AJR 2000; 175:1423-1430
© American Roentgen Ray Society
Ovarian Carcinoma in Patients with Endometriosis
MR Imaging Findings
Yumiko Oishi Tanaka1,
Takeshi Yoshizako1,2,
Masato Nishida3,
Masayuki Yamaguchi1,
Kazuro Sugimura2 and
Yuji Itai1
1
Department of Radiology, Institute of Clinical Medicine, University of
Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki 305-8575, Japan.
2
Department of Radiology, Shimane Medical University, 89-1 Enya, Izumo, Shimane
693-8501, Japan.
3
Department of Obstetrics and Gynecology, Institute of Clinical Medicine,
University of Tsukuba, Tsukuba, Ibaraki 305-8575, Japan.
Received June 4, 1999;
accepted after revision April 20, 2000.
Address correspondence to Y. O. Tanaka.
Abstract
OBJECTIVE. Various types of malignancy can develop in patients with
endometriosis. Enhancing mural nodules have been reported as an imaging
characteristic of malignant transformations. We evaluated contrast-enhanced MR
imaging to determine the optimum sequence to reveal mural nodules and other
characteristics of malignant transformations.
MATERIALS AND METHODS. We examined 10 patients with pathologically
proven ovarian adenocarcinoma in endometriosis and 10 patients (the control
group) with ovarian endometrioma suggestive of malignant transformation on the
basis of sonographic findings. We analyzed the size and nature of the
endometriomas in each patient. We compared four types of contrast-enhanced MR
imaging to determine which sequence best revealed mural nodules.
RESULTS. In the malignant and control groups, 80% of the cysts with
findings suggestive of malignant transformation showed unilateral disease or
larger endometrial cysts on the suggestive side than on the contralateral
side. High signal intensity on T1-weighted images and low signal intensity on
T2-weighted images relative to the myometrium were observed only in two of 10
malignant endometrial cysts and in all control cysts. All malignant
endometriomas had small mural nodules with low signal intensity on T1-weighted
contrast-enhanced images. Only three benign endometriomas had mural nodules
and none of them enhanced. The enhancement of mural nodules was easily seen on
dynamic subtraction imaging.
CONCLUSION. On the basis of our findings, endometrial cysts with
malignant transformation rarely show low signal intensity on T2-weighted
images and usually have enhancing mural nodules. Because the enhancement of
mural nodules is often difficult to evaluate on conventional T1-weighted
images, dynamic subtraction imaging can be valuable.
Introduction
Endometriosis is a common disease that affects women of reproductive age
[1]. Although the disease is
recognized as benign, endometriosis is occasionally accompanied by malignant
ovarian tumors, especially endometrioid and clear cell adenocarcinomas
[2,3,4,5,6,7,8,9].
However, to the best of our knowledge, the imaging features of malignant
ovarian tumors have not been published in the English literature
[10,
11].
We examined 10 patients with ovarian cancer in endometriosis. We describe
the MR imaging features of ovarian cancer in endometriosis and emphasize the
use of dynamic subtraction MR imaging to diagnose this entity.
Materials and Methods
Ten patients with surgically and pathologically proven primary ovarian
adenocarcinoma in endometriomas were examined from 1992 to 1999. All patients
had cancer that satisfied the criteria for malignant change in endometriosis
according to Sampson [2]:
endometriosis and carcinoma coexisting in the same ovary; carcinoma in the
region of endometriosis that is not metastatic; and a transitional lesion
between the carcinoma focus and the endometriosis lesion. Transitional lesions
are ectopic endometrium with mild to severe atypia consecutive between the
endometrium without atypia and adenocarcinoma. Our patients were from 32 to 51
years old (mean age, 43 years) at the time of the diagnosis. Four patients
were asymptomatic, two had lower abdominal pain, two had cystitis, one had
irregular menstruation, and one had dysuria. Cancer antigen 125 antigen levels
were elevated in eight of nine patients, and cancer antigen 19-9 tumor markers
were elevated in five of nine patients. Three patients had a history of
hormone therapy for endometriosis from 1 to 3 years before MR imaging. Radical
surgery for ovarian cancer in each institute was performed within 3 weeks of
MR imaging. Endometriosis was proven in all patients. Pathologic diagnosis was
confirmed as clear cell adenocarcinoma (n = 6), endometrioid
adenocarcinoma (n = 2), and mixed adenocarcinoma (n = 2).
All carcinoma was diagnosed as ovarian carcinoma developing from
endometriosis, according to the criteria of Sampson
[2]. Pathologic stage of
ovarian cancer was stage Ia in two patients, Ic in three, IIa in one, IIc in
two, and IIIc in two.
