AJR 2003; 180:765-769
© American Roentgen Ray Society
MR Imaging Findings and Patterns of Spread in Secondary Tumor Involvement of the Uterine Body and Cervix
Ur Metser1,
Masoom A. Haider1,
Korosh Khalili1 and
Scott Boerner2
1 Department of Medical Imaging, University Health Network—Mount Sinai
Hospitals, Princess Margaret Hospital, University of Toronto, 610 University
Ave., Toronto, Ontario M5G 2M9, Canada.
2 Department of Pathology, University Health Network—Mount Sinai Hospital,
Princess Margaret Hospital, University of Toronto, Toronto, Ontario M5G 2M9,
Canada.
Received May 9, 2002;
accepted after revision August 22, 2002.
Address correspondence to M. A. Haider.
Abstract
OBJECTIVE. Our study sought to describe the MR imaging features and
the patterns of spread in secondary tumor involvement of the uterus by
nonuterine tumors.
CONCLUSION. Direct extension of an adjacent tumor to the uterus is
the most common pattern of secondary tumor involvement. Concomitant invasion
of other pelvic organs is also typical. Although less common, hematogenous or
lymphatic metastases to the uterus are encountered in clinical practice.
Metastases should be added to the differential diagnosis of apparently
malignant masses in the uterine body or cervix, especially in patients with
metastatic disease or in patients whose uterus shows a preserved shape with
involvement by an infiltrative heterogeneously enhancing process.
Introduction
The most common mode of secondary tumor involvement of the uterine body or
cervix is through direct extension, most often from a colorectal or bladder
neoplasm [1]. With the
exception of the ovaries, the female genital tract is an infrequent site of
hematogenous or lymphatic metastases
[2]. When secondary tumors are
found in the female genital tract, the breast, gastrointestinal tract, ovary,
skin, and kidney are most frequently reported as the sites of primary disease
[3,
4]. Clinically, the most common
presenting symptom is vaginal bleeding
[2]. The clinical symptoms of
the metastases may precede the diagnosis of the primary tumor in up to 25% of
uterine metastases [3]. In one
series, 27% of the metastases presented clinically as possible primary
gynecologic lesions [5].
Although a few series in the pathology literature
[3,4,5,6,7,8,9,10]
describe secondary tumors in this location, the descriptions of these entities
in the imaging literature is limited to only a few case reports
[11,
12]. The purpose of our study
was to determine the MR imaging features of secondary tumor involvement of the
uterus and cervix.
Materials and Methods
Patient Population
After receiving approval from the institutional ethics review board, we
retrospectively reviewed our computerized database for MR imaging examinations
of the female pelvis performed at our institution during the period of April
2000—April 2002. Clinical and pathologic data were also obtained from
the database. Of the 529 women who underwent MR imaging examinations of the
pelvis, 21 patients (age range, 27-85 years; mean age, 62 years) were found to
have secondary tumor involvement of the uterus on MR imaging that was
histologically confirmed. Patients had been referred for staging of a known
malignancy (n = 15), for further evaluation of postmenopausal vaginal
bleeding (n = 5), or for evaluation of new-onset pelvic pain
(n = 1). For the purpose of this article, the terms "uterine
body" and "cervix" are used for those specific anatomic
parts, whereas the general term "uterus" refers to both the
uterine body and cervix.
