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


Original Article
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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

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.

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

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

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

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Table 2. Univariate analysis of MRI parameters and tumor markers between benign and borderline ovarian tumors.

All subjects (n ¼ 99) Subjects without a solid portion (n ¼ 72)

Parameter Benign (n ¼ 62) Borderline (n ¼ 37) P value Benign (n ¼ 60) Borderline (n ¼ 12) 12) 12) P value

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

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

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6 Acta Radiologica 0(0)

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
Fig 3. ROC curves of MRI parameters and tumor markers for (33–36). The combined analysis of those laboratory mar-
differentiating borderline ovarian tumors from benign tumors. kers with the current parameters may be useful for char-
Combined analysis of MRI and CA 125 had the best diagnostic acterizing ovarian tumors. Third, the quantitative or
performance (AUC ¼ 0.906), followed by the presence of an semi-quantitative analysis with DCEI was not performed
enhancing solid portion (AUC ¼ 0.822). although literatures introduced its feasibility in assessing
the tumor aggressiveness (37,38). However, in our study,
Meanwhile, in our study, CA 19-9 was not a signifi- the presence of a solid portion itself was a powerful pre-
cant parameter in differentiating between borderline dictor, and the quantitative or semi-quantitative analysis
and benign tumors in cases without a solid portion using a region of interest may cause the measurement
(P > 0.05), although it was a significant predictor error in cystic masses with only very thin septi. Finally,
when all patients were included in analysis (borderline, our study had a retrospective design. Hence, there might
40.4 U/mL; benign, 10.4 U/mL; P ¼ 0.021). Although have been potential selection bias. However, we tried to
CA 19-9 may be elevated in patients with mucinous include consecutive patients with data available on MRI,
types of ovarian epithelial tumors, there remains con- tumor markers, and surgical confirmation during the
troversy regarding the utility of using CA 19-9 to char- study period.
acterize tumor histologic type (whether the mass is In conclusion, the combination of MRI with CA 125
benign, borderline, or malignant) (29). Further studies may enable better differentiation between borderline
with a larger population are needed. and benign ovarian tumors compared with MRI or
In terms of the surgical approach for benign ovarian tumor markers alone by detecting borderline tumors
tumors, laparoscopic excision leads to a significant with multiseptation and an elevated CA 125 level that
reduction in operative morbidity, hospital stay, and do not exhibit a solid portion. Further prospective stu-
recovery period in comparison with laparotomy (30), dies are required to validate our results.
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- Conflict of interest
ation of cystic content (31). However, methods such as None declared.
laparoscopic cystectomy after cystic aspiration are not
well established for the treatment of borderline tumors,
because spilling needs to be avoided (3). From this Funding
point of view, our data may support the safety of lap- This research received no specific grant from any fund-
aroscopic cystectomy for cystic ovarian masses with ing agency in the public, commercial, or not-for-profit
few septa, but not those with a solid portion or elevated sectors.
tumor markers, regardless of size. Conversely, when the
combination of MRI with CA 125 suggests a high like-
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