Submitted: 10 April, 2022 Accepted: 09 May, 2022 Published: 15 June, 2022 DOI:10.22514/ejgo.2022.

017

ORIGINAL RESEARCH

Clinical and pathological examination of 11 cases of

ovarian seromucinous tumor at our institute
Takao Yamamoto1 , Kenbun Sone1, *, Ayumi Taguchi1 , Masako Ikemura2 ,
Harunori Honjoh1 , Akira Nishijima1 , Satoko Eguchi1 , Yuichiro Miyamoto1 ,
Michihiro Tanikawa1 , Mayuyo Uchino-Mori1 , Takayuki Iriyama1 , Tetsushi Tsuruga1 ,
Osamu Wada-Hiraike1 , Yutaka Osuga1

1
Department of Obstetrics and
Gynecology, Faculty of Medicine, The
University of Tokyo, 113-8655 Tokyo,
Japan
2
Department of Pathology, The
University of Tokyo Hospital, Bunkyo
City, 113-8655 Tokyo, Japan
*Correspondence
ksone5274@gmail.com (Kenbun Sone)
Abstract
Background: Seromucinous tumors, a category of ovarian epithelial tumors, were first
described in the 2014 World Health Organization’s (WHO) classification of tumors
of the female reproductive organs. However, seromucinous carcinoma was reviewed
and removed from the fifth edition of the WHO classification in 2020. We aimed to
report our experience with 11 seromucinous ovarian tumors (borderline tumors and
carcinomas). Methods: The clinical and pathological features of 11 seromucinous
ovarian tumors were examined. In addition, the pathological records of seromucinous
carcinoma were re-examined by a pathologist to determine if they could be considered
as a new classification. Results: Patient age ranged from 28 to 71 years, with a median
age of 45.6 years. The median tumor markers levels were 2.0 ng/mL, 68.0 U/mL,
and 36.6 U/mL for CEA, CA 19-9, and CA125, respectively. Pathological findings
showed that endometriosis was present in five cases (four seromucinous borderline
tumors and one seromucinous carcinoma). Most borderline tumors were diagnosed at an
early stage; three were diagnosed with the International Federation of Gynecology and
Obstetrics (FIGO) stage IA, three with stage ⅠC1, and one with stage IC2. Two cases of
seromucinous carcinoma were diagnosed with FIGO stage IA and two were diagnosed
with stage ⅠC2. There were two cases of recurrence; one was a seromucinous borderline
tumor and one was a seromucinous carcinoma. All cases were classified as endometrioid
carcinoma with mucinous differentiation. Conclusions: Our findings indicated the
low reproducibility of seromucinous carcinoma diagnosis. As seromucinous tumors
are relatively rare and the literature on them is limited, further studies on this topic are
warranted.

Keywords
seromucinous ovarian tumor; endometriosis; WHO classification

1. Introduction ovarian carcinomas [3]. According to the 2014 WHO clas-

Seromucinous tumors, a category of ovarian epithelial tumors,
were first described in the 2014 World Health Organization
(WHO) classification of tumors of the female reproductive
organs. Seromucinous tumors are epithelial tumors comprised
predominantly of serous and endocervical-type mucinous ep-
ithelium, often with foci showing clear cell, endometrioid, or
squamous differentiation [1]. Seromucinous tumors are con-
sidered endometriosis-related ovarian neoplasms, which are
often associated with endometriosis [1]. The characteristic mi-
croscopic findings include papillary structures with branching
patterns and a mixture of various types of epithelial cells [1].
The proportion of all borderline tumors among seromucinous
borderline tumors is low, at approximately 5–7% [2]. Sero-
mucinous carcinomas are relatively rare, and a previous study
reported that seromucinous carcinomas account for 4% of all
sification, seromucinous tumors are classified into seromuci-
nous cystadenomas/adenofibromas, seromucinous borderline
tumors, and seromucinous carcinomas. [1]. The fifth edition of
the WHO classification of female genital tumors was published
in 2020, and it reclassified serous mucinous carcinomas as
a subtype of endometrioid adenocarcinomas with mucinous
differentiation [4, 5]. Seromucinous tumors are a relatively
new classification of ovarian tumors, and there is a dearth
of literature on these tumors. We report our experience with
11 seromucinous ovarian tumors (borderline tumors and car-
cinomas). The clinical and pathological features of these
cases were examined. In addition, the pathological records
of the seromucinous carcinoma cases were re-examined by a
pathologist to determine if they could be categorized as a new
classification.