MR imaging was performed with a Gyroscan 1.5-T superconducting magnet
(Philips, Best, The Netherlands) in five patients, a Signa 1.5-T
superconducting magnet (General Electric Medical Systems, Milwaukee, WI) in
three patients, and a 1.0-T superconducting magnet (Magnex 100; Shimadzu,
Kyoto, Japan) in two patients. Axial T1-weighted spin-echo (TR range/TE range,
320-543/11-15) and axial T2-weighted spin-echo (1200-3000/80-90) or fast
spin-echo (1836-4000/88-110) images were obtained in all patients.
Contrast-enhanced T1-weighted axial images with 5 mmol of meglumine
gadopentetate (Magnevist; Nihon-Schering, Osaka, Japan) were also obtained in
all patients. Contrast-enhanced T1-weighted MR imaging was performed with a
fat-saturation technique in three patients and a dynamic technique in four.
The slice thickness was 5-10 mm, intersection gap was 0.5-5 mm, and data were
collected with matrices of 256 x 192-256. Field-of-view measurements
were 28-40 cm, and the number of excitations was two for T1- and T2-weighted
images. T1-weighted gradientecho images (11-15/5.0-5.6; flip angle,
25-40°) were obtained every 11-14 sec after the administration of contrast
material on the Gyroscan scanner, and a fast-field-echo technique was used.
The slice thickness was 10 mm, matrix was 256 x 192, field of view was
28 cm, and number of excitations was six. Dynamic subtraction
contrast-enhanced images were synthesized in three of four patients after the
examination.
MR images were interpreted by two radiologists who reached consensus
agreement after discussing the findings. In each patient, we analyzed the
volume of each adnexal mass; nature of the mass, including the presence of
loculations; signal intensity; volume ratio of the endometrial cysts with
ovarian cancer compared with the contralateral benign endometrial cysts; size
of the mural nodules in maximum diameter; and nature of the mural nodules,
including shape, signal intensity, and contrast enhancement. Each endometrioma
was considered an oval globe, and its volume was roughly calculated using the
following equation:
Where V is volume, a is transverse diameter divided by two,
and c is height divided by two.
We noticed that endometriomas with malignant transformation were larger
than contralateral benign endometriomas. We then needed some indexes, which
would have shown the asymmetry of the ovarian endometriomas. Therefore, volume
ratio is not a common measure, although we used this index. The shape of mural
nodules was classified as nodular when the surface of the nodule was smooth
and as papillary when the surface was irregular. Signal intensity of each
nodule was compared with that of myometrium on T1-weighted images and compared
with that of outer myometrium on T2-weighted images. We determined the
presence or absence of enhancement of mural nodules by visual inspection.
During the same period, we examined 10 patients (age range, 27-50 years;
mean age, 38 years) with endometriosis and mural nodulelike structures on
sonography. Although pathologic diagnosis for endometrioma was confirmed in
only five patients, none of the remaining endometriomas grew larger during or
after the study (follow-up examinations, 3-34 months). These patients were our
control group. Patients underwent MR imaging on one of two 1.5-T
superconducting units (Signa [n = 1] or Gyroscan [n = 9])
with the same technique as that for the malignant cohort. For three patients
with mural nodulelike structures, contrast enhancement was evaluated on
dynamic contrast-enhanced and dynamic subtraction images in two patients and
on fat-saturated T1-weighted images in one patient.
We also analyzed which sequence was best for evaluating contrast
enhancement: T1-weighted images (n = 12); fat-saturated T1-weighted
images (n = 4); dynamic contrast-enhanced images (n = 6); or
dynamic subtraction contrast-enhanced images (n = 5). In one patient,
two MR examinations were available for review: dynamic contrast-enhanced
T1-weighted images were obtained 2 weeks before surgery and conventional
T1-weighted images were obtained 18 months before surgery.
Results
A summary of MR imaging features of benign and malignant endometriomas is
shown in Table 1. For all
patients with malignant endometriomas, we found one or two cystic masses in
the pelvis. Although some of these lesions could be extraovarian
endometriomas, a normal ovary was not visible on the involved side; therefore,
the lesions were presumed to be ovarian endometriomas. This assumption could
not be proven on imaging. Adnexal masses with characteristics of endometrial
cysts, including a thick capsule or adhesion to adjacent structures, were
observed bilaterally in six of 10 patients and unilaterally in four. In six
patients with bilateral endometriomas, the ovarian cancer developed
unilaterally in one of the endometrial cysts, as previously reported by
Sampson [2]. Conversely, we
found cystic masses with typical MR imaging features for bilateral ovarian
endometrioma in four patients in the control group and for unilateral ovarian
endometrioma in six. The mean diameter of the endometriomas with malignant
transformation and in the control group were 9.4 cm and 5.0 cm, respectively.
The sizes of unilateral endometrial cysts with associated cancers were larger
than those of contralateral endometrial cysts in five patients and smaller in
one patient of six with bilateral lesions (Figs.
