
of the removed uterus at the time of the surgery to identify those patients in whom nodal metastases are likely

1. Kottmeier HL, editor. Annual report on the results of treatment

in carcinoma of the uterus and vagina. Stockholm: Kungl Boktryckeriet PA Norstedt and Soner, 1967:17-27.
2. Gusberg SB. The problem of staging endometrial cancer. Obstet
Gyriecol 1966; 28:305-8.
3. Gusberg SB, Yannopoulos D. Therapeutic decisions in corpus
cancer. Am \ Obstef Gyriecol 1964; 88:157-62.
4. Lewis BU, Stallworthy JA, Cowdell R. Adenocarcinoma of the
body of the uterus. Br \ Obstet Gyrraecol 1970; 77:343-8.
5. Boronow RC. Endometrial cancer: not a benign disease. Obstet
Gyriecol 1975; 47:630-4.
6. Creasman WT, Boronow RC, Morrow CP, DiSaia PJ, Blessing J.
Adenocarcinoma of the endometrium: its metastatic lymph
node potential. Gyriecol Oiicol 1976; 4:239-43.
7. Boronow RC, Morrow CP, Creasman WT, DiSaia PJ, Silverberg
SG, Miller A, et al. Surgical staging in endometrial cancer: clinical-pathological findings of a prospective study. Obstet Gyriecol
1984; 631825-32,
8. Creasman WT. New gynecologic cancer staging. Obstet Gyriecol
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9. Morrow CP, Bundy BN, Kurman RJ, Creasman WT, Heller P,
Homesley HD, et al. Relationship between surgical-pathological
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