MR Imaging of Uterine Carcinoma : Correlation with Clinical and Pathologic 1 Harold V. Posniak, Christine M. Dudiak, James Dolan, MD John H. Isaacs, MD Vladimir Bychkov,

Thirteen

patients

were gery.

sults

mens in 1 that depth pate tients

examined

MD #{149}Mary C. Olson, MD #{149} MD #{149}MelanieJ. Castel4, MD #{149} Robert A. Wisniewski,, BS, RT. #{149} Sudarshan K. S/,arma, MD MD

with with

clinical

stages

magnetic

I and

resonance

.

II endometrial (MR)

carcinoma

imaging

before

sur-

Depth of invasion and stage of disease were assessed, and the rewere compared with those from MR images of the surgical speciand pathologic findings. Staging with MR imaging was accurate 1 of 1 3 patients (85%) Our results agree with previous reports MR imaging is an accurate, noninvasive method of assessing of myometrial invasion and cervical involvement. We anticithat MR imaging will have an increasing role in treatment of pawith endometrial carcinoma. .

U INTRODUCTION Endometnial carcinoma is the fourth most prevalent cancer in American (1) and the most common invasive malignant neoplasm of the female (2,3) The currently accepted clinical staging system for endometnial

women genital tract carcinoma is

.

based on criteria of the Cancer Committee of the Federation Internationale de Gynecologie et d’Obstetnique (FIGO) (Table 1) However, clinical staging (including that based on findings from fractional dilation and curettage) which is the basis for therapy, is inaccurate in the assessment of extent of disease in up to 5 1 % of patients (2-5) In one series (4), in 30 .4% of patients with stage I carcinoma, the disease was clinically staged inaccurately before surgery. The presence of cervical involvement and depth of myometnial invasion-factons that correlate with the prevalence of vaginal recurrence and lymph node metastases-cannot be accurately assessed clinically (2,5) Although computed tomography is helpful in identifying stage III and stage IV disease, it cannot demonstrate the degree of myometnial invasion nor accurately depict cervical involve.

,

.

.

Abbreviation: Index

FIGO

terms:

Federation

tJterine

neoplasms,

1990;

10:15-27

Internationale 854

de Gynecologie

Uterine

.32

#{149}

neoplasms,

et d’Obstetrique. MR studies,

85-I

.

I 2 14

Uterine

#{149}

neoplasms,

staging.

854.32 RadloGraphics



From

the 1988 ceivedJune CRSNA,

the

Department

RSNA annual 13. Address 1990

of Radiology, meeting. reprint

Loyola

Received requests

University

January 20, to H.V.P.

Medical 1989;

Center,

accepted

2160 and

S First

revision

Ave. requested

Maywood. March

IL 60153. 16; revision

From re-

15

ment.

that

Several

recent

magnetic

studies

resonance

have

(MR)

weighted images. An intenimage gap of 1.5 mm was used in all sequences. Four excitations were obtained for Ti -weighted images and two excitations for T2-weighted images.

indicated

imaging,

with

its excellent soft-tissue contrast, is useful in evaluating depth of myometrial invasion and in differentiating stage I from stage II disease (6-9).

We prospectively with clinical cinoma with results with

gical

examined

The

1 3 patients

stages I and II endometnial carMR imaging and correlated the those from MR images of the sun-

specimens

and with

pathologic

find-

ings.

image

matrix

was

1 28 X 256.

An injec-

iion of 1 .0 mg of glucagon was given diately before imaging. Ti -weighted images were used for ing parametnial extension and pelvic

immeevaluatnodal

involvement. T2-weighted images were essary for defining the uterine anatomy, identifying the tumor, and for assessing depth

of invasion

and

cervical

involvement.

of Endometrial

Carcinoma

necfor

MATERIALS AND METHODS Thirteen patients ranging in age from 47 to 77 years with clinical stage I or II endometniU

al carcinoma (histologically proved by means of dilation and curettage or direct cervical biopsy) underwent MR imaging preop-

enatively. and none nal

All patients was receiving

therapy.

interpreted, with

those

FIGO

studies

and

the findings

were

were

MR imaging

of surgical

I

Criterion Carcinoma is confined to uterine corpus Uterine cavity is 8 cm long Uterine cavity is > 8 cm long Carcinoma has involved corpus cervix but has not extended outside uterus Carcinoma has extended outside

compared Ia lb II

specimens and with pathologic findings (Table 2). All MR imaging studies were performed on a 1 .5-T superconducting imager (Signa; GE Medical Systems, Milwaukee) Axial Ti weighted (600-800/25 [repetition times msec/echo time msec]) images and axial and sagittal T2-weighted (2,500/70) images of the pelvis were obtained in all patients. Cononal some ings.

taging

Stage

prospectively

.

