Acta Radiologica

ISSN: 0284-1851 (Print) 1600-0455 (Online) Journal homepage: http://www.tandfonline.com/loi/iard20

Characterization of Sonographically Indeterminate

Ovarian Tumors with MR Imaging

Yasuyuki Yamashita, Y. Hatanaka, M. Torashima, M. Takahashi, K. Miyazaki &

H. Okamura

To cite this article: Yasuyuki Yamashita, Y. Hatanaka, M. Torashima, M. Takahashi, K. Miyazaki

& H. Okamura (1997) Characterization of Sonographically Indeterminate Ovarian Tumors with MR
Imaging, Acta Radiologica, 38:4, 572-577

To link to this article: http://dx.doi.org/10.1080/02841859709174389

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Acta Rudiologicu 38 (1997)572-577 Copyright 0 Acta Radiologica 1997
Printed in Denmark . All rights reserved
A CTA R A D I O L O G I C A
ISSN 0284-1851

CHARACTERIZATION OF SONOGRAPHICALLY
INDETERMINATE OVARIAN TUMORS WITH MR IMAGING

A logistic regression analysis

Y. YAMASHITA~,
Y. HATANAKA', M. TAKA HAS HI^, K. MIYAZAKI~
M. TORASHIMA', and H. OKAMURA'
Departments of 'Radiology and 'Obstetrics and Gynecology, Kumamoto University School of Medicine, Kumamoto, Japan.

Abstract
Purpose: The goal of this study was to maximize the discrimination between Key words: Ovarian neoplasm, MR im-
benign and malignant masses in patients with sonographically indeterminate ovarian aging; tissue characterization, computer-
lesions by means of unenhanced and contrast-enhanced MR imaging, and to develop a assisted diagnosis.
computer-assisted diagnosis system.
Material and Methods: Findings in precontrast and Gd-DTPA contrast-enhanced Correspondence: Yasuyuki Yamashita,
MR images of 104 patients with 115 sonographically indeterminate ovarian masses Department of Radiology,
were analyzed, and the results were correlated with histopathological findings. Of 115 Kumamoto University School of
lesions, 65 were benign (23 cystadenomas, 13 complex cysts, 11 teratomas, 6 fibro- Medicine, 1-1-1 Honjo,
thecomas, 12 others) and 50 were malignant (32 ovarian carcinomas, 7 metastatic Kumamoto 860, Japan.
tumors of the ovary, 4 carcinomas of the fallopian tubes, 7 others). A logistic regres- FAX +81 96 362 4330.
sion analysis was performed to discriminate between benign and malignant lesions,
and a model of a computer-assisted diagnosis was developed. This model was pro- Accepted for publication 2 December
spectively tested in 75 cases of ovarian tumors found at other institutions. 1996.
Results: From the univariate analysis, the following parameters were selected as sig-
nificant for predicting malignancy (p10.05):a solid or cystic mass with a large solid
component or wall thickness greater thgn 3 mm; complex internal architecture; ascites;
and bilaterality. Based on these parameters, a model of a computer-assisted diagnosis
system was developed with the logistic regression analysis. To distinguish benign from
malignant lesions, the maximum cut-off point was obtained between 0.47 and 0.51. In
a prospective application of this model, 87% of the lesions were accurately identified
as benign or malignant.
Conclusion: Benign and malignant ovarian lesions can be distinguished in most
sonographically indeterminate lesions by means of parameters obtained from contrast-
I enhanced MR imaging.

The detection and characterization of an ovarian
mass is a continuing clinical and radiological chal-
lenge. The imaging characteristics of ovarian
masses do not always permit the differentiation of
malignant lesions from benign lesions. Although ul-
trasonography remains the foremost imaging mo-
dality for screening patients with adnexal lesions,
MR imaging may be of great help in identifying ma-
lignancy before surgery (8-10, 16, 17). However,
the cost of MR is high so it should be used to help
characterize a mass mainly when a sonogram is sub-
optimal or indeterminate (11, 14). MR imaging can
reliably diagnose fat-containing cystic teratoma and
endometrioma, which are often problematical in ul-
trasound. However, the characterization of some
epithelial or stromal ovarian lesions is occasionally
difficult. In order to differentiate these diagnosti-
cally indeterminate lesions, various trials have been
performed with morphological characteristics (6,
12) or flow analysis using color Doppler (4, 5, 18).