MR Imaging Protocol
A 1.5-T MR imaging scanner (Signa EchoSpeed LX; General Electric Medical
Systems, Milwaukee, WI) was used with a phased array torso coil. Patients were
asked to fast for at least 4 hr before the imaging examination, and each
received an antiperistaltic agent, either 10 mg of
hyoscine-N-butylbromide (Buscopan; Boehringer Ingelheim, Ingelheim,
Germany) or 1 mg of glucagon intramuscularly or IV 5-30 min before imaging was
initiated. Pulse sequences performed were a coronal T1-weighted localizer, an
axial T1-weighted, an axial T2-weighted fast spin-echo, a sagittal or coronal
T2-weighted fast spin-echo with or without fat saturation, dynamic
gadolinium-enhanced fast spoiled gradient-echo (flip angle, 90°; fat
saturation at 30, 60, and 90 sec after administration of contrast material),
and coronal gadolinium-enhanced fast spoiled gradient-echo delayed
(approximately 3 min after contrast material administration) imaging. The
matrix size was 256 x 160-256 pixels. Slice thickness ranged from 4 to 8
mm. A dose of 0.1 mmol/kg body weight of gadodiamide (Omniscan; Nycomed
Amersham, Oslo, Norway) or gadopentetate dimeglumine (Magnevist; Schering,
Berlin, Germany) was delivered at a rate of 2 mL/sec for contrast enhancement.
An MR vaginogram was obtained in one patient to better delineate a cervical
mass. In this procedure, distention of the vaginal vault is achieved by
injecting saline into the vagina with a Foley catheter, thereby facilitating
assessment of the extent of tumor in the cervix.
Data Analysis
Medical records were reviewed for histologic diagnosis of tumor type and
tumor grade, as well as for other imaging tests performed for staging.
Overall, tumor grade was available for 17 of the 21 patients. Four patients
underwent hysterectomies; six patients, cervical or endometrial biopsies; and
11 patients, biopsies either of the primary tumor only (for direct tumor
invasion) or of the primary tumor and a separate pelvic mass (for local
recurrence or peritoneal deposits directly invading the uterus).
All patients underwent other forms of imaging within 60 days of the MR
imaging (range, 0-60 days; mean, 10 days). All 21 underwent chest radiography;
eight, chest CT; 19, abdominal CT; two, abdominal sonography; and two
patients, brain CT. Images from these examinations were evaluated for the
presence of lymphadenopathy or distant metastatic disease. Metastatic
lymphadenopathy was defined as lymph nodes exceeding 10 mm in the short-axis
diameter on either CT scans or MR images.
MR images were retrospectively interpreted by the consensus of two
radiologists specializing in abdominal imaging who, in keeping with the study
design, were aware of the histologic diagnoses. The radiologists determined
whether the involvement of the uterine body or cervix was contiguous or
noncontiguous. Contiguous tumor spread was defined as either direct extension
from adjacent organs or peritoneal implantation. Noncontiguous tumor spread
(e.g., hematogenous or lymphatic) was defined as a separate focus of tumor at
least 5 mm away from the primary or recurrent tumor site.
The reviewing radiologists recorded the following MR imaging features: the
shape of the uterine body (preserved or abnormal), the presence and location
of a discrete mass in the uterus (in the myometrium, endometrium, or cervix)
or evidence of a diffuse infiltrative process, the loss of T2-weighted zonal
anatomy of the uterine body or the visualization of hypointense fibrous stroma
of the cervix, and the type of enhancement pattern—homogenous or
heterogeneous. Because the enhancement of myometrium on early dynamic
contrast-enhanced MR images is often heterogeneous, focal regions of decreased
enhancement on these particular images were not considered abnormal if the
regions did not persist and if a corresponding abnormality was not seen on
T2-weighted MR images. If a mass was present, the radiologists noted whether
the mass was centered in the uterus. For the purposes of our study, fibroids
were disregarded. The original MR imaging reports were reviewed to determine
whether a prospective diagnosis of secondary tumor involvement had been
made.
Results
Thirteen (62%) of the 21 patients showed secondary uterine involvement
resulting from the direct spread of tumor. Noncontiguous spread of tumor was
found in nine patients (43%). One patient had both contiguous and
noncontiguous spread of tumor. Overall, the most common sites of the primary
tumor were the colon (55%) and the bladder (14%). In 20 (95%) of the 21
patients, multiple sites of metastatic disease—defined as the presence
of distant metastases, lymphadenopathy, or multiorgan pelvic
involvement—were found. Table
1 summarizes data for the groups of patients with noncontiguous
and contiguous spread.