1A,1B,1C,1D
and
2A,2B,2C,2D,2E,2F).
In the control group, the size of endometrial cysts with mural nodules on
sonography was at least five times larger than that of contralateral
endometrial cysts in two patients, the size was larger but less than five
times the size in one patient, and the size was smaller in one of four
patients with bilateral disease. On T1-weighted images, 29 of 30 endometriomas
in both groups of patients showed significantly higher signal intensity than
myometrium; the remaining endometrioma with malignant transformation showed
slightly higher signal intensity compared with that of the myometrium. For
both the ovarian cancer and control groups, the endometrial cysts were
multilocular in seven patients and unilocular in three patients. High signal
intensity on T1-weighted images and low signal intensity on T2-weighted images
relative to the myometrium were observed in only two of the 10 endometrial
cysts complicated with ovarian cancer. Conversely, all six contralateral cysts
without ovarian cancer and all 14 cysts in the control group showed high
signal intensity on T1-weighted images and low signal intensity on T2-weighted
images (Fig.
2A,2B,2C,2D,2E,2F).
One or several mural nodules were observed in all the endometrial cysts
complicated with cancer (Figs.
1A,1B,1C,1D,2A,2B,2C,2D,2E,2F,3A,3B,3C,3D,3E,3F).
None of the benign contralateral cysts had mural nodules (Figs.
1A,1B,1C,1D
and
2A,2B,2C,2D,2E,2F)
in the malignant group. In the control group, only three of 10 endometriomas
had nonenhancing mural nodules (Fig.
4A,4B,4C,4D,4E,4F).
The size of the mural nodules in the malignant cysts ranged from 2.0 to 6.5
cm; the mural nodules showed low signal intensity on T1-weighted images and
various signal intensity on T2-weighted images compared with that of
myometrium. The shapes of the mural nodules were nodular in six patients and
papillary in four patients. The nodules protruded from the cyst wall with an
acute angle in nine patients and with an obtuse angle in one. Conversely, the
mural nodularity in the control group ranged from 0.6 to 1.5 cm in size; it
showed intermediate (n = 1) and high (n = 2) signal
intensity on T1-weighted images and showed low signal intensity (n =
3) on T2-weighted images, compared with that of the myometrium. The shape of
the mural nodules was nodular and they protruded from the cyst wall with an
acute angle in two patients and an obtuse angle in one patient.
View larger version (136K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 1A. —43-year-old woman with clear cell adenocarcinoma that
developed from endometrial cyst of right ovary. Patient had history of
administration of danazol to control endometriosis. Axial spin-echo
T1-weighted MR image (TR/TE, 500/15) shows multilocular cystic mass (M) that
includes hyperintense fluid behind uterus (U). Bilateral cysts and uterus have
adhered to one another as shown by absence of fat between them.
|
|
View larger version (152K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 1B. —43-year-old woman with clear cell adenocarcinoma that
developed from endometrial cyst of right ovary. Patient had history of
administration of danazol to control endometriosis. Axial fast spin-echo
T2-weighted MR image (4000/88) shows extensive shading on left cyst (L). Note
signal loss on right cyst is limited to small area.
|
|
View larger version (105K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 1C. —43-year-old woman with clear cell adenocarcinoma that
developed from endometrial cyst of right ovary. Patient had history of
administration of danazol to control endometriosis. Axial spin-echo
T1-weighted MR image (500/15) slightly cranial to A and B
reveals small hypointense mural nodule (arrow) on wall of right cyst.
Left endometrial cyst cannot be seen at this level. Most of mural nodule shows
higher signal intensity than outer myometrium of uterus as seen on
B.
|
|
View larger version (103K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 1D. —43-year-old woman with clear cell adenocarcinoma that
developed from endometrial cyst of right ovary. Patient had history of
administration of danazol to control endometriosis. Contrast-enhanced axial
spin-echo T1-weighted MR image (500/15) shows weakly enhanced mural nodule. It
is difficult to evaluate contrast enhancement because of hyperintense fluid
surrounding mural nodule.
|
|
View larger version (114K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 2A. —42-year-old woman with clear cell adenocarcinoma that
developed in endometrial cyst of left ovary. Axial spin-echo T1-weighted MR
image (TR/TE, 442/14) reveals large multilocular hyperintense cystic mass with
mural nodule (arrow) behind uterus. Note smaller right ovarian
endometrial cyst (R) is also seen between uterus and larger endometrial
cyst.
|
|
View larger version (109K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 2B. —42-year-old woman with clear cell adenocarcinoma that
developed in endometrial cyst of left ovary. Axial fast spin-echo T2-weighted
MR image (1836/110) shows signal loss of smaller endometrial cyst (R);
however, larger cyst remains hyperintense. Mural nodule shows slight
hyperintensity compared with signal of outer myometrium of uterus (U).