1 S

FIGO

were postmenopausal, replacement hormo-

The from

Table

III

-

uterus

Iv

IVa

T2-weighted images were obtained in patients, depending on previous findImage thickness was i cm for Ti weighted images and 3 on 5 mm for T2-

IVb

-

but

Carcinoma true pelvis involved rectum Carcinoma organs Carcinoma organs

not

outside

true

and

pelvis

has extended outside or has obviously mucosa of bladder or has spread

to adjacent

has spread

to distant

Table

2 Comparison Pathologic

of MR Imaging Stages Age (y)

Patient 1

U

RadioGraphics

U

Posniak

et a!

with

Clinical Stage

Clinical

and

MR Imaging Stage

Pathologic Stage

56 69

I

IS

IS

2

I

IS

IS

3 4

63 66

I I

IS IS

IS IS

5

71

I

ID

ID

6 7 8 9 10 11 i2 13

67 65

I I

ID ID

71

II

ID

56

II II II II I

ID II ID II IV

ID ID ID ID II II III IV

Note-S

16

Stage

67 77 47 68 =

superficial

invasion,

D

deep

invasion.

Volume

10

Number

1

Both Ti and T2-weighted images to evaluate the ovaries. T2-weighted (2,500/70) images uterine specimens were obtained coronal, and sagittal planes within -

were

used

of the in axial, 4 hours

of

surgery. U

IMAGE

ANALYSIS

. Normal Anatomy On T2-weighted images,

several

distinct

uterine zones are visible ( 1 0) A central high-signal-intensity zone corresponds to the endometnium. The peripheral medium-intensity area corresponds to the myometnium. A low-intensity zone of demarcation between the endometnium and myometnium, termed the junctional zone, is seen in 40%-60% of patients (6,iO,i i). The appearance of the normal endometniurn is influenced by hormonal stimuli. In .

women urn

of reproductive

is thickest

age,

during

the

the endornetni-

secretory

phase.

In

postmenopausal women receiving exogenous estrogen, the endornetriurn has a sirnilan appearance. In women using oral contraceptives and in postmenopausal women, the endometnium is atrophic (1 2) The endometrium measures less than 3 mm in width in postmenopausal women not receiving hon. monal therapy (6). .

The

normal

cervix

has a lower

signal

inten-

sity than that of the myometrium, while the endocervical canal has a signal intensity similar to that of the endometnium ( 1 0) The normal ovaries, not routinely seen in all patients, are isointense relative to the uterus on Ti -weighted images and become hypenintense relative to fat on T2-weighted images (i 3). .

. Endometrial On T2-weighted

Carcinoma images, the endometnial

Stage I (Figs 1-5).-In the FIGO system, this stage is subdivided into Ia and lb on the basis of uterine size. However, size has been shown to be an unreliable prognostic sign, since enlargement may be due to unrelated causes such as leiomyomata and adenomyosis. In one report (14), carcinoma ofthe endometnium was the cause of uterine enlargement in only i 5% of patients with endometrial carcinoma. Of more prognostic importance is differentiation between superficial and deep invasion. For the purpose of this study, superficial invasion was defined as tumors confined to the endometnium or involvement of the inner one-half of the myometnium. Extension of tumor into the outer one-half of the myometrium was interpreted as deep invasion. In patients with a visible junctional zone, an intact zone mdi-

cated

tumor

confined

to the endometnium.

Segmental disruption of the junctional zone indicated invasion. In the absence of a junctional zone, invasion was defined as irregulanity of the endometnium-myometnium interface. Stage II (Fig 6).-The cervix can be involved by direct extension of tumor from the endometnial cavity, which causes the cervical canal to widen. There may also be dis-

crete 7,

masses

in the cervical

stroma

(Figs

8).