572
 MR IMAGING OF OVARIAN TUMORS

Table 1 made on the sonographic appearance of one of the

Pathological diagnosis following findings (7, 13): a) a predominantly solid
mass adjacent to pelvic organs with extension to the
Lesions. n
pelvic sidewalls; b) the presence of peritoneal, me-
Benign lesions, n=65
senteric, or omental disease; c) metastasis; d) large
Complex cyst of the ovary including ovarian torsion 13
Cystadenoma of the ovary lymph node swelling. Lesions were diagnosed as
Serous cystadenoma 11 benign when 3 of the following 4 criteria were met
Mucinous cystadenoma 11 (7, 13): a) lesion size less than or equal to 4 cm in
Cystadenofibroma 1 the largest diameter; b) entirely cystic; c) lesion wall
Mature cystic teratoma of the ovary 11 less than 3 mm thick; d) lack of internal structure.
Fibrothecoma of the ovary 6
Endometrioma of the ovary 4
The interval between ultrasound and MR imag-
Tubo-ovarian abscess 3 ing was within 3 weeks. All patients underwent sur-
Ovarian hemorrhage 2 gery or laparoscopy, and a pathological diagnosis
Hydrosalpinx 2 was made within one month of MR imaging. At
Struma ovarii 1 pathological examination, 65 masses were found to
Malignant lesions, n 4 0
Ovarian carcinoma be benign, 10 to be of low malignant potential
Serous cystadenocarcinoma 9 (LMP), and 40 to be malignant. The pathological di-
Mucinous cystadenocarcinoma 13 agnoses of the lesions included in this study are
Mixed endometrioid and clear-cell carcinoma 2 listed in Table 1. LMP was regarded as malignant in
Serous papillary adenocarcinoma 2 this analysis. Tumors were unilateral in 79 patients
Undifferentiated carcinoma 2
Endometrioid carcinoma 3
and bilateral in 25. The mean sizes of the tumors
Adenofibroma of low potential malignancy 1 were 9.6 cm for benign lesions and 11.O cm for ma-
Granulosa cell tumor of the ovary 2 lignant lesions. Ascites was seen in 6 patients with
Unclassified ovarian tumor 2 benign lesions and in 33 patients with malignant le-
Metastatic tumors of the ovary 7 sions. Peritoneal dissemination was found in 11 pa-
Mixed miillerian tumor of the ovary 1
Liposarcoma of the ovary 1
tients with malignant tumors.
Dysgerminoma of the ovary 1 MR imaging was performed with two 1.5 T su-
Carcinoma of the fallopian tube 4 perconductive units (Magnetom H15 and Magne-
Total 115 tom Vision, Siemens). With the Magnetom H15
unit, T1-weighted spin-echo (SE) images were ob-
tained with a repetition time (TR) of 600 ms, an
However, there is still considerable overlapping be- echo-time (TE) of 15 ms, a 256x192 matrix, and 2
tween benign and malignant lesions (1). excitations. T2-weighted SE images were obtained
To determine the most significant parameters for with TR/TE 2000/80 ms, 256x256 matrix, and one
differentiating the sonographically indeterminate le- excitation. The body coil was used for data acquisi-
sions referred to MR imaging, we performed a mul- tion. With the Magnetom Vision unit, TI-weighted
tivariate analysis and established a computer- SE images were obtained with TR/TE 600/14 ms, a
assisted diagnosis model for distinguishing malig- 292x5 12 acquisition matrix, and one excitation. T2-
nant from benign masses. weighted turbo SE imaging was performed in an ax-

