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1460

Dnternational Federation of Gynecology

and Obstetrics Staging of Endometrial

Cancer 988

John J Mikuta

M D

In 1988 he International Federation of Gynecology and

Obstetrics (FIGO)Cancer Committee changed the staging

of endometrial carcinoma from a clinical one to a surgi-

copathologic one. The emphasis in the new FIGO system

was changed to the pathologic findings in the uterus, cer-

vix, adnexa, and pelvic and/or periaortic nodes, and peri-

toneal cytologic findings. The major changes in this stag-

ing system were

1)

the use of the depth of myometrial

invasion and

2)

the identification of tumor cells in perito-

neal cytologic examination and of invasion in the retro-

peritoneal lymph nodes. Preoperative endocervical curet-

tage was no longer necessary. Currently, the high level of

operability of patients with endometrial carcinoma

makes this staging system a viable one, which will pro-

vide 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 inappropri-

ate

for

the architectural grade. In serous adenocarci-

nomas, clear cell adenocarcinomas, and squamous cell

carcinomas, nuclear grading took precedence. Adenocar-

cinomas with squamous differentiation were graded ac-

cording 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 gyne-

cologic malignancy, with an estimated 33,000 new

cases diagnosed in 1990 with

4500

deaths. Despite the

overall appearance of a favorable prognosis in this ma-

lignancy (survival rate range, 80-90 when the disease

is confined to the uterine corpus), recently, a new look

Presented at the N ational Conference o n Gynecologic Cancers,

Orlan do, Floris, April 2-4,1992.

From the University

of

Pennsylvania School of Medicine, Hospi-

tal 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 Spruc e 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 inva-

sion, cervical involvement, lymph node metastases,

and peritoneal cytologic findings. These prognostic fac-

tors were used to define a surgicopathologic staging

system for endometrial carcinoma that was adopted by

the International Federation of Gynecology and Obstet-

rics (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 de-

gree of spread of the tumor into the uterine muscle it-

self, into adjacent structures, and to distant areas. As in

any system that recently has been proposed, there are

bound to be discrepancies, inadequacies, and inconsis-

tencies 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 crite-

ria. 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 con-

fined to the corpus, and Stage I 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 exami-

nation and included the findings at the time of a diag-

nostic dilatation and curettage with endocervical curet-

tage (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 addi-

tion, the quality of anesthesia, blood availability, and

gynecologic surgeons with the expertise

to

do more

ex-

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FIGO

Staging

of

Endometrial CancerlMikuta

1461

stage 0.

Cases which the pathologist considers most likely to be of a

carcinomatous nature though it is impossible to arrive at a

defin ite 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 na ture alth ough 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

I I

growth ha s 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. I t 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 involve-

ment or spread outside the pelvis (Fig. 2).1

By 1971, it was evident that other factors were sig-

nificant in the prognosis and natural history of endo-

metrial cancer. It was emphasized repeatedly that three

parameters of virulence should be added to the stag-

ing.2 These were: the size of the uterine cavity, the lack

of differentiation of the tumor, and clinical involve-

ment of the cervix. The FIGO Committee on Cancer in

Stage

0

Histological findings suspicious of malignancy but not

proven.

Stage I.

The carcinoma is confined to t he corpus.

Stage 11.

The carcinoma has involved the corpus and the cervix.

Stage 111.

The carcinoma has extended outside the uterus but not

outsid e t he true pelvis.

Stage

IV.

The carcinoma has extended outsi de the true pelvis or has

obviou sly in volved the mucosa of t he bladder or rectun.

Figure 2. FIGO staging for endometrial cancer

1962-1971.

Stage 0,

histologic findings suggesting malignancy but n ot proved. Stage I

the carcinoma is confined to the corpus. Stage 11 the carcinoma h as

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 extend ed outside the true pelvis or ha s

involved the mucosa of the bladder or rectum obviously.

1971 changed the corpus cancer staging as follows.

Stage I was still defined as tumor confined to the cor-

pus, using clinical criteria and including fractional curet-

tage 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

0 s to the top of the interior portion of the uterus that

was less than 8cm 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 pri-

marily 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 hys-

terectomy and pelvic lym pha den e~t omy .~n 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 conven-

tional teaching of many years. Second, the treatment of

endometrial cancer for three decades consisted of preop-

erative intrauterine radium placement by various tech-

niques (e.g., tandem, Crossen, and Heyman) followed

in 6 weeks by hysterectomy and bilateral salpingo-oo-

Stage

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

The length

of

the uterine cavity is greater than

8

cm.

It is desirabl e that Stage I cases be subgrouped wit h regard tp

the histological type

of

the adenocarcinoma as follows:

G1. Highly differentiated adenomatous carcinoma.

GZ. Differ entiat ed adenomatous carcinoma with partly solid

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 th at 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.

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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 reas-

sessing 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

3. The prognostic factors have been defined suffi-

4. Pelvic and aortic nodes are of little or no conse-

defined.

ciently.

quence 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 en-

dometrial 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 find-

ings.

Recognizing the advances in information with re-

spect 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 sys-

tem 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 mu-

IVb. Distant, intra-abdominal spread, inguinal

Each case will also be graded histologically G1,

G2, G3.

cosa.

nodes.

This staging system, loosely called a surgical one, is

really a surgicopathologic one.

It

is evident that the defi-

nition 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 find-

ings. When intracavitary radiation is used, immediate

hysterectomy may show no significant histologic

changes. Again, a delay of some time between the ap-

plication and the surgery might. This new staging sys-

tem assumes that most patients will be treated by a

primary surgical approach to provide the best informa-

tion 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. Fi-

nally, it is recommended that the myometrium be mea-

sured

so

that the depth of myometrial invasion be iden-

tified in relation to the full thickness of the myome-

trium.

As mentioned earlier, with respect to the grading of

the tumor:

1. Significant nuclear atypia will increase the histo-

logic grade one step.

2. In serous papillary, adenosquamous, and clear cell

carcinomas, the nuclear grade will take preference.

3. Adenocarcinoma with squamous differentiation

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