Acta Radiol OnlineFirst, published on July 31, 2015 as doi:10.

1177/0284185115597266

Original Article
Acta Radiologica
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! The Foundation Acta Radiologica
Differentiation between borderline and 2015
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DOI: 10.1177/0284185115597266
of MRI with tumor markers for large acr.sagepub.com

cystic masses (5 cm)

Sung Yoon Park, Young Taik Oh and Dae Chul Jung

Abstract
Background: There is overlap in imaging features between borderline and benign ovarian tumors.
Purpose: To analyze diagnostic performance of magnetic resonance imaging (MRI) combined with tumor markers for
differentiating borderline from benign ovarian tumor.
Material and Methods: Ninety-nine patient with MRI and surgically confirmed ovarian tumors 5 cm or larger (borderline,
n ¼ 37; benign, n ¼ 62) were included. On MRI, tumor size, septal number (0; 1–4; 5 or more), and presence of solid portion
such as papillary projection or septal thickening 0.5 cm or larger were investigated. Serum tumor markers (carbohydrate
antigen 125 [CA 125] and CA 19-9) were recorded. Multivariate analysis was conducted for assessing whether combined
MRI with tumor markers could differentiate borderline from benign tumor. The diagnostic performance was also analyzed.
Results: Incidence of solid portion was 67.6% (25/37) in borderline and 3.2% (2/62) in benign tumors (P < 0.05). In all
patients, without combined analysis of MRI with tumor markers, multivariate analysis revealed solid portion (P < 0.001)
and CA 125 (P ¼ 0.039) were significant for predicting borderline tumors. When combined analysis of MRI with CA 125
((i) the presence of solid portion or (ii) CA 125 > 44.1 U/mL with septal number 5 for borderline tumor) is incorpo-
rated to multivariate analysis, it was only significant (P ¼ 0.001). The sensitivity, specificity, PPV, NPV, and accuracy of
combined analysis of MRI with CA 125 were 89.1%, 91.9%, 86.8%, 93.4, and 90.9%, respectively.
Conclusion: Combined analysis of MRI with CA 125 may allow better differentiation between borderline and benign
ovarian tumor compared with MRI alone.

Keywords
Borderline tumor, ovary, magnetic resonance imaging (MRI), tumor marker, CA 125
Date received: 6 April 2015; accepted: 19 June 2015

washing or biopsy through laparotomy has been rec-

Introduction
Borderline ovarian tumors account for 15–20% of
ovarian epithelial tumors (1,2). They may involve the
peritoneum or lymphatics, which may be the cause of
tumor recurrence after incomplete resection (3,4). For
benign ovarian tumors, laparoscopic tumor excision is
the preferred surgical approach to preserve ovarian
function (5). On the contrary, insufficient surgical resec-
tion such as laparoscopic cystectomy may lead to
inaccurate tumor staging and a higher recurrence rate
in borderline ovarian tumors (4,6–8). Thus, a broader
range of surgical resection and exploration including
salgingo-ophorectomy, hysterectomy, or peritoneal
ommended to reduce the recurrence rate (3,9,10).
Radiologically, borderline ovarian tumors typically
manifest as septated cystic masses with solid nodules or
septal thickening (11,12). About 60–90% of the tumors
Department of Radiology and Research Institute of Radiological Science,
Yonsei University College of Medicine, Seoul, Republic of Korea
Corresponding author:
Young Taik Oh, Department of Radiology and Research Institute of
Radiological Science, Severance Hospital, Yonsei University College of
Medicine, 50 Yonsei-ro, Seodaemun-gu, Seoul, 120-752, Republic of
Korea.
Email: oytaik@yuhs.ac