|
|
View larger version (147K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 2C. —42-year-old woman with clear cell adenocarcinoma that
developed in endometrial cyst of left ovary. Unenhanced MR image (fast
gradient echo; 12/5.1; flip angle, 40°) of dynamic sequence shows mural
nodule on anterior endometrial cyst wall.
|
|
View larger version (176K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 2D. —42-year-old woman with clear cell adenocarcinoma that
developed in endometrial cyst of left ovary. Axial dynamic contrast-enhanced
MR image (fast gradient echo; 12/5.1; flip angle, 40°) obtained 92 sec
after administration of contrast material shows enhancement of uterus;
however, enhancement of mural nodule is harder to recognize
(arrow).
|
|
View larger version (100K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 2E. —42-year-old woman with clear cell adenocarcinoma that
developed in endometrial cyst of left ovary. Unenhanced dynamic subtraction MR
image synthesized from C reveals no abnormal pelvic structures or
masses with mural nodules.
|
|
View larger version (138K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 2F. —42-year-old woman with clear cell adenocarcinoma that
developed in endometrial cyst of left ovary. Axial dynamic substraction MR
image synthesized from D shows enhancement of root of mural nodule
(arrow).
|
|
View larger version (155K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 3A. —51-year-old woman with clear cell adenocarcinoma in
endometrial cyst of right ovary. Sagittal spin-echo T1-weighted MR image
(TR/TE, 500/15) obtained before diagnosis of ovarian cancer reveals unilocular
hyperintense cystic mass with mural nodule (arrow). Note smaller
endometrial cyst in left ovary on other slice level.
|
|
View larger version (148K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 3B. —51-year-old woman with clear cell adenocarcinoma in
endometrial cyst of right ovary. Contrast-enhanced sagittal spin-echo
T1-weighted MR image (500/15) reveals slight enhancement of mural nodule
(arrow). We could not conclude whether the nodule was benign or
malignant.
|
|
View larger version (147K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 3C. —51-year-old woman with clear cell adenocarcinoma in
endometrial cyst of right ovary. Sagittal spin-echo T1-weighted MR image
(408/15) obtained 18 months after A and B reveals enlarged
tumor, mural nodule, and another mural nodule (arrow) visible on
anterior wall of endometrial cyst, despite hormone therapy for
endometriosis.
|
|
View larger version (158K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 3D. —51-year-old woman with clear cell adenocarcinoma in
endometrial cyst of right ovary. Sagittal fast spin-echo T2-weighted MR image
(2076/130) does not show signal loss of endometrial cyst. Mural nodules show
lower intensity compared with signal of myometrium.
|
|
View larger version (174K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 3E. —51-year-old woman with clear cell adenocarcinoma in
endometrial cyst of right ovary. Sagittal unenhanced MR image (fast gradient
echo; 11/5.6; flip angle, 25°) of dynamic sequenceshows two hypointense
mural nodules on endometrial cyst wall.
|
|
View larger version (156K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 3F. —51-year-old woman with clear cell adenocarcinoma in
endometrial cyst of right ovary. Sagittal dynamic contrast-enhanced MR image
(fast gradient echo; 11/5.6; flip angle, 25°) obtained 99 sec after
administration of contrast material shows enhancement of mural nodule on
anterior wall of endometrioma. Enhancement of mural nodule on superior wall is
harder to recognize.
|
|
View larger version (108K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 4A. —46-year-old woman with ovarian endometrioma and mural nodule
on sonography. Sagittal spin-echo T1-weighted MR image (TR/TE, 442/14) reveals
multilocular hyperintense mass with slightly more hyperintense area
(arrow) on posteroinferior wall. This area corresponds to mural
nodule on sonography (not shown).
|
|
View larger version (152K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 4B. —46-year-old woman with ovarian endometrioma and mural nodule
on sonography. Sagittal fast spin-echo T2-weighted MR image (1836/110) shows
hyperintense mass with hypointense mural nodule (arrow).
|
|
View larger version (113K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 4C. —46-year-old woman with ovarian endometrioma and mural nodule
on sonography. Sagittal unenhanced MR image (fast gradient echo; 12/5.1; flip
angle, 40°) of dynamic sequence shows high signal intenisty similar to
that in A.
|
|
View larger version (162K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 4D. —46-year-old woman with ovarian endometrioma and mural nodule
on sonography. Sagittal dynamic contrast-enhanced MR image (fast gradient
echo; 12/5.1; flip angle, 40°) obtained 117 sec after administration of
contrast material does not reveal enhancement of mural nodule
(arrowhead).
|
|
View larger version (84K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 4E. —46-year-old woman with ovarian endometrioma and mural nodule
on sonography. Unenhanced dynamic subtraction MR image synthesized from
C shows no abnormal pelvic structures or masses with mural nodules.
|
|
The evaluation of contrast enhancement of the mural nodules in the
malignant (n = 10) and control (n = 3) groups was often
difficult because the signal intensity of the fluid surrounding the mural
nodules was similar to that of the mural nodules themselves after the
administration of contrast material (Figs.