Stage

III (Figs

7, 8).-Tumor

into the parametnia, discrete ian masses, or lymphadenopathy seen. Stage

IV (Figs

manifestations tes, peritoneal volvement.

infiltration

adnexal

or ovar-

may

be

9, 1O).-Within the pelvis, of stage IVb disease are asciimplants, and omental in-

cavity was widened in all our patients. We defined abnormal widening as being greater than 3 mm, because all our patients were postmenopausal and were not receiving estrogen replacement therapy. In patients with the smallest or most superficial lesions, the

carcinoma could not be differentiated from the normal endometnium. The larger lesions all had signal intensity lower than that of the endometnium myometnium.

January

but

1990

higher

than

that

of the

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17

a.

b.

c.

d.

Figure 1. Patient 1. Clinical stage I, MR imaging stage I superficial, pathologic stage I superficial. (a) Sagittal MR image demonstrates slight widening of the endometrium (short arrow) in the region of the fundus. There is no evidence of deep myometrial invasion or cervical involvement. Long arrow cervical canal. Curved arrow normal-sized endometrial cavity. B bladder. (b) Sagittal MR image of specimen demonstrates a small tumor in the fundus (open arrow) Short arrow incidental endometnial polyp. Curved arrow normal endometrium. (c) Midline sagittal section of the uterus reveals thickened endometnium representing tumor (long arrows) A benign endometrial polyp is noted at the fundus (short arrow). (d) Whole-mount sagittal section of the uterus, 1 cm lateral to the midline, reveals superficially invasive adenocarcinoma with extension to a maximum myometnial depth of 3 mm (arrows). .

.

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d. Figure 2. Patient 2. Clinical stage I, MR imaging stage I superficial, pathologic stage I superficial. Sagittal (a) and axial (b) MR images reveal an intact junctional zone (arrows) with widened endometrial cavity (a) There is no evidence of deep myometrial invasion. B bladder. (c) Coronal section of the uterus reveals the tumor near the fundal aspect of an asymmetrically distended endometrial cavity (straight arrows). Myometrial invasion is superficial (curved arrow). (d) Transmural section of the uterus in the region of maximum tumor involvement reveals infiltration to a depth of 4 mm (arrows). C-

.

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a.

b.

Figure 3- Patient 5. Clinical stage I, MR imaging stage I deep, pathologic stage I deep. (a) Axial MR image demonstrates large tumor (*) distending the endometrial canal. Arrowhead incidental leiomyoma. (b) Coronal MR image shows endometrial tumor (*) with disruption of the junctional zone (straight arrows) and deep myometrial invasion (open arrow). (c) Coronal MR image of specimen demonstrates deep invasion of tumor (*). Arrowheads = leiomyomata. (d) Coronal section of the uterus reveals a large fungating tumor (*) distending and distorting the endometrial cavity. Deep myometnial invasion is evident (open arrows). Arrowheads = leiomyomata.

20

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10

Number

1

d.

C.

Figure 4. Patient 6. Clinical stage I, MR imaging stage I deep, pathologic stage I deep. (a) Sagittal MR image shows widened endometrial cavity (*) and deep myometrial invasion anteriorly (curved arrow). Note low-signal endometrial polyp (straight arrow). B = bladder. (b) Transaxial MR image reveals deep myometrial invasion (arrow) along right lateral aspect of the uterine fundus. Right ovarian mass (0) has signal intensity similar to that of the bladder in a, consistent with a cyst. * = widened endometrial cavity. (C) Sagittal MR image of specimen shows deep anterior myometrial invasion (curved arrow), widened endometrial cavity (*), and endometrial polyp (straight arrow) . (d) Coronal section of the uterus reveals a large tumor (*) obliterating the fundal aspect of the endometrial cavity, with deep myometnial invasion in the area of the right uterine horn (open arrow). Arrows = benign endometnial polyp. (e) Transmural section of the uterus from the area of the right uterine horn reveals endometrial carcinoma (*) infiltrating deeply into the myometrium (arrows). Arrowheads = serosal surface.