This is an open access article under the CC BY 4.0 license (https://creativecommons.org/licenses/by/4.0/).

Eur. J. Gynaecol. Oncol. 2022 vol.43(3), 127-133 ©2022 The Author(s). Published by MRE Press. https://www.ejgo.net/
 128
TA B L E 1. Clinical characteristics of patients.
Case Age Type Operation Laterality Size (cm) CEA (ng/mL) CA19-9 (U/mL) CA125 (U/mL) Stage Endometriosis Recurrence Dead
1 71 Carcinoma TAH+BSO+pOM Left 12 2.7 109 43 IA no no -
2 51 Carcinoma TAH+BSO+pOM+PLA+PALA Left 14 1.3 13 18 IA yes no -
3 67 Carcinoma TAH+BSO+pOM Right 14 1.8 31 45 IC2 no yes Dead
4 39 Carcinoma LSO+pOM Left 7 2.7 26 30 IC2 no no -
5 45 Borderline TAH+BSO+pOM Right 7 2.1 224 24 IC1 yes no -
6 40 Borderline RSO+pOM Right 7 2.8 264 87 IC1 yes no -
7 33 Borderline RSO+pOM Right 7 1.3 27 14 IA no no -
8 44 Borderline TAH+BSO+pOM Right 16 2.7 1 49 IC1 yes no -
9 28 Borderline LSO+pOM Left 5 1.6 10 20 IA no no -
10 55 Borderline TAH+BSO+pOM Left 10 1.8 15 45 IC2 no no -
11 28 Borderline Bilateral cystectomy+pOM Bilateral 9 1.2 28 28 IA yes yes -
TAH, total abdominal hysterectomy; BSO, bilateral salpingo-oophorectomy; pOM, partial omentectomy; PLA, pelvic lymphadenectomy; PALA, para-aortic lymphadenectomy; LSO, left
salpingo-oophorectomy; RSO, right salpingo-oophorectomy.
 129

TA B L E 2. Pathological features.
Case Architecture Immunohistochemical Staining
1 Papillary N/A
2 Papillary N/A
3 Papillary CK7(+), ER(+), PR(+), CK20(-), CDX2(-), WT-1(-)
4 Papillary, Tubular CK7(+), ER(+), PR(+), CK20(-), CDX2(-), WT-1(-)
5 Papillary N/A
6 Papillary CK7(+), ER(+), PR(+), CK20(-), CDX2(-), WT-1(-)
7 Papillary N/A
8 Papillary, Tubular N/A
9 Papillary N/A
10 Papillary N/A
11 Papillary N/A
N/A, not applicable; CK7, cytokeratin 7; ER, estrogen receptor; PR, progesterone
receptor; CK20, cytokeratin 20; CDX2, Caudal-type homeobox 2; WT1, Wilms’
tumor protein 1.