1A,1B,1C,1D,2A,2B,2C,2D,2E,2F,3A,3B,3C,3D,3E,3F,4A,4B,4C,4D,4E,4F).
Evaluation of contrast enhancement was easy on one of 12 T1-weighted images,
on none of four fat-saturated T1-weighted images, on one of six dynamic
images, and on five of five dynamic subtraction images
(Fig. 5).
View larger version (94K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 5. —Bar chart shows difficulty in evaluation of contrast
enhancement of mural nodules with various imaging sequences. We can easily
evaluate contrast enhancement of mural nodules on five dynamic subtraction
images. Conversely, we can evaluate enhancement in only one of 12 conventional
T1-weighted images. Dynamic subtraction imaging is best for evaluating
contrast enhancement of mural nodules in endometrial cysts.
|
|
Discussion
Endometriosis is defined as the presence of endometrial tissue outside the
uterus, and it can cause extensive adhesions in the pelvis. It affects
approximately 7% of women of reproductive age in the United States, and these
patients may have abdominal pain or infertility as a result. The disease is
considered benign; however, since Sampson
[2] first reported some
patients with malignant transformation in endometriosis, pathologists and
gynecologic oncologists are aware of a malignant entity. Why endometriosis
undergoes malignant transformation remains unknown; however, some
investigators have postulated that estrogen may have a role in the development
of malignancy [4,
6]. Also implicated in the
development of premalignant transformation of endometriosis is estrogenic
stimulation, such as atypical adenomatous hyperplasia
[4]. In patients with
endometriosis who develop ovarian cancer, endometrioid adenocarcinoma is the
most commonly reported malignant tumor after clear cell adenocarcinoma, when
the primary site is the ovary
[4,
12]. Extragonadal lesions are
reported to be mostly endometrioid tumors and sarcomas
[4]. This disease is seen in
women who are 10-20 years younger than those who develop endometrial or
ovarian cancer [4]. The
incidence of malignancy in ovarian endometriosis is 0.6-1.0%
[4,
5,
13]. Conversely, the incidence
of endometriosis in patients with ovarian cancer varies from 4.2% to 14.5%
[9]. The highest incidence was
observed in Japan, which has the lowest incidence of lifetime risk for
developing ovarian cancer. This could be an explanation for the incidence of
clear cell adenocarcinoma being relatively high in Japan because clear cell
adenocarcinoma has the closest relationship to benign pelvic endometriosis
[4,
5].
We found two case reports that describe the imaging findings of malignant
transformation in extraovarian endometriosis
[10,
11]; however, cases of ovarian
cancer in endometriosis have not been published in English literature. We
found only two Japanese case reports describing ovarian cancer in
endometriosis [14,
15]. According to the
literature, the presence of mural nodules on the wall of endometrial cysts,
which are enhanced by meglumine gadopentetate, is considered key in diagnosing
the malignant transformation of endometriosis. However, it is difficult to
evaluate the contrast enhancement of mural nodules because endometrial cysts
have high signal intensity on T1-weighted images caused by the presence of
deoxyhemoglobin or methemoglobin from old hemorrhage
[16], and the mural nodules
are often very small [14,
15]. Therefore, our goal was
to describe the MR imaging features of the malignant transformation of
endometriosis and to find the most useful method to evaluate the contrast
enhancement of the mural nodules surrounded by hyperintense fluid on
T1-weighted images.
Endometrial cysts have been reported to be hyperintense on T1-weighted
images with multiplicity, a thick fibrous capsule, or adhesions to surrounding
organs [16,
17]. On T2-weighted images,
the endometrial cysts have low signal intensity. In our study, all 10 masses
with malignant transformation showed hyperintensity on T1-weighted images and
had thick walls (maximum thickness, >3 mm). However, only two of 10
endometrial cysts with malignant transformation showed low signal intensity on
T2-weighted images compared with six contralateral benign cysts. Togashi et
al. [17] reported that low
signal intensity on T2-weighted images was noted in 55 (64%) of 86 benign
endometrial cysts. The incidence of low signal intensity on T2-weighted images
in our malignant transformation group was lower (20%) than that in their
report. Additionally, all 10 masses in the control group had low signal
intensity on T2-weighted images. This intensity pattern is believed to be
caused by a magnetic susceptibility effect generated by hemosiderin in old
hemorrhage, densely concentrated fluid, or fibrosis
[16]. Because MR imaging
findings of most ovarian carcinomas were reported to be mixed solid and cystic
tumors [18], we speculate that
adenocarcinomas in endometriosis may produce some fluid. Then once malignant
transformation occurs, the fluid can dilute thick hemorrhagic fluid. This
process may be the reason why endometrial cysts with malignant transformation
seldomly show low signal intensity on T2-weighted images and tend to be large
cysts. Although the mean diameter of the endometriomas with malignant
transformation was larger than that in the control group, we could not
determine the threshold size for malignant transformation of endometrial cysts
because there was a lot of overlap between the malignant and control groups.