Contiguous Spread
In the 13 patients with contiguous spread, primary tumors were a colorectal
adenocarcinoma (9/13), a transitional cell carcinoma of the bladder (2/13), a
granulosa cell tumor of the ovary (1/13), and a gastric adenocarcinoma (1/13).
The spread was due either to the extension of the primary tumor (11/13) or the
invasion of serosal deposits (2/13). It was noted that in three of the 13
patients, the tumor was centered in the uterus rather than in the organ of
origin. Secondary tumor involvement was suggested in the original MR imaging
report in 10 of the 13 patients.
The MR images of five of the six patients with contiguous spread of tumor
involving the cervix (either the cervix alone or both the cervix and the
uterine body) showed a partial or total loss of the hypointense signal in the
cervical stroma on T2-weighted images. Lesions involving the cervix alone were
masslike, with heterogeneous enhancement.
In eight of the nine patients with contiguous spread to the uterine body,
the shape of the uterine body was abnormal. In five of the nine patients, at
least partial loss of the junctional zone was seen. Four patients had
infiltrative lesions, whereas five had discrete masses (Fig.
1A,1B).
The enhancement pattern on delayed contrast-enhanced MR images was
heterogeneous in eight of the nine patients
(Fig. 2).
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Fig. 1A. —39-year-old woman who underwent subtotal gastrectomy for
signet-ring cell adenocarcinoma of stomach. Transverse sonogram of pelvis
shows large cauliflowerlike mass (arrows) protruding into bladder
lumen. Biopsy revealed mass to be metastatic gastric adenocarcinoma.
Contrast-enhanced CT scan (not shown) showed left ovarian mass and seeding
along peritoneal reflections between bladder and uterus.
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Fig. 1B. —39-year-old woman who underwent subtotal gastrectomy for
signet-ring cell adenocarcinoma of stomach. Axial T2-weighted MR image shows
complex, partially cystic left adnexal mass (M) consistent with Krukenberg's
tumor invading myometrium (arrowheads).
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Fig. 2. —80-year-old woman with moderately differentiated
adenocarcinoma of colon situated 20 cm from anal verge. Sagittal
contrast-enhanced T1-weighted MR image obtained for staging reveals 4.6-cm
mass (M) in sigmoid colon invading posterior body (arrowheads) of
uterus (asterisk).
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Noncontiguous Spread
In the nine patients with noncontiguous spread, the primary tumor was a
colorectal adenocarcinoma (n = 4), an ovarian adenocarcinoma
(n = 2), a lobular carcinoma of breast (n = 1), a
transitional cell carcinoma of the bladder (n = 1), or a squamous
cell carcinoma of vulva (n = 1). The prospective MR imaging reports
suggested metastatic disease for only two of the nine patients.
The cervix was involved in eight of the nine patients with noncontiguous
spread. Total or partial loss of the hypointense signal in the cervical stroma
was seen on T2-weighted MR images. A discernible cervical mass was seen in
seven of eight patients (Fig.
3A,3B).
In the remaining patient, no discernible mass was evident, but the cervix was
bulky, with abnormal foci of high and intermediate intensity signal seen on
T2-weighted MR images and with heterogeneous enhancement on contrast-enhanced
T1-weighted MR images.
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Fig. 3A. —85-year-old woman with 1-month history of postmenopausal
bleeding. Biopsy of friable growth on cervix showed adenocarcinoma of
indeterminate origin. MR imaging shows two separate abnormalities. Axial
T2-weighted MR image shows complex, partially cystic mass in left adnexa
(arrows) and polypoid mass of intermediate signal intensity
encompassing both anterior and posterior lips of cervix
(arrowheads).