2. Materials and Methods
2.1 Ethics Approval and Consent to
Participate
This was a retrospective, single-center, observational study.
The study was approved by the ethics committee of the Uni-
versity of Tokyo (approval number 3084-(3)). Patient consent
was obtained using an opt-out form. In the patient appli-
cation forms and the relevant website, it was clearly stated
that patients were allowed to reject or withdraw from the
clinical study at any time. In addition to the application form
(with a provision for “opt out”), written informed consent
was obtained from the patients in this study. Eleven cases of
seromucinous tumors (borderline and carcinoma) were diag-
nosed from the surgical pathology files of the University of
Tokyo Hospital Obstetrics and Gynecology Department be-
tween April 2014 and April 2019. According to the 2014 WHO
criteria, four cases were classified as seromucinous carcinomas
and seven cases were classified as seromucinous borderline
tumors. Seromucinous carcinoma has been removed from the
2020 WHO classification of female genital tumors, but in this
study, “seromucinous carcinoma” was adopted according to
the original description of the disease name.
2.2 Clinical and Pathological Investigation
Information analyzed from the medical records of patients in-
cluded age, tumor size, tumor markers, operation, recurrence,
and status at the end of the study. We extracted pathologi-
cal data from the pathological reports of our hospital, which
included the tumor subtype, location (right, left, or both),
presence of a coexisting pathology such as endometriosis, and
histopathological stage. We classified tumors according to the
2014 WHO classification of female genital tumors, and staged
tumors according to the Tumor Node Metastasis (TNM) and
International Federation of Gynecology and Obstetrics (FIGO)
classifications. Formalin fixation and paraffin embedding
were performed on the pathological specimens. We performed
hematoxylin and eosin (H&E) staining on all specimens, and
CK7, ER, PR, CK-20, CDX2, and WT-1 expressions were
evaluated via immunohistochemistry for diagnosing seromuci-
nous ovarian tumor. In addition, a pathologist diagnosed four
seromucinous carcinomas based on the 2020 WHO classifica-
tion of female genital tumors.
3. Result
Table 1 shows the clinical and pathological findings of the 11
patients with ovarian seromucinous tumors. Of the 11 patients,
seven had borderline tumors and four had carcinomas. The
age at diagnosis ranged from 28 to 71 years with a median
age of 44 years. The median tumor marker levels (median ±
standard deviation) were 1.8 ± 0.6 ng/mL, 27 ± 91.9 U/mL,
and 30 ± 20.6 U/mL for carcinoembryonic antigen (CEA),
cancer antigen 19-9, and cancer antigen 125, respectively.
Of the 11 cases, the tumor was unilateral in ten cases and
bilateral in one case (Table 1). The size of the tumors ranged
from 5.0 cm to 15.6 cm (mean 8.4 cm). Pathological findings
showed that endometriosis was present in five cases (four
borderline and one carcinoma). All cases were diagnosed at
an early stage. Two of the borderline tumors were classified
as FIGO stage IA, four as stage ⅠC1, and one as stage IC2.
In the seromucinous carcinomas, two cases were classified as
FIGO stage IA and two were classified as stage IC2. Patho-
logical findings showed that all 11 tumors contained papillary
architecture and a mixture of cell types (serous, eosinophilic,
mucinous, clear, endometrioid, and a variety of other cell
types) in various proportions (Figs. 1,2 and Table 2). Immuno-
histochemical staining was performed in only three cases, all
of which were positive for ER, PR, and CK7, and negative for
CK-20, CDX2, and WT-1 (Fig. 3 and Table 2). The four cases
of seromucinous carcinoma were reviewed by pathologists in
our institute according to the FIGO 2020 classification. All
four cases were diagnosed with endometrioid adenocarcinoma
with mucinous differentiation.
In this study, there were two cases of recurrence: one with
seromucinous borderline tumor and one with seromucinous
carcinoma. We describe these two recurrent cases in detail
below. In the recurrent case of seromucinous borderline tumor,
the patient was 28 years of age. Tumors were present on
both ovaries and the patient underwent bilateral cystectomy
in the first surgery. Pathological findings showed that the
130
F I G U R E 1. Typical hematoxylin and eosin imaging find-
ings show the papillary architecture of the seromucinous
tumor in this examination (Original magnification × 4).
disease was seromucinous borderline tumor at FIGO stage
IC1. However, the borderline tumor recurred in the right
ovary 15 months after the first surgery, and we performed
right salpingo-oophorectomy and partial omentectomy for this
patient. No recurrence was observed in this patient after the
second surgery.
The patient with recurrent seromucinous carcinoma was 67
years of age. She was referred to our outpatient clinic with
a multi-cystic lesion (23 cm) observed on ultrasonography.
