229
OBJECTIVE: To analyze the sonographic features of
different histopathological subtypes of borderline ovarian
tumors (BOTs) confirmed by pathology, and to study the
ultrasound performances of various types in borderline
ovarian tumors.
STUDY DESIGN: Retrospective analysis was performed
on the pathological results and ultrasound projection
findings of 129 patients diagnosed as BOTs by ultra-
sound department of our hospital from January 2012 to
November 2019. All patients were confirmed by surgical
pathology and scanned consecutively by the investiga-
tors using transabdominal or transvaginal ultrasound
examination.
RESULTS: Serous borderline tumors (SBOTs) were
observed, and the prevalence rate (53%) was signifi-
cantly higher than that of other subtypes, and the prob-
ability of bilateral lesions was higher (40%). The sono-
gram often showed ultrasound features of papillary
neoplasm in the lesion and good internal echo (p<0.05).
Mucinous borderline ovarian tumors (MBOTs) were
mostly unilateral lesions (86%). The prevalence was
second only to SBOTs. Histomorphological exam-
inations were divided into gastrointestinal-type and
endocervical-type. Among them, the gastrointestinal
type of MBOTs were mostly unilateral, and their in-
cidence was higher than that of endocervical-type of
MBOTs. Compared with other pathological subtypes,
the gastrointestinal type is more likely to show the
sonographic characteristics of huge space occupying in
the pelvic and abdominal cavity (mean diameter >10
cm), polycystic, multiple septums, and poor internal
echo (p<0.05). The ultrasonographic features of the
endocervical-type of MBOTs were simi­
lar to those of
SBOTs. Compared with gastrointestinal type, the so-
nographic images showed smaller lesion diameter, less
septal or cyst, and more papillary excrescences in the
tumor (p<0.05). The borderline clear cell tumor is
the intermediate transition between the clear cell ade-
nofibroma and the clear cell carcinoma. The clinical
manifestations are diverse and lack specificity. The his­
tology of sonography was mainly solid, and the multi-
ple microcapsules were honeycomb-like. It can also be
shown as cystic. Among the 169 patients with BOTs,
20 cases of SBOTs, 17 cases of MBOTs, and 10 cases
of other rare subtypes were complicated with other
diseases or multiple subtypes. This study did not find
sig­
nificant ultrasonic characteristics were used for dis-
tinguish them from other subtypes.
CONCLUSION: BOTs is a common disease in women
during the reproductive period. It is characterized by the
development of malignant tumors. Its clinical and patho-
logical subtypes are complex and diverse. It leads many
doctors to use the terms “large pelvic mass” and “solid
ovarian mass” for diagnosis because of their lack of ex-
perience and understanding. (Anal Quant Cytopathol
Histpa­thol 2021;43:229–234)
Keywords: adenocarcinoma, mucinous; adenocar-
Analytical and Quantitative Cytopathology and Histopathology®
0884-6812/21/4304-0229/$18.00/0 © Science Printers and Publishers, Inc.
Analytical and Quantitative Cytopathology and Histopathology®
Ultrasound Findings of Different Subtypes of
Ovarian Borderline Tumors
Yuehang Liu, M.D., and Zongli Yang, M.D.
From the Department of Abdomen Ultrasound, The Affiliated Hospital of Qingdao University, Qingdao, Shandong Province, PR China.
Yuehang Liu is Resident Physician.
Zongli Yang is Professor.
Address correspondence to: Yang Zongli, M.D., Department of Abdomen Ultrasound, The Affiliated Hospital of Qingdao University,
No. 16 Jiangsu Road, Shinan District, Qingdao 266000, Shandong Province, PR China (qingyichaosheng@126.com).
Financial Disclosure: The authors have no connection to any companies or products mentioned in this article.

cinoma, serous; borderline ovarian tumors; diag-
nostic imaging; ovarian neoplasms; papillary neo-
plasms; prognosis; transvaginal ultrasound, ultra-
sonography.
According to its biological characteristics, ovarian
borderline tumors (BOTs) are defined as an ovari-
an tumors between benign and malignant ovarian
tumors, which has a potential risk of develop-
ing into malignant tumors. Compared with the
same stage of ovarian cancer, the clinical outcome
is better due to proliferation (mild-moderate cell
dysplasia) and no obvious stoma infiltration. Com-
mon types of BOTs are serous borderline ovarian
tumors (SBOTs) and mucinous borderline ovarian
tumors (MBOTs). Rare types include seromucin­
ous, endometrioid, clear cell, and Brenner tumors.