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2 Acta Radiologica 0(0)
have discrete solid portions, which may provide clues
for differentiating borderline ovarian tumors from
benign tumors (11,13,14). Conversely, some borderline
tumors may appear as multiseptated cystic masses with-
out a solid portion, which may complicate differenti-
ation between benign and borderline tumors because
many benign ovarian tumors also exhibit multisepta-
tion (13,15). Hence, intraoperative frozen section ana-
lysis is sometimes additionally conducted to assess the
histologic aggressiveness of ovarian tumors when they
are preoperatively indeterminate in nature (16).
Previous studies have demonstrated that serum tumor
markers such as carbohydrate antigen 125 (CA 125) or
CA 19-9 can be elevated in borderline ovarian tumors,
and thus be useful for screening; about 30–70% of patients
with borderline tumors show increased levels of tumor
markers (17–19). Based on this background, we assumed
that the additional utilization of CA 125 or CA 19-9 in
MRI evaluation for ovarian cystic masses might contrib-
ute to accurate identification of borderline ovarian tumors
without remarkable septal thickening or solid nodules.
Thus, the purpose of our study was to retrospect-
ively analyze the diagnostic performance of MRI com-
bined with tumor markers for differentiating borderline
tumors from benign ovarian tumors.
Material and Methods
Study subjects
The institutional review board approved this retro-
spective study and the requirement of informed consent
was waived. Based on a search of electronic medical
records from January 2005 to December 2013 at our
institution, we found 133 consecutive patients who had
undergone preoperative pelvic MRI and had surgically
confirmed borderline or benign ovarian tumors (Fig. 1).
Of the patients, 24 were excluded for the following rea-
sons: (i) absence of available serum tumor markers such
as CA 125 or CA 19-9 (n ¼ 15); (ii) tumor size less than
5 cm (n ¼ 9); (iii) co-morbid endometriosis (n ¼ 9); and
(iv) co-morbid endometrial cancer (n ¼ 1). Ovarian
cystic masses less than 5 cm were excluded because of
the low risk of malignancy; consequently, they usually
undergo active surveillance without surgical interven-
tion unless morphologic changes or elevated tumor
markers are detected (20,21). Patients with co-morbid
endometriosis or endometrial cancer were also excluded
because they may cause elevated serum tumor markers,
regardless of ovarian pathology (22–24). In addition,
the presence of endometriosis could be correctly diag-
nosed by imaging because they showed typical mani-
festation of MRI in our patients, which was a cystic
tubo-ovarian lesion of high signal intensity on T1-
weighted (T1W) imaging with T2 shading (25).
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Thus, a total of 99 patients who had borderline ovar-
ian (n ¼ 62) or benign ovarian (n ¼ 37) tumors were
finally included in our study. None of the included sub-
jects had evidence of diffuse uterine adenomyosis, mature
cystic teratoma, or pelvic inflammatory disease clinically
and radiologically. Of the 99 patients, four had bilateral
ovarian lesions with the same pathologic results (border-
line, n ¼ 2; benign, n ¼ 2). In patients with surgically con-
firmed bilateral lesions, a lesion with the solid portion or
greater septal number was only included in analysis
because these radiologic features suggested more aggres-
sive histology (13,14). All of the lesions were mainly
cystic masses radiologically and pathologically.
MRI protocols
The pelvic MRI was performed on one of three 3T scan-
ners (Intera Archieva, Philips Medical System, Best, The
Netherlands; Discovery MR750, GE Healthcare,
Milwaukee, WI, USA; TrioTim, Siemens, Erlangen,
Germany) with a phased-array body coil. T1W imaging,
T2-weighted (T2W) imaging, and dynamic contrast-
enhanced imaging (DCEI) were included on MRI. MRI
protocols are summarized in Table 1. Before MRI, 20 mg
of butyl scopolamine (Buscopan, Boehringer Ingelheim,
Ingelheim am Rhein, Germany) was intramuscularly
injected to suppress bowel peristalsis. For DCEI, the
gadolinium-based contrast agent (Dotarem; Guerbet,
Villepinte, France) was infused intravenously.
Analysis of MRI and tumor markers
Two radiologists (with 15 and 3 years of pelvic MRI
experience, respectively), who were blinded to clinical
and pathological data, analyzed the MRI examinations
in consensus. Mass size, septal number, and the pres-
ence of a solid portion were investigated with T1W
imaging, T2W imaging, and DCEI. Mass size was
defined as the longest diameter of a lesion to be mea-
sured on T2W imaging. Using T2W imaging, the septal
number of a lesion was classified into one of three
groups (0; 1–4; 5 or more) according to a previous clas-
sification method (26). The presence of a solid portion
was defined as when an enhancing nodular portion or
thickened septum or wall 5 mm or greater with iso or
low signal intensity on T2W imaging was seen within
the lesion (13). In all patients, preoperative serum CA
125 and CA 19-9 levels were recorded.
Statistical analysis
For comparison of mass size, CA 125, and CA 19-9
between borderline and benign ovarian tumors, the
Mann–Whitney test was used because the data did
not have a normal distribution. For comparison of
Park et al. 3