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Fig. 3B. —85-year-old woman with 1-month history of postmenopausal
bleeding. Biopsy of friable growth on cervix showed adenocarcinoma of
indeterminate origin. MR imaging shows two separate abnormalities. Coronal
T2-weighted MR image more clearly delineates cervical mass
(arrowheads). Note inflated balloon of Foley catheter (B) and fluid
in vagina. Pathologic examination found well-differentiated papillary serous
adenocarcinoma of left ovary involving left fallopian tube. Cervical mass
represented metastatic deposit.
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In four of nine patients in whom the uterine body was involved, the primary
tumor was a colorectal carcinoma (n = 2), a lobular carcinoma of
breast (n = 1), or a transitional cell carcinoma of bladder
(n = 1). In all these patients, the shape of the uterine body was
preserved, but a total or partial loss of the hypointense signal in the
junctional zone on T2-weighted MR images was observed (Fig.
4A,4B).
An infiltrative tumor involving extensive portions of the myometrium or the
endometrium or both showed heterogeneous enhancement on delayed
contrast-enhanced MR images (Fig.
5A,5B,5C,5D,5E).
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Fig. 4A. —64-year-old woman who presented with hematuria. She had
undergone transurethral resection of high-grade transitional cell carcinoma of
bladder 12 months earlier, and findings at cystoscopy performed 6 months after
surgery had been normal. Recent cystoscopic findings suggested presence of
mass thought to be invading bladder from external source. Sagittal T2-weighted
image shows mass in uterine body and cervix with loss of definition of
junctional zone (arrows) and extension into upper vagina
(arrowhead). Both ovaries were also involved (not shown).
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Fig. 4B. —64-year-old woman who presented with hematuria. She had
undergone transurethral resection of high-grade transitional cell carcinoma of
bladder 12 months earlier, and findings at cystoscopy performed 6 months after
surgery had been normal. Recent cystoscopic findings suggested presence of
mass thought to be invading bladder from external source. Sagittal T1-weighted
contrast-enhanced MR image shows enlarged, heterogeneously enhancing uterine
body, cervix, and bladder wall consistent with tumor infiltration
(arrows). Endometrial involvement (arrowheads) is also seen.
Initial radiologic diagnosis was primary cervical or endometrial tumor. At
biopsy, tumor was found to be high-grade papillary urothelial carcinoma with
capillarylike space involvement by tumor.
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Fig. 5A. —47-year-old woman who presented with intermittent vaginal
bleeding. Pap smear showed malignant cells compatible with adenocarcinoma.
Contrast-enhanced CT scan of pelvis shows enlarged uterus (arrows).
Retroperitoneal lymphadenopathy and bone metastases (not shown) were also
found.
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Fig. 5B. —47-year-old woman who presented with intermittent vaginal
bleeding. Pap smear showed malignant cells compatible with adenocarcinoma.
Sagittal T2-weighted MR image shows enlarged uterus with preserved shape as
well as diffuse heterogeneous low signal of myometrium and loss of junctional
zone (arrows). Diffuse bone marrow infiltration (arrowheads)
consistent with metastases is visible.
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Fig. 5C. —47-year-old woman who presented with intermittent vaginal
bleeding. Pap smear showed malignant cells compatible with adenocarcinoma.
Axial delayed (120 sec) contrast-enhanced fat-suppressed T1-weighted MR image
of lower uterine segment and cervix shows persistent hypointense foci in
myometrium (arrowheads). Abnormal signal (arrows) in
endometrial and endocervical canals shown in B can also be seen on both
images.
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Fig. 5D. —47-year-old woman who presented with intermittent vaginal
bleeding. Pap smear showed malignant cells compatible with adenocarcinoma.
T2-weighted MR image of lower uterine segment and cervix (corresponding to
C) shows thickening of myometrium with loss of junctional zone
(arrows). Abnormal signal (arrowheads) within endometrial
and endocervical canal can also be seen.
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Fig. 5E. —47-year-old woman who presented with intermittent vaginal
bleeding. Pap smear showed malignant cells compatible with adenocarcinoma.