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Figure 5. Patient ing stage I deep,

8. Clinical stage II, MR imagpathologic stage I deep. Sagittal (a) and coronal (b) MR images demonstrate endometnial widening (*) due to tumor with extension into the outer one-half of the anterior myometrium (short arrows) . Note distended cervical canal of higher intensity than that of the tumor (long arrow in a), compatible with blood clot. Curved arrow in a = incidental Nabothian cyst. (C) Axial MR image of specimen, opened following surgery, demonstrates deep invasion of tumor (arrows). (d) Axial section of the uterus reveals tumor infiltrating deeply into the myometrium (arrows). (e) Transmural section of the anterolateral uterine wall reveals deep tumor invasion (arrows).

e.

22

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10

Number

1

a. b. Figure 6. Patient 10. Clinical stage II, MR imaging stage II, pathologic stage II. (a) Sagittal MR image demonstrates the tumor-distended endometrial cavity with intact junctional zone (straight arrows). Cervical canal (curved arrow) is enlarged due to tumor extension. (b) Cervical biopsy specimen reveals involvement by infiltrating adenocarcinoma of endometnial origin (long arrows). Fragment of normal squamous cervical mucosa remains intact (short arrows). (No resected specimen was available, since the hysterectomy was performed at another institution.)

S

i

a.

D.

Figure 7. Patient 12. Clinical stage II, MR imaging stage II, pathologic stage III. The primary tumor was in the uterine fundus, and there were metastases to the cervix and left ovary. (a) Axial MR image demonstrates extension of tumor ( T) from the fundus into the inner one-half of the myometrium,

a finding

indicating

superficial

in-

vasion. (b) Axial MR image shows no evidence of invasion of tumor in the uterine isthmus (*) . The left ovary (0) has relatively high intensity but less than that of the bladder in C. This finding is compatible with a metastatic lesion and was not appreciated prospectively. (C) Axial MR image reveals tumor mass involving most of the cervical stroma (curved arrow). B = bladder.

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-

,(

,,

4

#{163} .

-*

a.

;,*

b.

d. Figure 8. Patient 12. (a) Coronal MR image of specimen shows superficial invasion in the fundus (*), cervical mass (arrow) , and ovarian metastasis (0) . (b) Coronal section of the uterus reveals tumor filling the fundal portion of the endometrial cavity (*) , with superficial myometrial invasion (solid arrow) . The uterine isthmus is free of tumor (open arrow). (C) Another section shows the cervix distorted by tumor (*), with deep stromal invasion (arrows). (d) Bivalved left ovary reveals replacement by metastasis (*). C.

24

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10

Number

1

Figure

Clinical stage I, MR imagstage IV. Axial (a), coronal (b), and sagittal (C) MR images show a large endometrial tumor (T) distending the endometnial cavity and invading the outer one-half of the myometnium (straight arrow). Cervical canal is distended by high-signal-intensity blood clot (open arrow in C). There are numerous peritoneal metastases (curved arrows) and ascites (A). B = bladder. ing

stage

9. Patient

13.

IV, pathologic

C.

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.,,

,

.

a. Figure 10. Patient 13. (a) Coronal MR image of specimen shows large tumor ( T) with deep myometnial invasion (straight arrows) . Curved arrow = blood clot. (b) Coronal section of the uterus reveals a large tumor (*) distending the endometrial cavity, with deep myometrial invasion (straight arrows). Curved solid arrow = inferior extent of tumor. Open arrow = blood clot in the cervical canal. (C) Another section shows peritoneal metastases (arrows) involving uterine serosa.

C.

U RESULTS Clinical staging patients (69%)

was

accurate

in nine

of i 3

. In two patients, the disease was undenstaged. Patient i 2 (Figs 7, 8) had clinical stage II disease and pathologic stage

III disease, and patient 1 3 (Figs 9, i 0) had clinical stage I disease and pathologic stage IV disease. In two patients (patients 8 and 9), the cancer was clinically overstaged. These patients had stage II disease based on fractional dilation and curettage results and pathologic stage I disease at the time of sur-

gery.