An ovarian borderline tumor was suspected from the MRI
findings (Fig. 4). Although surgery was recommended for this
patient, she refused surgery out of fear. One year after the first
consultation, her symptoms and abdominal fullness worsened
and she underwent surgery at this point.
Total abdominal hysterectomy, bilateral salpingo-
oophorectomy, and omentectomy were performed.
Pathological examination revealed a seromucinous carcinoma
in the right ovary and confirmed the diagnosis of FIGO stage
IC2. This patient refused to receive postoperative adjuvant
chemotherapy. Eleven months after the first surgery, the
patient’s disease recurred in the liver as seen on computed
tomography (Fig. 5). She received paclitaxel and carboplatin
chemotherapy. Because of disease progression, chemotherapy
was discontinued. The patient died one year after surgery.
4. Discussion
We performed a clinical and pathological review of 11 sero-
mucinous ovarian tumors. Seromucinous tumors were first
classified as a type of ovarian tumor by the 2014 WHO clas-
sification of tumors of the female reproductive organs. How-
ever, seromucinous carcinomas exhibited morphological and
immunophenotypic overlap with other ovarian carcinoma his-
totypes. Kruman and Shin questioned the definition of ovarian
seromucinous carcinoma in 2016 [6]. Rambau et al. [7]
examined the genotype of seromucinous carcinoma. There
were no disease specific features, and the features overlapped
with endometrioid carcinoma and mucinous and low-grade
serous carcinoma. This indicates that the morphological diag-
nosis of seromucinous carcinoma is uncharacteristic and does
not show a distinct immunophenotype or genotype. In the
fifth WHO classification (2020), seromucinous carcinoma was
removed due to poor diagnostic reproducibility. Moreover,
in the pathologic findings, seromucinous and endometrioid
carcinomas show a morphological overlap. Therefore, cases
that were diagnosed as seromucinous carcinoma until that point
were henceforth classified as endometrioid carcinomas with
mucinous differentiation.
The pathologists at our institute classified all cases as en-
dometrioid carcinomas with mucinous differentiation. There-
fore, this change in pathological classification was appropriate.
According to the 2020 WHO classification, benign and bor-
derline seromucinous tumors remain distinct entities. Previous
reports have shown that seromucinous borderline tumors are
usually diagnosed in young women (aged 33–44 years) and
have been reported to have an average size of 8–10 cm [8–
10]. Therefore, our cases are consistent with previous studies.
Most tumors in our series were unilateral. This differs from
previous reports; however, there may be bias because of the
small number of cases [8–10]. Pathological findings show that
seromucinous tumors are typically cystic and often have thick
walls. Characteristic microscopic findings of seromucinous
borderline tumors typically include papillary structures with
globular, edematous, and sometimes sclerotic stroma [11, 12].
Large numbers of neutrophils and eosinophils infiltrate the
stroma, epithelium, and lumen.
The most common cell types are endocervical-type muci-
nous, endometrioid, serous and eosinophilic; however, clear
cells, hobnail cells, squamous cells, and signet-ring cells may
also be observed in various proportions [1]. In our study,
all cases included endocervical-type mucinous cells, and most
cases included serous cells. Immunohistochemical findings
of seromucinous tumors are often positive for ER, PR, CK7,
PAX8, and vimentin, and negative for focal WT1 and CEA
staining, CK20, or CDX2 [13].
Endometriosis is frequently observed in seromucinous carci-
noma; endometriosis was present in 45% of cases (five of 11 tu-
mors). ARID1A is a chromatin remodeling factor encoding the
BAF250a protein. With regards to ovarian tumors, ARID1A
mutation and loss of BAF250a expression are useful in the
diagnosis of endometriosis-related ovarian tumors [14–17].
This abnormality was identified in approximately one-third
of the seromucinous tumor cases, and previous reports have
shown that seromucinous tumors coexist with endometriosis
in 30–70% of patients, suggesting that these tumors are closely
related to endometriosis [9]. Approximately 90% of seromu-
cinous borderline tumors present as FIGO stage I, and there
are few cases of stage IV tumors in the literature. However,
the prognosis is good even for advanced stage disease [18–
20]. In our study, all cases of seromucinous borderline tumors
(seven/seven) were diagnosed as stage I tumors. Standard
surgeries for seromucinous borderline tumors include total
hysterectomy, bilateral adnexal resection, partial omentec-
tomy, peritoneal biopsy, and ascites cytopathology [21]. Only
one case recurred in the right ovary, with no signs of recurrence
after the second surgery. In this case, the patient underwent
bilateral cystectomy to preserve fertility, which may have
 131