The MBOTs are divided into gastrointestinal-type
and endocervical-type.1 Since the pathological clas-
sification of BOTs is complex and the histobio-
logical characteristics are diverse, it is difficult to
accurately identify the different pathological types,
and ultrasound combined with various valuable
clinical indicators are used to improve the accu-
rate diagnosis of ovarian tumors. We aimed to
explore the advantages and disadvantages of pre­
operative diagnosis of BOTs.
Materials and Methods
Information
This study was retrospective. From January 2012
to November 2019, the pathological data of 129
patients diagnosed with BOTs by the Ultrasound
Department and confirmed by pathology were col-
lected. Among them, 69 cases of serous border-
line tumor were diagnosed, 46 cases of mucinous
tumors, 8 cases of endometrial, 2 cases of clear cell,
2 cases of seromucinous, and 2 cases of Brenner
tumor (Table I). The patients ranged in age from
17–80 years, with a median age of 45. All patients
were surgically resected and specimens were ob-
tained intraoperatively. Postoperative pathological
diagnosis results were obtained.
Instruments and Methods
Transabdominal ultrasound 3.5–5 Hz and trans-
vaginal ultrasound 5–10 Hz were performed on
all patients. Data were analyzed using SPSS Ver-
sion 20 statistical software (IBM Corp., Released
2011, IBM SPSS Statistics for Windows, Version
20.0, Armonk, New York, USA). The χ2 test was
used to analyze the Kruskal-Wallis test of multiple
independent samples, and p<0.05 was statistically
significant.
When the larger means of mass could not be
fully explored, the combined examination methods
of transabdominal and transvaginal were used to
ensure that the visual field was comprehensive
and sufficient. The sonographic features of differ-
ent pathological types were retrospectively ana-
lyzed. Combined with clinical and pathological
findings, the number of masses, the extent of in-
volvement (unilateral or bilateral, left or right),
and the shape of the mass (internal echo, papil-
lary and papillary morphology, septal and septal
morphological features, multilocular or single locu-
lar) were analyzed and discussed.
Results
Incidence and Sonographic Characteristics of Each
Subtype in 129 BOTs Patients
Incidence of Two Common BOTs Subtypes and Ultra-
sound Findings. The prevalence of SBOTs (53%)
was significantly higher than that of other sub-
types, and the probability of bilateral lesions was
higher (40%). The sonogram often showed the
ultrasonic characteristics of papillary neoplasm
with single atrium, little separation, good internal
echo, large number of papillary neoplasms, and
irregular shape in the lesion (p<0.05) (Table II).2
MBOTs were mostly unilateral lesions (86%), and
the prevalence rate was second only to the results
of SBOTs. Histopathological examination was di­
vided into gastrointestinal type and endocervical
type, of which gastrointestinal type was mostly
unilateral lesions, and the incidence rate was high­
er than that of endocervical type. Although the in-
230 Analytical and Quantitative Cytopathology and Histopathology®
Liu and Yang
Table I Pathological Data of 129 Patients with Ovarian Borderline Tumors
Pathological
classification SBOTs MBOTs Seromucinous Clear cell Endometrioid Brenner
Unilateral 41 40 1 2 7 2
Bilateral 28 6 1 0 1 0
Total 69 46 2 2 8 2

cidence of endocervical type was less than that of
gastrointestinal type, the bilateral incidence (45%)
was significantly higher than that of gastrointesti­
nal type. The gastrointestinal MBOTs with unilat-
eral and larger diameter (mean diameter >10 cm)
may be characterized by occupying a large pel-
vic space, multiple cysts and septations, smooth
capsule, and few definite solid or papillary neo-
plasms found in the lesions. Regarding the sono-
gram feature with poor echo in the lesion (p<0.05),3
endocervical-type of MBOTs and SBOTs have sim-
ilar ultrasonic manifestations. Compared with gas-
trointestinal MBOTs, the sonogram of these two
types of tumors shows smaller lesion diameter, less
compartmentalized cystic cavity, and more papil-
lary neoplasms in the tumor (Table III).1
Incidence of the Remaining Rare Subtypes and Ultra-
sound Findings. There were fewer cases of rare
types of BOTs in this study, although the inci-
dence was not statistically significant: 2 seromu-
cinous type, 8 endometrial type, and 2 Brenner
tumors were all rare types, and no significant ul-
trasound findings were identified to distinguish
other subtypes. The borderline clear cell tumor has
some characteristic ultrasound findings.