Material and Methods

Table 2
The cases were reviewed of 104 women and girls
(aged 13-83 years; mean 45.5 years) with 115 histo- Results of univariate analysis
logically proven ovarian masses and who had been Parameters Probability
examined by means of both precontrast and Gd-en- Solid vs cystic <0.01
hanced MR imaging. All patients were referred for Septum (none or thin vs thick) 0.25
MR imaging because the transvaginal sonographic Ascites (present vs absent) <0.01
findings were considered indeterminate as to the le- Unilateral vs bilateral (0.01
sions being benign or malignant because a definitive Necrosis (present or absent) 0.01
Internal structure (complex or simple) 0.08
diagnosis of malignancy or benignity could not be Wall structure (thin or thick or papillaritic) <0.01
made with ultrasound. The majority of endometrio- Signal intensity on T1-weighted SE 0.59
mas and mature cystic teratomas were diagnosed as (high vs iso-low relative to uterus)
benign by ultrasound and were not included in this Signal intensity on T2-weighted SE 0.35
analysis. A definitive diagnosis of malignancy was (high vs iso-low relative to uterus)

573

Table 3
Results of logistic regression analysis
Variable Regression SD
coefficient
C: intercept -2.70 0.80
b,: size 0.04 0.03
b,: ascites 1.76 0.81
b,: bilaterality 1.38 0.72
b4:complex internal architecture 0.48 0.52
b,: solid or irregular wall structure 1.60 0.62
R=0.5508,variance 0.303
Formula for predicting malignancy is calculated as follows: If y is the
probability of malignancy, the equation is logit (y)=-2.7+
0.04x,+1.8x,+1.4x,+0.5x4+1.6x5, where x, is tumor size (cm), x2-x5 is
1 (present) or 0 (absent).
If y is solved, the expression that results (possibility of malignancy) is:
y=l/[l+e -(-2.7+0.O4x ,+1.8x2+1.4x3+O.5x,+1.6x5)]
ial plane with TR of 4500 ms, an effective TE of
120 ms, and a 15-echo train with a 128x512 acquisi-
tion matrix, and 2 excitations. Immediately after in-
jection of Gd-DTPA, postcontrast T1-weighted SE
images were obtained with the same imaging tech-
nique as the precontrast study. Gd-DTPA was given
intravenously at a dose of 0.1 mmovkg b.w., lasting
1-2 min. Images were obtained in the axial andor
coronal planes with a section thickness of 5 or 7 mm
with 10-20% interslice gap. Fat-saturation images
were used in the Magnetom Vision unit.
MR images obtained in each patient were inter-
preted independently by 3 radiologists. Surgical and
pathological reports were not available. Both pre-
contrast T1-weighted, TZweighted, and postcon-
trast MR images were evaluated. Each reader evalu-
ated the lesion for: 1) size of the lesion; 2) bilateral-
ity; 3) wall structure (cystic with smooth thin,
<3mm, wall vs cystic with thick irregular wall or
-
solid wall); 4) internal architecture (heterogeneous
vs homogeneous); 5) presence of thick (>3 mm)
septa; 6) signal intensity of the mass relative to the
uterine myometrium; 7) massive ascites. Any peri-
toneal or pelvic extension or lymph node swelling
was also recorded.
Statistics: To obtain a logistic regression model,
two procedures were performed. First, a univariate
analysis was made of each histological factor by
means of 2x2 contingency table analysis. The p -
value was obtained by computing the exact binomial
probability. Second, using the variables identified as
significant from this analysis, we performed a logis-
tic regression analysis as described below.
In a variety of typical biomedical applications, it
has proved useful to assume that the probability of
574
Y. YAMASHITA ET AL.
being in one group, for instance the malignant
group, is of the form l/(l+e-"), where x is a linear
combination of the predictors. The probability of
Probability
being in the benign group is then 1-1/( l+e-"). In this
form, x is referred to as the log-odds of being in the
<0.01
0.24 first group (2,3). In our particular application, x was
0.03 taken as a linear combination of subjective indica-
0.06 tors: x=C+b,x,+b,x,+ --- bnxn,where C and b, ___
0.35 are the constant and logistic regression coefficients.
0.01
x1___ stands for a particular diagnostic feature (e.g.
x=l if a finding is present, x=O if a finding is ab-
sent). The constant C and coefficient b, ... are com-
puted so that the likelihood of the data, as it was ac-
tually observed, is a maximum. The number of vari-
ables used for the logistic regression analysis was
limited to 5, with the step-down stepwise procedure
used to avoid confusion. Tumor size was used as a
linear variable. With each C and b, _.. used for a
specific tumor type, a model of predicting likeli-
hood of malignancy can be obtained. By giving 0 (if
absent) or 1 (if present) on the basis of the visual
analysis of MR images, one can calculate the likeli-
hood of malignancy.
This computer-assisted diagnosis system was ap-
plied to MR images of 75 ovarian lesions found at
other hospitals during the same period, and the effi-
cacy of the model was tested for both definite and
indeterminate lesions.
Results
Univariate analysis yielded the following primary
criteria of malignancy at a p-value of 50.05: a) a
cystic mass with wall thickness greater than 3 mm or
predominantly solid mass; b) heterogeneous internal
Fig. 1. Mucinous cystadenoma in the left ovary of a woman
aged 65 years, visualized with a body coil. a) Precontrast T1-
weighted SE (600/15) and b) T2-weighted SE image (2000/80)
images show a multiloculated cystic mass. The signal intensity
of the cystic fluid differs between the 2 cavities. The wall and
septum are thin. The solid portion was not seen on the postcon-
trast study. If y is the probability of malignancy, the equation is
logit (y)=-2.7+0.04xl+1.8x,+1 .4x3+0.5x,+1.6x,. In this case,
x1=14 (size), x,=O (massive ascites absent), x3=0 (unilateral),
x,=O (homogeneous internal architecture), x,=O (thin wall) is
given. The estimated probability of malignancy is 10%.
 MR IMAGING OF OVARIAN TUMORS