The size of endometriomas with malignant transformation tended to be larger
than contralateral benign cysts in the malignant group. However, in eight of
10 control patients, the endometrial cysts suggestive of malignancy were
unilateral or larger than contralateral endometrial cysts. Therefore, for
diagnosing this entity, the asymmetry of the endometriomas did not seem as
important as signal intensity on T2-weighted images.
As mentioned before, endometrial cysts tend to be multiloculated; however,
three of 10 cysts were unilocular (Fig.
3A,3B,3C,3D,3E,3F).
They had thick walls and hyperintense fluid on T1-weighted images. Prospective
diagnosis of endometriosis was difficult, especially when contralateral cysts
did not show typical features of endometriomas.
The signal intensity of the mural nodules was low on T1-weighted images in
all 10 malignant nodules; however, the signal intensity on T2-weighted images
was variable in each nodule and not related to histologic subtype. This
finding may be caused by cellularity or the degree of stromal edema rather
than histologic subtype. Also, the shape of the mural nodules was not related
to histologic subtype.
Because the maximum diameter of the mural nodules surrounded by
hyperintense fluid was smaller than 3 cm in six of 10 malignant and three
control nodules, it was difficult to evaluate whether the nodules enhanced
after the administration of meglumine gadopentetate. This difficulty was
caused by the enhancement of the uterus and other adjacent structures and the
increase in background signal intensity. We used fat-saturated T1-weighted
images, dynamic contrast images, and dynamic subtraction images to evaluate
the presence or absence of enhancement. Although contrast-enhanced MR imaging
was performed with different techniques in each patient, all the radiologists
who evaluated the MR images judged that the dynamic subtraction images were
the best to visualize the enhancement of mural nodules, followed by the
dynamic images and the fat-saturated T1-weighted images. We could not diagnose
malignant transformation in one patient (Fig.
3A,3B,3C,3D,3E,3F),
with MR images obtained 18 months before diagnosis. In that study, only
conventional T1-weighted images were obtained after the administration of
contrast material, and we could not evaluate positive enhancement of the mural
nodule. Eighteen months later, the mass was bigger and another mural nodule
appeared. At the time the patient's condition was diagnosed as malignant
transformation, peritoneal dissemination had already occurred; she died of
carcinoma 3 years after the diagnosis.
Sonography, especially transvaginal scanning, is used to identify adnexal
masses and may play a role in identifying malignant transformation. However,
although endometrial cysts are typically round and homogeneously hypoechoic
[19,
20], epithelial ovarian
carcinomas typically appear as anechoic thin-walled cysts with echogenic
endocystic vegetation [21] on
sonography. It may be as difficult to detect tiny echogenic endocystic
components. Also, it may be as difficult on sonography as on T1-weighted MR
imaging to detect enhanced mural nodules. Furthermore, blood clot or focal
fibrosis caused by recurrent hemorrhage may show focal wall nodularity on
sonography, and it is difficult for sonographers to differentiate these
findings from malignant transformation with only a B-mode scan
[20]. Doppler imaging may be
helpful in detecting malignant transformation. Endometriomas do not show
significant differences in flow indexes (resistive index and pulsatility
index) compared with other benign cystic lesions
[22]. However, once malignant
transformation occurs, it may be that the resistive and pulsatility indexes
change to show malignant patterns. However, no such findings have been
reported to date. MR imaging can provide higher specificity in diagnosing
endometriosis [17]. Therefore,
patients with indeterminate sonographic findings and in whom there is a
suspicion of endometriosis may benefit from MR imaging.
Simple endometrial cysts—benign neoplasms that develop from
endometrial cysts—and decidual change of the ectopic endometrium during
pregnancy should be considered in the differential diagnosis. In endometrial
cysts, blood clots on the cyst wall can be seen as mural nodules; however,
they do not enhance [14,
15,
23]. Adenofibroma, which can
develop in endometrial cysts, has been reported to show hypointense mural
nodules, in contrast to hyperintense endometrioid adenocarcinomas
[24]. However, we encountered
two patients with adenocarcinoma in endometrioma in whom the mural nodules
showed low signal intensity on T2-weighted images. Furthermore, adenofibroma
of the uterus has been reported to mimic endometrial carcinoma
[25]. Therefore, we speculate
that benign neoplasms in endometrial cysts cannot be distinguished from
adenocarcinoma. Decidual change of the ectopic endometrial tissue has also
been reported to mimic malignant transformation
[26]; it can also show mural
nodules on the wall of endometrial cysts and is hard to distinguish from blood
clots on MR imaging because contrast material is not used in pregnant
patients. However, in our limited experience, MR imaging characteristics of
mural nodules composed of deciduosis are slightly different from those of
malignant transformation. They tend to appear multifocal and rectangular in
shape. Nevertheless, it is necessary to investigate imaging findings of
decidualized endometrial cysts to gain a better understanding.
