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
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U
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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.
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than
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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.
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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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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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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.
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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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