Fig. 2. Serous ovarian cancer in the left ovary of a woman aged 51 years, visualized with a phased-array coil. a) T1-weighted SE
(600/14), b) T2-weighted turbo SE (4500/120/15 ETL) and c) postcontrast T1-weighted (600/14) images show a mass composed of a
solid and a cystic component. Ascites is not present. In this case, x,=18 (size), x,=O (massive ascites absent), x,=O (unilateral), x,=l
(heterogeneous internal architecture), and x,=l (solid) is given. The estimated probability of malignancy is 53%.

Fig. 3. Struma ovarii in the right ovary of a woman aged-58years, visualized with a phased-array coil. a) T1-weighted SE (600/14), b)
T2-weighted turbo SE (4500/120/15 ETL) and c) postcontrast T1-weighted (600/14) images show a predominantly cystic mass. The
wall of the cyst is thick and irregular. In this case, xl=8 (size), x,=O (ascites absent), x,=O (bilateral), x,=O (no internal architecture),
x,=l (wall with nodules). The estimated probability of malignancy is 31%.

Fig. 4.Fibroma associated with a simple cyst in the left ovary of a woman aged 37 years, visualized with a body coil. a) Precontrast
(600/15), b) T2-weighted TSE (2000/80) and c) postcontrast T1-weighted SE (600/15) images show a solid and cystic mass in the left
adnexa. In the solid mass, the signals in the T1-weighted and T2-weighted images are both hypointense, indicating a fibrous tumor. In
this case, x1=15(size), x,=O (ascites absent), x,=O (bilateral), x,=O (no internal architecture), x,=l (wall with nodules). The estimated
probability of malignancy is 38%.

architecture; c) presence of tumor necrosis; d) mas-
sive ascites; and e) bilaterality (Table 2). Thick sep-
tum and signal intensity in either TI- or T2-weighted
images had less significant predictive values.
The results of the logistic regression analysis are
shown in Table 3. The most significant finding for
malignancy was massive ascites, followed by wall
structure and internal architecture. Size and bilater-
ality had little value. From the data obtained from
the logistic regression analysis, a model of compu-
ter-assisted diagnosis was developed. By giving 0 or
1 in xl,x2, --- x5,depending on the presence or ab-
sence of findings, the predicted likelihood of malig-
nancy was calculated for the individual tumor. If y is
the probability of malignancy, the equation is logit
(y)= -2.7+0.04x1+1.8x2+1.4x3+0.5x4+1.6x5.For

