Introduction
Hysterectomy is one of the most common operations
in gynecology.[] The majority of hysterectomies are
performed for benign indications, such as abnormal
uterine bleeding, uterine fibroids, adenomyosis, endometriosis,
uterine prolapse, pelvic inflammatory
disease, and chronic pelvic pain.[,] Hysterectomy
may be performed abdominally (open, laparoscopic
and robotic) or vaginally.[,] Although open abdominal
hysterectomy is the most common method,
laparoscopic and robotic hysterectomies have been
preferred in recent years because these techniques offer
less bleeding, early mobilization, shorter hospital stay,
and cosmetic recovery.[] Vaginal hysterectomy is the
surgical removal of the uterus through the vagina is
usually preferred in women with uterine prolapse. This
technique provides fewer complications, a shorter hospital
stay, and a faster recovery compared with abdominal
hysterectomy.[,,]
Endometrial sampling is usually used to identify a
possible malignant pathology in the endometrium. Recent
studies reported that routine endometrial sampling
is unnecessary in patients undergoing hysterectomy for
benign conditions in the absence of clinical findings
suggestive of endometrial malignant pathology.[,]
Although endometrial biopsy results are benign, unexpected
uterine malignancies were incidentally reported
in hysterectomy specimens in patients who underwent
hysterectomy for benign indications.[,]
This study aimed to investigate the incidence of occult
gynecologic malignancies in women undergoing
hysterectomy for benign indications. For this purpose,
we evaluated the final pathologies of hysterectomy
specimens performed for benign indication and their
compatibilities with preoperative endometrial sampling
results.
Methods
This study was conducted approving by the Clinical
Research Ethics Committee of Ataturk University,
Medical Faculty, Erzurum, Turkey. Due to the retrospective
design of this present study, signed informed
consent was not obtained from participants. The medical
records of patients who underwent hysterectomy
for benign indications in Erzurum Nenehatun Hospital
between 2009-2019 were evaluated using the hospital"s
electronic system. Before surgery, blood biochemical
analyzes, including liver enzyme values, complete
blood count, clotting tests, and tumor markers and electrocardiography and telecardiography were performed
on all patients. At the same time, all patients
were evaluated by the anesthesiologist preoperatively.
The most suitable surgical method among abdominal
(open, laparoscopic, robotic) or vaginal hysterectomy
techniques was chosen based on the patient"s preference,
physical examination and clinical findings.
Patients 40 years and older with benign endometrial
biopsy results and who underwent a hysterectomy
due to benign indications were included. Patients diagnosed
with atypia or malignancy in cervical biopsy
or endometrial biopsies were excluded from the study.
Patients whose frozen section was reported as malignant
during surgery were excluded from this study.
Also, cases performed hysterectomy for a malign reason
or obstetric indication were excluded. The patients"
age, indications for hysterectomy, endometrial biopsy
and pap smear results, hysterectomy methods, and
histopathological results of hysterectomy specimens
were recorded.
The data were analyzed with Statistical Package for
Social Sciences 13.0 for Windows package software
(SPSS Inc., Chicago, IL, USA). A descriptive statistical
analysis was performed, and mean±standard deviation,
percentages and frequencies values were used.
Results
During the study period, 1630 patients who underwent
hysterectomy for benign indications were included.
The data in the medical records of these cases were
evaluated retrospectively. The mean age of the patients
was 48.4±6.9 years. One thousand two hundred thirty-
five patients (75.76%) underwent a total abdominal
hysterectomy, 194 patients (11.90%) underwent
a total laparoscopic hysterectomy, 50 patients underwent
(3.07%) robotic hysterectomy and 151 patients
(9.27%) underwent vaginal hysterectomy (Table 1).
Hysterectomy was performed as a primary indication
for uterine myoma (n=788, 48.3%), abnormal uterine
bleeding (n=539, 33.1%) and uterine prolapse (n=133,
8.2%) (Table 2). Preoperative endometrial sampling
was performed in 1160 cases (71.16%), and pathology
results are presented in Figure 1. The proliferative endometrium
was the most common with 43.87%, it was
determined endometrial polyp as 22.5%, and chronic
endometritis as 14.31%, endometrial hyperplasia as
6.72%, secretory endometrium as 5.77%, irregular proliferative
endometrium as 3.44%, atrophic endometrium
as 1.81% and insufficient material as 1.55%. Bilateral
or unilateral salpingoooferectomy was performed in 1002 (61.47%) of 1630 cases. Final histopathology results
of specimens are given in Figure 2 and Table 3.