Fig 1. Flowchart of study group.

Table 1. MRI protocols.

Parameter T1W imaging T2W imaging DCEI

Orientation Axial Three planes* Sagittal

TR (ms) 470–590 3500–4500 6.3
TE (ms) 10 80–120 1.7
Flip angle ( ) 90 90 90
Matrix 256  256 (416–512)  (256–419) 320  180
NEX 2 1–3 1
FOV (mm) 240–300 240–300 240–300
Slice thickness (mm) 4–5 4–5 4–5
*Three planes consisted of axial, sagittal, and coronal images.
NEX, number of excitations; TE, echo time; TR, repetition time.

the number of septa and the ratio of subjects with a

solid portion, the Fisher’s exact test was used.
Multivariate analysis via logistic regression was applied
to determine which MRI parameters or tumor markers
were predictive factors for discriminating borderline
tumors from benign ones. Receiver operating characteris-
tic (ROC) curve analysis was performed to analyze the
areas under the curve (AUCs) or optimal cutoff values of
MRI parameters and tumor markers for predicting bor-
derline tumors. Finally, the sensitivity, specificity, positive
predictive value (PPV), negative predictive value (NPV),
and accuracy of the combined MRI/CA 125 analysis for
predicting borderline tumors were calculated.
Statistical analyses were performed using SPSS (ver-
sion 20.0; SPSS, Inc., Chicago, IL, USA) and MedCalc
(version 13.0, MedCalc Software, Mariakierke, Belgium).
A P value <0.05 was considered statistically significant.
Results
Table 2 summarizes the MRI parameters and tumor mar-
kers between borderline and benign ovarian tumors. In
univariate analysis, the ratio of tumors with solid portions
was higher in borderline tumors than in benign tumors
(67.6% versus 3.2%, respectively, P < 0.001). Both CA
125 and CA 19-9 were significantly higher in borderline
tumors than benign tumors (P < 0.05). However, tumor
size and septal number were not significantly different
between the two groups (P > 0.05).
In subjects without a solid portion, the septal
number and CA 125 were only significantly different
between two groups (P < 0.05), while tumor size and
CA 19-9 were similar (P > 0.05). The ROC curve ana-
lysis revealed the optimal cutoff values of the two sig-
nificant parameters, number of septa, and CA 125, for
predicting borderline tumor in subjects without a solid