26

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Staging with MR imaging was accurate in i i of 1 3 patients (85%) . Nine patients had pathologic stage I disease. In all nine, the disease was correctly staged at MR imaging. Two patients had pathologic stage II disease. In one of them, the cancer was incorrectly assessed as stage I on MR images. Even in retrospect, no cervical involvement was evident on the MR images. Patient 1 2 (Figs 7, 8),

who

had pathologic

moderately T2-weighted terpreted

stage

high-intensity images. This preoperatively.

Volume

III disease, ovarian finding She also

10

had

a

mass on was misinhad a mass

Number

1

in the cervical stroma, which was correctly diagnosed on MR images. In patient 1 3 (Figs 9, 1 0) , who had pathologic stage IV disease, ascites

and

penitoneal

implants

were

MR images and were correctly MR imaging findings allowed dictions

of the

tients

before

depth

of invasion

has been

shown

in staging documented ma and also provides

accurate

5.

pre-

in all pa-

on the FIGO with surgical

definition

system staging.

is

MR imaging

will

of the depth

have

7.

to be accurate

endometnial carcinounique information for

an important

REFERENCES Cancer facts and figures, 1989. American Cancer Society, 1989. 2. Berman ML, Ballon SC, Lagasse WG. Prognosis and treatment al cancer. AmJ Obstet Gynecol

York:

LD, Watring of endometri1980; 136:

1986;

159:725-730.

1986;

10.

DM,

Lee

MR imaging.

JKT, et al. Radiology

93:353-360.

175-179. 1 1.

13.

U

New

neoplasms:

Fishman-Javitt MC, Stein HL, LovecchioJL. MM in staging of endometrial and cervical carcinoma. Magn Reson Imaging 1987; 5:83-92. LeeJKT, Gersell DJ, Balfe DM, Worthington JL, Picus D, Gapp G. The uterus: in vitro MR-anatomic correlation of normal and abnormal specimens. Radiology 1985; 157:

12.

1.

Uterine

9.

on

We thank Barbara Medley in the preparation of this manu-

1987; 162:297-305. WorthingtonJL, Balfe

Powell MC, Womack C, BuckleyJ, Worthington BS, Symonds EM. Pre-operative magnetic resonance imaging of stage I endometnial adenocarcinoma. BrJ Obstet Gynaecol

treatment.

ACknowledgment: for her assistance script.

30:147-169.

Hricak H, SternJL, Fisher MR, Shapeero LG, Winkler ML, Lacey CG. Endometrial carcinoma staging by MR imaging. Radiology

8.

of invasion.

affect

Cowles TA, Magnina JF, Masterson BJ, Capen CV. Comparison of clinical and surgical staging in patients with endometnial carcinoma. Obstet Gynecol 1985; 66:413-416. Jones HW. Treatment of adenocarcinoma of the endometrium. Obstet Gynecol Surv 1975;

6.

Previous reports have indicated that MR imaging is up to 97% accurate in the differentiation between deep myometnial invasion and superficial myometnial invasion or tumor confined to the endometnium (6) . Our accuracy with MR imaging in a relatively small number of patients was i 00%, a fact that supports the findings of previous studies. Because it enables accurate staging of early endometnial carcinoma and accurate assessment of depth of invasion, we anticipate that patient

.

on

surgery.

U CONCLUSIONS Clinical staging based suboptimal compared

MR imaging

seen

interpreted. accurate

4

14.

Bryan PJ, Butler HE, LiPumaJP, scanning of the pelvis: initial

et al. NMR experience

withao.3Tsystem.AJR 1983; 141:11111118. HeikenJP, Lee JKT. MR imaging of the pelvis. Radiology 1988; 166:11-16.

Mitchell DG, Mintz MC, Spritzer CE, et al. Adnexal masses: MR imaging observations at 1.5 T, with US and CT correlation. Radiology 1987; 162:319-324. Javert C, Douglas R. Treatment of endometrial adenocarcinoma. AJR 1956; 75:508514.

679-688.

3.

Boronow RC, Morrow CP, Creasman WT, et al. Surgical staging in endometrial cancer: clinical-pathologic findings of a prospective study. Obstet Gynecol 1984; 63:825-832.

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MR imaging of uterine carcinoma: correlation with clinical and pathologic findings.

Thirteen patients with clinical stages I and II endometrial carcinoma were examined with magnetic resonance (MR) imaging before surgery. Depth of inva...
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