Photomicrograph of histopathologic specimen shows abnormal increase in
cellularity of cervical stroma and linear infiltrates of abnormal small cells
with scattered signet-ring morphology (arrow). Morphology of
malignant cells and pattern of infiltration are classic signs of metastatic
lobular carcinoma of breast. On subsequently obtained mammogram (not shown),
2-cm spiculated mass was seen adjacent to inverted nipple, consistent with
primary carcinoma of the breast. (H and E, x200)
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Discussion
Metastasis to the uterine body or cervix is an infrequent clinical event.
Although the reason for the rarity of this occurrence remains unclear, several
possible causes have been postulated, including the centrifugal drainage of
lymphatics from the uterus, the fibrous nature of cervical stroma, and the
understimation of the incidence of such metastasis due to a lack of routine
microscopic examination of the uterus at autopsy
[7,
8]. The diagnosis of contiguous
spread of tumor is often easily made because of direct visualization of the
adjacent invading tumor on MR imaging; however, noncontiguous uterine
metastases pose a more difficult diagnostic challenge.
Contiguous Spread
Our results are in agreement with those reported in the literature
[2,3,4,5]
in that we found the tumors most likely to invade the uterus locally were
colorectal and bladder neoplasms, most of which were moderately or poorly
differentiated. On MR imaging, tumors with contiguous spread to the uterus may
be either masslike or infiltrative, with involvement of the myometrium alone
or of both the myometrium and endometrium. The loss of junctional zone or
hypointense signal in the cervical stroma with the involvement of endometrium
or endocervical canal are not consistently seen because these findings are
dependent on the depth of tumor invasion. Often metachronous or synchronous
invasion of other pelvic organs, such as the bladder, is seen. We found it
interesting that in three of our 13 patients with contiguous extension of
tumor to the uterus, the tumor appeared to be centered in the uterus rather
than in the organ of origin. A tumor in this position could cause confusion in
determining the site of primary tumor.
Noncontiguous Spread
Although less common than contiguous spread, noncontiguous metastatic
disease occurred in a considerable number of our patients. The differentiation
of most of these tumors was poor or moderately poor, with the exception of two
well-differentiated ovarian tumors. The difference in differentiation may be
explained by the ability of ovarian cancers to disseminate to the uterus
through the fallopian tubes [9,
10]. On T2-weighted MR
imaging, uterine involvement displayed a partial or total loss of the
hypointense signal in the cervical stroma or myometrial junction zone,
depending on location of involvement; uterine involvement showed heterogeneous
enhancement on contrast-enhanced MR images. Concomitant metastatic disease in
other body sites was also common. If such findings are seen in a patient with
a history of malignancy, the possibility of a metastatic uterine process
should be considered.
Lesions displaying abnormal signal in a preserved uterine body on MR
imaging should receive special attention because these findings suggest
possible diffuse tumor infiltration. In our study, this pattern was
encountered in patients with noncontiguous spread of colon cancer, lobular
carcinoma of the breast, and transitional cell carcinoma of the bladder but
has also been described in patients with noncontiguous spread from other types
of tumors, including lymphoma and leukemia
[11,
13].
The relatively small number of patients and the retrospective nature of our
study are potential limitations. However uterine metastases are generally
rare, so a study with a large number of cases is difficult to arrange.
In summary, direct extension of tumor is the most common pathway for
secondary involvement of the uterus. In patients with such involvement,
concomitant invasion of other pelvic organs is common. The possibility of
noncontiguous metastatic lesions in the uterus should be recognized and
included in the differential diagnosis of uterine masses that appear to be
malignant, especially in patients with diffuse metastatic disease.
Noncontiguous metastatic involvement should also be considered in patients
with a uterus in which the normal shape is preserved but in which involvement
with a diffuse, heterogeneously enhancing infiltrative process is seen.
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Abstract
Introduction