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4 Acta Radiologica 0(0)
Table 2. Univariate analysis of MRI parameters and tumor markers between benign and borderline ovarian tumors.
All subjects (n ¼ 99)
Parameter Benign (n ¼ 62) Borderline (n ¼ 37)
Size (cm) 14.4 (5.1–37.7)* 12.5 (5.6–36.2)
Septal number
0 16.1% (10/62) 8.1% (3/37)
1–4 19.4% (12/62) 10.8% (4/37)
5 64.5% (40/62) 81.1% (30/37)
Solid portion 3.2% (2/62) 67.6% (25/37)
CA125 (U/mL) 19.4 (4.4–232.0) 38.8 (5.1–1009.6)
CA19-9 (U/mL) 10.4 (0.1–320.0) 40.4 (0.0–1580.0)
*Data are presented as the median (range).
CA 125, carbohydrate antigen 125; CA19-9, carbohydrate antigen 19-9.
portion as follows: (i) septal number 5 (P < 0.001);
and (ii) CA 125 > 44.1 U/mL (P ¼ 0.003). With a
septal number cutoff of 5 and of CA 125 > 44.1 U/mL,
eight of 12 borderline tumors without a solid portion
(66.7%) were additionally diagnosed, while there were
only four false-positive cases from among 38 benign
tumors without a solid portion (10.5%) (Fig. 2).
Based on the cutoff values for septal number and CA
125 derived from ROC curve analysis, the diagnostic
criteria of MRI combined with tumor markers (i.e. CA
125) for predicting borderline tumor were defined as
follows: (i) the presence of solid portion; or (ii) CA
125 > 44.1 U/mL and septal number 5. In all patients,
without combined MRI/tumor marker prediction,
multivariate analysis revealed that the presence of a
solid portion (odds ratio ¼ 104.574, P < 0.001) and
CA 125 (odds ratio ¼ 1.015; P ¼ 0.039) were significant
predictors of borderline tumors (Table 3). When com-
bined analysis of MRI with CA 125 was added to the
multivariate analysis, it was only significant factor
(odds ratio ¼ 77.449, P ¼ 0.001).
The AUC of MRI combined with CA 125 was 0.906,
followed by the presence of the solid portion
(AUC ¼ 0.822), for predicting borderline ovarian
tumors in all subjects (Table 4 and Fig. 3). In addition,
the sensitivity, specificity, PPV, NPV, and accuracy of
the combined MRI/CA 125 analysis for predicting bor-
derline tumors were 89.1%, 91.9%, 86.8%, 93.4%, and
90.9%, respectively.
Discussion
In our study, the presence of a solid portion (an enhan-
cing nodular portion, or thickened septum or wall 5 mm
or greater) within the mass was a powerful radiologic
predictor for differentiating borderline tumors from
benign tumors (AUC ¼ 0.822). A solid portion was
found in more than half of the patients with borderline
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Subjects without a solid portion (n ¼ 72)
P value Benign (n ¼ 60) Borderline (n ¼ 12) 12) 12) P value
0.607 14.2 (5.1–37.7) 21.3 (8.9–36.2) 0.083
0.267 0.047
16.7% (10/60) 0% (0/12)
20.0% (12/60) 0% (0/12)
63.3% (38/60) 100% (12/12)
<0.001 N.A. N.A. N.A.
0.001 19.0 (4.4–232.0) 59.7 (11.4–537.8) 0.004
0.021 10.4 (0.1–320.0) 31.1 (0.0–1580.0) 0.380
ovarian tumors (67.6%) on MRI, while it was seen in
only 3.2% of patients with benign tumors (P < 0.001).
Thus, we can confidently suggest the possibility of bor-
derline or more aggressive types of ovarian tumors when
MRI demonstrates a solid portion within a cystic mass.
However, the usefulness of this characteristic may still be
limited in characterizing large ovarian cystic masses
because 10–40% of borderline tumors may not exhibit
a definite solid portion (11,13,14). Concordantly, for
32.4% of patients with borderline tumors in our study,
a solid portion was not seen on MRI.
In the comparison between borderline and benign
ovarian tumors without a solid portion, all of the
patients with borderline tumors exhibited multisepta-
tion (5 or more) (100%, 12/12; P ¼ 0.047) and a
higher serum level of CA 125 than those with benign
tumors (median, 59.7 U/mL versus 19.0 U/mL;
P ¼ 0.004). Accordingly, with a septal number cutoff
of 5 and CA 125 > 44.1 U/mL derived from ROC
curve analysis, eight of 12 borderline tumors without
a solid portion (66.7%) were additionally diagnosed,
while there were only four false-positive cases in 38
benign tumors without a solid portion (10.5%). For
this reason, two steps of analysis ((i) the presence of
solid portion, or (ii) CA 125 > 44.1 U/mL and septal
number 5) with combined MRI/CA 125 analysis
showed the best diagnostic performance
(AUC ¼ 0.906) and was the only significant predictor
in multivariate analysis (odds ratio ¼ 77.449,
P ¼ 0.001). To the best of our knowledge, the current
combined approach with MRI and tumor markers is
the first attempt to differentiate borderline ovarian
tumors from benign tumors and seems to provide
good diagnostic performance (accuracy, 90.9%).
A previous study conducted by deSouza et al.
reported that patients with borderline ovarian tumors
had marginally elevated CA 125 (median, 45 U/mL)
(11). Lenhard et al. also reported that patients with
Park et al. 5