575
 Y. YAMASHITA ET AL.
0.7-
0.6-
0.5-
0.4-
0.3-
0.2-
0.1 -
0' I sions, and is found to be useful in differentiation be-
5 10 15 20 25
Tumor diameter (cm)
Fig. 5. If y is the probability of malignancy, the equation is logit
(y)=-2.7+0.04x ,+1.8x2+1.4x,+0.5x,+1.6x,. For each of the val-
ues of x2 (massive ascites), x3 (bilaterality), x, (internal archi-
tecture), x5 (thick wall or solid), a regression curve can be
drawn for logit (y) versus size (x,). The figure illustrates esti-
mated probability of malignancy as a function of size and se-
lected values of (x2,x3. x,, x5).
each of the values of xl, x2, x3, x4, x5; a regression
curve can be drawn for logit (y) versus size. For ex-
ample, corresponding to x2=0 (massive ascites ab-
seht), x3=0(unilateral),x4=1 (heterogeneousinternal
architecture), x5=0 (thin wall), the equation is logit
(y)= -2.2+0.04x1. Therefore the curve y= l/(l+e -
[2.2+0.04x]) as a function of tumor size is obtained.
If the tumor is 30 cm in diameter, the estimated
probability of malignancy is calculated by giving
x,=30 to the equation, and calculated as 27% (Fig.
1). Figs 2,3 and 4 are examples of calculations using
this model for malignant tumors. Fig. 5 illustrates
the estimated probability of malignancy as a func-
tion of size and selected values of (x2,xg,x4, x5).
In a retrospective application of this model, max-
imum accuracy in discriminating between benign
and malignant was obtained at a cut-off point of
0.49 (between 0.47 and 0.51) (Fig. 6). When this
model was prospectively applied to the 75 cases
found at other hospitals, 50 tumors (43 benign and 7
malignant) had an estimated probability of malig-
nancy of 0.49 or less, and 25 tumors (4 benign and
21 malignant) more than 0.49. The mean point value
obtained was 0.26f0.17 for the benign masses and
0.70f0.25 for the malignant tumors. The model had
an accuracy of 86% (sensitivity 89%, specificity
89%) in distinguishing between benign and malig-
nant sonographically indeterminate lesions at a cut-
off point of 0.49.
576
Discussion
The cost of MR imaging precludes its use in initial
screening for ovarian cancer. It should be used spe-
cifically to help characterize a mass, particularly
when a sonogram is suboptimal or indeterminate (11,
14). On the basis of advances made in MR imaging
over the past several years, evaluation of adnexal
masses has become more accurate and a number of
studies have evaluated the sensitivity and specificity
of MR imaging in distinguishingbenign from malig-
nant ovarian masses. Contrast enhancement with
Gd-DTPA allows better depiction of the internal ar-
chitecture and differentiation of cystic from solid le-
tween malignant and benign lesions (13, 15). Pelvic
MR imaging with use of a phased-may coil unques-
tionably improves image quality. Normal ovaries can
be detected in the majority of patients, and fine inter-
nal architectural details can be visualized with high
resolution fast SE T2-weighted images. In body-coil
MR imaging, a Gd-DTPA-enhanced study is manda-
tory for detecting fine internal architectural details.
In phased-array-coil MR imaging, on the other hand,
high resolution T2-weighted images may elimiate
the need for contrast enhancement.
Small cystic or epithelial neoplasms were better
characterized by transvaginal ultrasonography
owing to its ability to resolve the internal architec-
tural details such as the focal mural wall thickness
or a solid component protruding from a predomi-
nantly cystic mass. A scoring system based on the
morphological characteristics of a mass at ultra-
sonography can, with reasonable accuracy, differen-
tiate benign from malignant masses (6, 12). In these
cn 20
.- 16
5
(I)
I2 12
w-
0
0
8
= 4
0
0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1
Estimated probability of malignancy
Fig. 6. In retrospective calculation, with the logistic regression
model for all tumors, maximum accuracy in discriminating be-
tween benign and malignant lesions was obtained at a cut-off
point of 0.49 (between 0.47 and 0.51). 0 Benign lesion. W Ma-
lignant lesion.
 MR IMAGING OF OVARIAN TUMORS

studies, however, each variable was arbitrarily benign or not. However, a combination of ap-
scored. In addition, false-positive predictive diag- proaches, such as the one developed in this study,
noses were frequently seen in mature cystic terato- will probably be able to improve the differentiation
mas, fibrothecomas, and less frequently, endometri- of benign and malignant ovarian and adnexal lesions.
omas, because these diseases have variable sono-
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577