Unfortunately, our study has some limitations because of its retrospective
nature, small sample size, and selection bias in the control group. MR imaging
was performed with different equipment. Dynamic subtraction imaging was
performed in only five patients. The control group was composed of patients
with endometriosis and possible malignant transformation on sonography, and
pathologic confirmation of benign endometrioma was obtained in only five of 10
control patients. On the basis of our 10 patients with ovarian carcinoma in
endometriosis, we conclude that endometrial cysts with malignant
transformation rarely show low signal intensity on T2-weighted MR images. They
usually have enhancing nodules that are most clearly depicted on dynamic
subtraction imaging. We recommend performing dynamic subtraction imaging when
this uncommon entity is suspected.
Acknowledgments
We thank Hajime Tsunoda, Ken Nishide, Keiko Kohno, Sayuri Otani, and Hiroko
Shimizu-Tsunoda for recruiting patients to undergo MR imaging. We also thank
the radiologic technologists at our institute, especially Masashi Shindo, Yuji
Hirano, and Nobuyoshi Fujisawa, for their endeavors to obtain precise MR
images.
References
-
D'Hooghe TM, Hill JA. Endometriosis. In: Berek JS, Adashi EY,
Hillard PA, eds. Novak's gynecology, 12th ed.
Baltimore: Williams & Wilkins, 1996:887
-914
-
Sampson JA. Endometrial carcinoma of the ovary, arising in
endometrial tissue in that organ. Arch Surg
1925;10:1
-72[Abstract/Free Full Text]
-
Stevenson CS. Malignant transformation of ovarian endometriosis:
nature, treatment, and report of two cases. Obstet
Gynecol 1970;36:443
-457[Medline]
-
Heaps JM, Nieberg RK, Berek JS. Malignant neoplasms arising in
endometriosis. Obstet Gynecol
1990;75:1023
-1028[Medline]
-
Tohya T, Shibata S, Fujisaki S, Maeyama M. Clear cell carcinoma and
endometrioid carcinoma arising in a endometriotic cyst of the ovary.
Acta Obstet Gynaecol Jpn
1986;38:1111
-1114
-
McMeekin DS, Burger RA, Manetta A, DiSaia P, Berman ML.
Endometrioid adenocarcinoma of the ovary and its relationship to
endometriosis. Gynecol Oncol
1995;59:81
-86[Medline]
-
Chew S, Tham KF, Ratnam SS. A series of ovarian clear cell and
endometrioid carcinoma and their association with endometriosis.
Singapore Med J
1997;38:289
-291[Medline]
-
Vercellini P, Parazzini F, Bolis G, et al. Endometriosis and
ovarian cancer. Am J Obstet Gynecol
1993;169:181
-182[Medline]
-
Jimbo H, Yoshikawa H, Onda T, Yasugi T, Sakamoto A, Taketani Y.
Prevalence of ovarian endometriosis in epithelial ovarian cancer.
Int J Gynaecol Obstet
1997;59:245
-250[Medline]
-
Weinfeld RM, Johnson SC, Lucas CE, Saksouk FA. CT diagnosis of
perihepatic endometriosis complicated by malignant transformation.
Abdom Imaging
1998;23:183
-184[Medline]
-
Stringfellow JM, Hawnaur JM. CT and MRI appearances of sarcomatous
change in chronic pelvic endometriosis. Br J Radiol
1998;71:90
-93[Abstract]
-
Scully RE, Barlow JF. Mesonephroma of ovary: tumor of
Müllerian nature related to the endometrioid
carcinoma. Cancer
1967;20:1405
-1417[Medline]
-
Corner GW Jr, Hu C, Hertig AT. Ovarian carcinoma arising in
endometriosis. Am J Obstet Gynecol
1950;59:760
-774
-
Fujiwara T, Sugimura K, Yoshizako T, Imaoka I, Kitao M. MR findings
of two cases of endometrial carcinoma accompanied with endometrial cysts [in
Japanese]. Jpn J Clin Radiol
1994;39:983
-986
-
Nobusawa H, Munechika K, Kushima M, Gokan T, Ishikawa N. MR imaging
of malignant tumor arised from the wall of endometrial cysts; report of two
cases [in Japanese]. Jpn J Clin Radiol
1995;40:745
-748
-
Nishimura K, Togashi K, Itoh K, et al. Endometrial cysts of the
ovary: MR imaging. Radiology
1987;162:315
-318[Abstract/Free Full Text]
-
Togashi K, Nishimura K, Kimura I, et al. Endometrial cysts:
diagnosis with MR imaging. Radiology
1991;180:73
-78[Abstract/Free Full Text]
-
Ghossain MA, Buy JN, Ligneres C, et al. Epithelial tumors of the
ovary: comparison of MR and CT findings. Radiology
1991;181:863
-870[Abstract/Free Full Text]
-
Mais V, Guerriero S, Ajossa S, Angiolucci M, Paoletti AM, Melis GB.