Clear cell tumors are intermediate transitions
between clear cell adenofibroma and clear cell
carcinoma. The ages of the two patients with
borderline clear cell tumors in this study were 55
and 69 years old, respectively. The clinical mani-
festations were lack of specificity, often unilateral
onset, may be accompanied by vaginal bleeding,
abdominal distending local discomfort or pain,
and so on. Acoustic histology showed a solid-
dominated and multiple cystic cavity (Figure 1)
with honeycomb-like structure and cystic.4
Concurrent BOTs with Other Diseases or Subtypes.
There was 1 patient with bilateral SBOTs com­
plicated with left ovarian Brenner tumor, 1 patient
with bilateral SBOTs complicated with right ovar-
ian hyperdifferentiated serous adenocarcinoma,
1 patient with right SBOTs with pelvic giant het-
erogeneous cystic mass (Figure 2), 2 patients with
unilateral SBOTs with contralateral ovarian tera-
toma, 6 patients with unilateral SBOTs complicat­
ed with serous cystadenoma, and 9 patients with
Volume 43, Number 4/August 2021 231
Ultrasound Findings of Ovarian Borderline Tumors
Table II Sonographic Features of 129 Ovarian Borderline Tumors
Ultrasound
Feature findings SBOTs MBOTs Seromucinous Clear cell Endometrioid Brenner
Location of lesion Left 18 13 1 1 1 2
Right 22 19 0 1 5 0
Bilateral 26 6 1 0 1 0
Pelvic/retroperitoneal 3 8 0 0 1 0
Maximum diameter, Approximate value 18 25 10 6 9 10
cm Unable to measure 1 5 0 0 0 0
Separation Multiple 13 37 2 2 4 2
Single 47 6 0 0 3 0
No/solid 9 3 0 0 1 0
Papillae Yes 61 12 2 0 3 1
No 8 34 0 2 5 1
Internal echo Good 59 5 0 1 0 1
Poor 10 41 2 1 8 1
Table III Ultrasound Characteristics of Different Pathological Subtypes of Mucinous Borderline Ovarian Tumors
Average
Pathological diameter,
classification Number Bilateral Unilateral cm Papillae Separation
Gastrointestinal type
35
1 34 13
4 33
Endocervical 11 5 6 8 7 4

unilateral SBOTs with low-grade invasive ovarian
cancer.
MBOTs Complicated with Other Diseases or Subtypes.
We identified 1 patient with right MBOTs com­
plicated with left ovarian goiter, 1 patient with
right MBOTs with a cancerous side with ovarian
Brenner tumor, 2 patients with unilateral MOBTs
complicated with ectopic endometrium, and 13 pa-
tients with hyperdifferentiated mucinous adenocar-
cinoma.
Other Rare Subtypes. We identified 1 patient with
right endometrial BOTs complicated with left
ovarian serous cystadenoma, 2 patients with en-
dometrial BOTs complicated with hyperdifferen­
tiated endometrial adenocarcinoma with secretion,
3 patients with endometrial BOTs complicated with
tumor cystic wall ectopic cyst, 1 case of left sero­
mucinous BOTs with partial carcinogenesis, squa-
mous metaplasia, and endometriosis, and 1 case
of right clear cell BOTs complicated with highly
differentiated clear cell carcinoma with left ovar-
ian serous cystadenoma. Both ovarian Brenner tu-
mors in this study were associated with other con-
current subtypes (Table IV).
Discussion
Borderline ovarian tumors are one of the common
diseases in women in reproductive stage. The
World Health Organization included it in the clas-
sification of ovarian tumor tissue in 1973. Because
of the large number of BOT pathological subtypes,
there is no typical symptom differentiation among
the subtypes. BOTs have the histological charac-
teristics of malignant tumors. The range of plasma
CA125 and CA199 elevation in borderline tumor
patients is large, not lending itself to becoming the
diagnostic standard.5
In this study, 110 (86%) of 129 patients came to
our department with a pelvic mass. It was found
that the resolution of transabdominal ultrasound
in the fine structures such as papillary neoplasm
in the capsule was worse than that of transvagi-
232 Analytical and Quantitative Cytopathology and Histopathology®
Liu and Yang
Figure 1
The left borderline clear cell
tumor of the ovary is
complicated with
intraepithelial canceration and
microinfiltration. Ultrasound
showed that the solid was
mainly accompanied by a
small cystic cavity.