F I G U R E 2. Typical hematoxylin and eosin imaging findings of different cell types in in this examination. (A)
Serous+mucinous cells. (B) Eosinophilic cells. (C) Clear cells (Original magnification × 40).

F I G U R E 3. Typical immunohistochemistry imaging findings in in this examination. (A) CK7 (positive). (B) CK20
(negative). (C) ER (positive). (D) WT1 (negative) (Original magnification × 20).

contributed to tumor recurrence. para-aortic lymphadenectomy, peritoneal biopsy, and ascites

Previous studies have shown that most patients with sero-
mucinous carcinomas have a good prognosis, but those with
high stage seromucinous carcinomas have a poor prognosis.
In our study, all cases of seromucinous carcinoma (four/four)
were diagnosed as stage I disease. Two cases were stage
ⅠA and two were stage IC. Standard procedures for advanced
stage I seromucinous carcinoma include total hysterectomy,
bilateral adnexal resection, partial omentectomy, pelvic and
cytopathology for staging laparotomy [21]. Postoperative
chemotherapy is recommended for stage ⅠC ovarian carcinoma
[21].
In this study, we encountered a fatal case of seromucinous
carcinoma, although the neoplasm was stage IC. In this fatal
case, the patient refused to undergo surgery for a year and
refused chemotherapy after surgery. The fact that the patient
did not receive standard treatment may have contributed to the
132

F I G U R E 4. A 67-year-old woman with seromucinous carcinoma that was diagnosed as a seromucinous borderline tumor.
Magnetic resonance imaging: (A) axial T2-weighted image. (B) sagittal T2-weighted image.

subject is small, further studies are required on this topic.

A UTHOR CONTRIBUTIONS

TY, KS, and AT designed the research study. TY and KS

performed the research. AT, HH, AN, SE, YM, MT, MU-
M, TI, TT, OW-H, and YO provided assistance and advice
on. TY, KS, and MI analyzed the data. TY and KS prepared
the manuscript and figures. AT, MI, HH, AN, SE, YM,
MT, MU-M, TI, TT, OW-H, and YO revised the manuscript
for important intellectual content. All authors contributed to
editorial changes in the manuscript. All authors read and
approved the final manuscript.

F I G U R E 5. Recurrence in the S6 liver segment. Contrast

E THICS APPROVAL AND CONSENT TO
enhanced computed tomography.
PA R TICIPATE

This was a retrospective, single-center, observational study.

rapid progression of the disease. In contrast to this case, the
The study was approved by the ethics committee of the Uni-
prognosis of the other three patients with seromucinous car-
versity of Tokyo (approval number 3084-(3)). Patient consent
cinoma who received standard treatment was good. Further-
was obtained using an opt-out form. In the patient appli-
more, previous reports have shown that bilateral involvement
cation forms and the relevant website, it was clearly stated
is observed in 40% of seromucinous tumors, and up to 20%
that patients were allowed to reject or withdraw from the
have peritoneal implant or lymph node involvement [22, 23].
clinical study at any time. In addition to the application form
This study had some limitations. First, genetic analysis of (with a provision for “opt out”), written informed consent was
ARID1A was not carried out in this study. Second, because of obtained from the patients in this study.
the small sample size, additional cases are needed to clarify the
characteristics of seromucinous ovarian tumor.
ACK NOWLEDGMENT
5. Conclusions
The authors thank Editage for English language editing
Most of the clinical, pathological, and immunohistochemical (https://www.editage.com/).
findings of our 11 cases are consistent with those of previous
reports. One case in which the patient died may illustrate a F UNDING
natural history of seromucinous carcinoma. As seromucinous
tumors are relatively rare and the number of articles on this This research received no external funding.

CO NFL ICT OF IN T ERE ST
The authors declare no conflict of interest.
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How to cite this article: Yamamot T, Sone K, Taguchi
A, Ikemura M, Honjoh H, Nishijima A, et al. Clinical and
Pathological Examination of 11 Cases of Ovarian Seromucinous
Tumor at Our Institute. European Journal of Gynaecological
Oncology. 2022; 43(3): 127-133. doi: 10.22514/ejgo.2022.017.