The efficiency of transvaginal ultrasonography in the diagnosis of
endometrioma. Fertil Steril
1993;60:776
-780[Medline]
-
Patel MD, Feldstein VA, Chen DC, Lipson SD, Filly RA.
Endometriomas: diagnostic performance of US. Radiology
1999;210:739
-745[Abstract/Free Full Text]
-
Buy JN, Ghossain MA, Sciot C, et al. Epithelial tumors of the
ovary: CT findings and correlation with US. Radiology
1991;178:811
-818[Abstract/Free Full Text]
-
Aleem F, Pennisi J, Zeitoun K, Predanic M. The role of color
Doppler in diagnosis of endometriomas. Ultrasound Obstet
Gynecol 1995;5:51
-54[Medline]
-
Togashi K, Konishi J. Magnetic resonance imaging in the evaluation
of gynecologic malignancy. Magn Reson Q
1990;6:250
-275[Medline]
-
Matsuo Y, Doi J, Matsubayashi R, et al. Two cases of adenofibroma
accompanied with endometrial cyst [in Japanese]. In: Nakamura H, ed.
12th annual meeting of the Japanese Society for Abdominal
Radiology. Osaka, Japan: Japanese Society for Abdominal
Radiology, 1998: 59
-
Kaji Y, Sugimura K, Okizuka H. Uterine adenofibroma mimicking
endometrial carcinoma: MR findings (letter). AJR
1992;158:214[Medline]
-
Miyakoshi K, Tanaka M, Gabionza D, et al. Decidualized ovarian
endometriosis mimicking malignancy. AJR
1998;171:1625
-1626[Free Full Text]
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati What's this?
This article has been cited by other articles:
|
|
|
|
 
S. Choudhary, N. Fasih, D. Papadatos, and V. R. Surabhi
Unusual Imaging Appearances of Endometriosis
Am. J. Roentgenol.,
June 1, 2009;
192(6):
1632 - 1644.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T HIROMURA, Y O TANAKA, T NISHIOKA, M SATOH, and K TOMITA
Clear cell adenocarcinoma of the uterine cervix arising from a background of cervical endometriosis
Br. J. Radiol.,
January 1, 2009;
82(973):
e20 - e22.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S Ghattamaneni, M J Weston, and J A Spencer
Imaging in endometriosis
Imaging,
December 1, 2007;
19(4):
345 - 368.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
I. Imaoka, A. Wada, Y. Kaji, T. Hayashi, M. Hayashi, M. Matsuo, and K. Sugimura
Developing an MR Imaging Strategy for Diagnosis of Ovarian Masses
RadioGraphics,
September 1, 2006;
26(5):
1431 - 1448.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. I. Lee
Imaging Evaluation of Adnexal Masses: Self-Assessment Module
Am. J. Roentgenol.,
September 1, 2006;
187(3_Supplement):
S457 - S459.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. I. Lee
Radiological reasoning: imaging characterization of bilateral adnexal masses.
Am. J. Roentgenol.,
September 1, 2006;
187(3 Suppl):
S460 - S466.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Takeuchi, K. Matsuzaki, H. Uehara, and H. Nishitani
Malignant Transformation of Pelvic Endometriosis: MR Imaging Findings and Pathologic Correlation.
RadioGraphics,
March 1, 2006;
26(2):
407 - 417.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
I Imaoka, Y Kaji, Y Kobashi, A Wada, G Honjo, M Hayashi, M Yoshida, and M Matsuo
Cystic adenomyosis with florid glandular differentiation mimicking ovarian malignancy
Br. J. Radiol.,
June 1, 2005;
78(930):
558 - 561.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. E. Jung, J. M. Lee, S. E. Rha, J. Y. Byun, J. I. Jung, and S. T. Hahn
CT and MR Imaging of Ovarian Tumors with Emphasis on Differential Diagnosis
RadioGraphics,
November 1, 2002;
22(6):
1305 - 1325.
[Abstract]
[Full Text]
[PDF]
|
|
|
Top
Abstract
Introduction