Fig 2. MRI of two patients with an ovarian cystic mass. (a) A 35-year-old woman with a surgically confirmed borderline tumor of the
right ovary. T2W axial image shows a cystic mass measuring 15.0 cm with multiseptation (more than five) in the pelvic cavity. No solid
portion 0.5 cm or larger was found. The serum CA 125 and CA 19-9 levels were 72.0 U/mL and 9.6 U/mL, respectively. Combined
analysis of MRI and CA 125 correctly predicted borderline tumor. (b) A 40-year-old woman with a surgically confirmed benign tumor
of the left ovary. T2W axial image shows a cystic mass measuring 14.6 cm with multiseptation (more than five) in the pelvic cavity. No
solid portion 0.5 cm or larger was found. Serum CA 125 and CA 19-9 were 19.1 U/mL and 10.5 U/mL, respectively. Combined analysis
of MRI and CA 125 correctly predicted benign tumor.

Table 3. Multivariate analysis of MRI parameters, tumor markers, and combined MRI with CA 125 for predicting borderline ovarian tumor.

Before combined MRI/CA 125 analysis After combined MRI/CA 125 analysis

Parameter Odds ratio P value Odds ratio P value

Size 0.991 (0.912–1.077) 0.844 0.972 (0.855–1.104) 0.663

Septal number 2.284 (0.714–7.298) 0.163 2.120 (0.362–12.406) 0.404
Solid portion 104.574 (15.643–699.061) <0.001 2.364 (0.095–58.495) 0.599
CA 125 1.015 (1.001–1.030) 0.039 0.988 (0.969–1.007) 0.238
CA 19-9 1.003 (0.999–1.007) 0.097 1.006 (0.998–1.013) 0.120
MRI combined with CA 125 N.A. N.A. 77.449 (5.693–1053.490) 0.001
CA 125, carbohydrate antigen 125; CA19-9, carbohydrate antigen 19-9.

Table 4. ROC curve analysis of MRI parameters and tumor markers for predicting borderline ovarian tumor in all subjects.

Diagnostic performance

Parameter Cutoff AUC Sensitivity Specificity P value

Size (cm) 26.0 0.531 94.6% 19.4% 0.599

Septum (n) 5 0.584 81.1% 35.5% 0.064
Solid portion Positive 0.822 67.6% 96.8% <0.001
CA 125 (U/mL) >36.2 0.689 54.1% 80.6% 0.001
CA 19-9 (U/mL) >17.8 0.639 64.9% 69.4% 0.025
MRI combined with CA 125 Positive 0.906 89.2% 91.9% <0.001
AUC, area under the curve; CA 125, carbohydrate antigen 125; CA19-9, carbohydrate antigen 19-9.

borderline ovarian tumors showed a higher CA 125
level (median, 34.7 U/mL) than healthy women
(median, 13.5 U/mL) (27). Our data for 37 patients
with borderline tumors were also in line with
the results of deSouza et al. (median, 38.8 U/mL;
range, 5.1–1009.6 U/mL). Generally, a serum level of
35 U/mL of CA 125 has been accepted as the normal
upper limit (28). Thus, marginal elevation of CA 125 in
patients with a multiseptated cystic mass of the ovary
may be suggestive of borderline tumor.