Figure 2
Serous borderline tumor of
the ovary with intraepithelial
canceration with ovarian
torsion bleeding. Large pelvic
mass was diagnosed by
ultrasound.

nal. However, the range of lesions was better than
transvaginal ultrasound. The papillae in the ultra-
sound images showed solid protuberances with a
height ≥3 mm and a width ≤10 mm from the sac
wall or from the compartment.6 Papillary neoplasm
is the characteristic sonographic manifestation of
borderline ovarian tumor, but some benign and
malignant ovarian lesions can also show papillary
structure, but BOTs are more irregular neoplasm.7
The crescent sign of the ovary is defined as the
normal ovarian tissue near the tumor with or
without follicles, located near the cystic wall, sur-
rounded by the tumor, which is not separated
from the ovarian envelope when properly pres-
surized. Application to exclude invasive ovarian
cancer8 when a healthy ovarian group is found
near the tumor. The presence of multiple papillae
and ovarian crescent sign is typical of SBOTs or
endocervical-type.9 The honeycomb nodules are
mainly solid multilocular nodules, cystic cavity
number ≥10%, and the cystic area mostly origi-
nates from the cystic wall. Honeycomb nodules
are highly suggestive of gastrointestinal-type, and
when a multilocular cyst ≥10 microcystic cavi-
ties, possible gastrointestinal MBOTs should be
considered (Figure 3).10 However, typical features
are absent in a third of the cases, and these cases
are usually misdiagnosed.11 This retrospective
study compared the operation of patients post-
pathological results, and preoperative ultrasound
diagnosis found that most of the preoperative
ultrasound diagnoses used terms such as “pelvic
and abdominal giant mass,” “ovarian cystic solid
mass,” and other morphological descriptions. Few
senior experts can diagnose possible BOTs, due
to lack of experience and inadequate understand-
ing of the disease, as well as the fact that BOTs
can include a variety of diseases and features and
diagnostic significance of ultrasound findings are
easily masked, coupled with some metastatic ovar-
ian tumors, such as gastric ring cell carcinoma
complicated by Krukenberg tumor, or metastatic
ovarian space occupying from appendiceal ade-
nocarcinoma, all of which increased the diagnostic
difficulties of ultrasound doctors.
On the other hand, many studies have attempt-
ed to use systematic assessment methods to estab-
lish a standardized scoring model to evaluate the
classification of ovarian masses, simple criteria and
logistic regression models such as IOTA (Interna-
tional Association for Ovarian Tumor Analysis),
classified from tumor morphological sonographic
manifestations.12 The risk of malignancy index
(RMI) classifies by the condition of the capsule, the
size of the capsule, the age of the patient (divided
by 50 years of age), and ascites to predict malig-
Volume 43, Number 4/August 2021 233
Ultrasound Findings of Ovarian Borderline Tumors
Table IV Significant Differences in Sonographic Characteristics
of Different Pathological Types
Sonographic
features of Internal
6 subtypes Papillae Separation echo
χ2 46.427 51.430 72.375
p Value <0.05* <0.05* <0.05*
*p<0.05, the sonographic characteristics of different pathological types
were statistically significant.
Figure 3
(Left) Typical sonogram of
a serous borderline tumor.
(Right) Typical sonogram of a
mucinous borderline tumor.

nant risk for ovarian masses.13 These methods
which distinguish between benign and malignant
ovarian tumors have high accuracy, but the diag-
nostic rate in BOTs is generally low. With the
popularity of 3D technology in recent years, some
scholars have tried to use new technology to find
the difference from the previous 2D diagnosis.
Unfortunately, there is no definite evidence that
3D ultrasound is superior to the traditional 2D
examination in diagnostic BOTs.14
The sonographic characteristics of borderline
ovarian tumors with different pathological sub-
types were compared in this retrospective ana­
lysis. The number of samples of individual rare
types still needs to be improved in subsequent
studies. Although ultrasound is still very limited
in the accurate diagnosis of various subtypes of
BOTs, ultrasound, as a noninvasive method, has
unparalleled advantages in the changes of tissue
morphology, involvement range, fine structure,
post-operative, and recurrence of the mass. As
technology advances and our understanding of the
disease deepens, ultrasound will be more useful for
preoperative evaluation and surgical procedures in
BOTs patients, providing great clinical value.
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