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6 Acta Radiologica 0(0)
Fig 3. ROC curves of MRI parameters and tumor markers for
differentiating borderline ovarian tumors from benign tumors.
Combined analysis of MRI and CA 125 had the best diagnostic
performance (AUC ¼ 0.906), followed by the presence of an
enhancing solid portion (AUC ¼ 0.822).
Meanwhile, in our study, CA 19-9 was not a signifi-
cant parameter in differentiating between borderline
and benign tumors in cases without a solid portion
(P > 0.05), although it was a significant predictor
when all patients were included in analysis (borderline,
40.4 U/mL; benign, 10.4 U/mL; P ¼ 0.021). Although
CA 19-9 may be elevated in patients with mucinous
types of ovarian epithelial tumors, there remains con-
troversy regarding the utility of using CA 19-9 to char-
acterize tumor histologic type (whether the mass is
benign, borderline, or malignant) (29). Further studies
with a larger population are needed.
In terms of the surgical approach for benign ovarian
tumors, laparoscopic excision leads to a significant
reduction in operative morbidity, hospital stay, and
recovery period in comparison with laparotomy (30),
thereby it is generally performed for benign tumors.
Even for benign cystic masses larger than 10 cm, the
use of laparoscopy allows safe excision after the aspir-
ation of cystic content (31). However, methods such as
laparoscopic cystectomy after cystic aspiration are not
well established for the treatment of borderline tumors,
because spilling needs to be avoided (3). From this
point of view, our data may support the safety of lap-
aroscopic cystectomy for cystic ovarian masses with
few septa, but not those with a solid portion or elevated
tumor markers, regardless of size. Conversely, when the
combination of MRI with CA 125 suggests a high like-
lihood of borderline tumor, radiologists should recom-
mend a more invasive surgical approach, such as
laparotomy, to avoid understaging or tumor rupture.
Our study had several limitations. First, malignant
ovarian tumors were not analyzed. Because there was
clinical, radiological, and even pathological (i.e. frozen
section analysis) overlap between borderline tumors
and early-stage malignant tumors (11,19,32), our criteria
derived from the combination of MRI with CA 125 may
be limited in predicting borderline tumors. Nevertheless,
the current study may be meaningful because
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preoperative underestimation and following insufficient
surgery may be reduced with our combined analysis
(4). When the lesion meets our criteria for borderline
tumors, the interpretation should suggest at least border-
line tumor, with the potential for malignancy. Second,
tumor markers other than CA 125 or CA 19-9 were
not analyzed. Researchers have reported that various
markers (i.e. carcinoembryonic antigen, CA 72-4, or
tissue polypeptide antigen) have shown promise as mar-
kers for borderline tumor or early-stage ovarian cancer
(33–36). The combined analysis of those laboratory mar-
kers with the current parameters may be useful for char-
acterizing ovarian tumors. Third, the quantitative or
semi-quantitative analysis with DCEI was not performed
although literatures introduced its feasibility in assessing
the tumor aggressiveness (37,38). However, in our study,
the presence of a solid portion itself was a powerful pre-
dictor, and the quantitative or semi-quantitative analysis
using a region of interest may cause the measurement
error in cystic masses with only very thin septi. Finally,
our study had a retrospective design. Hence, there might
have been potential selection bias. However, we tried to
include consecutive patients with data available on MRI,
tumor markers, and surgical confirmation during the
study period.
In conclusion, the combination of MRI with CA 125
may enable better differentiation between borderline
and benign ovarian tumors compared with MRI or
tumor markers alone by detecting borderline tumors
with multiseptation and an elevated CA 125 level that
do not exhibit a solid portion. Further prospective stu-
dies are required to validate our results.
Conflict of interest
None declared.
Funding
This research received no specific grant from any fund-
ing agency in the public, commercial, or not-for-profit
sectors.
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