Leiomyoma was observed to be the most common with
63.19%. In the final histopathological evaluation results,
malignancy was identified in 12 cases (0.73%), and the
mean age of these cases was 50.41±12 years. These malignancies
included four leiomyosarcomas (33.33%),
one endometrial sarcoma (8.33%), two endometrial
adenocarcinomas (16.66%), four ovarian carcinomas
(33.33%), and one ovarian fibrosarcoma (8.33%) (Table
4). Since malignancy was not suspected in the Doppler
ultrasonographic examination, none of these seven patients
with fibroids had Magnetic Resonance Imaging.
However, leiomyosarcoma was reported in four of these
patients in the final histopathological evaluation. All of
the occult malignant cases had preoperative endometrial
sampling, and no malignancy was observed in the
endometrial pathology results. However, endometrial
sarcoma was reported in a patient and endometrial adenocarcinoma
was reported in two patients in the final
histopathological evaluation. The pap smear results of
all patients diagnosed with occult cancer were negative
for intraepithelial lesion or malignancy. Occult ovarian
cancer was identified in five patients. All of these patients
had normal serum CA 125 levels preoperatively. Interestingly, the patient whose final pathology was reported
as ovarian fibrosarcoma had no ovarian cyst detected
using preoperative transvaginal ultrasonography.
In the other four cases reported occult ovarian carcinomas,
three cases had no ovarian mass in the transvaginal
ultrasonographic examination preoperatively. One case
had a 6 cm right ovarian cystic mass with normal serum
CA 125 levels. Although the intraoperative frozen section
report of this patient was benign, the ovarian fibrosarcoma
was reported in the final histopathological
examination (Table 4).
Table 1: Operation types in cases
Table 2: Clinical indications in cases
Fig 1: Pathology reports of patients with endometrial
sampling (n=1160).
Fig 2: Final histopathology results of hysterectomy
specimens.
Table 3: Final histopathology results of oophorectomy
specimens
Table 4: Characteristics of patients whose final histopathological results were reported as malignant
Discussion
The objective of this study was to investigate the incidence
of unexpected gynecological malignancies diagnosed
after hysterectomy for benign indications. We
analyzed 1630 women who underwent hysterectomy
for benign indications. Among these women, 1160
(71.16%) of them had an endometrial sampling. The
incidence of unpredictable gynecological cancer was 0.73%, and 58.3% of them were related to the uterus,
and 41.6% were related to ovarian tissues.
Hysterectomy is one of the most commonly performed
major surgical interventions worldwide.[]
The most common indications for hysterectomy include
uterine fibroids, abnormal uterine bleeding,
adenomyosis, endometriosis, uterine prolapse, pelvic
inflammatory disease, and chronic pelvic pain.[,]
In this current study, 48.34% of benign hysterectomies
were performed for uterine fibroids and 33.06% for
abnormal uterine bleeding. On the other hand, among
women found to have occult uterine malignancy, hysterectomy
was also performed as a primary indication
for uterine fibroids (58.33%) and abnormal uterine
bleeding (33.33%). All of the occult malignant cases
had preoperative endometrial sampling and the proliferative
endometrium was the most common with
66.66%. Unlike our results, the most common indications
for hysterectomy were reported as abnormal
bleeding (47%) and postmenopausal bleeding (15%)
in Parsons et al.'s[] study. Similar to our findings,
Topdagi et al.[] reported that 57.42% of benign hysterectomies were performed for uterine myoma and/or
treatment-resistant menometrorrhagia.
Studies showed that abnormal uterine bleeding is
the most common symptom in women with endometrial
cancer.[,] Thus, routine endometrial sampling
is recommended in all symptomatic women.[]
However, preoperative endometrial sampling has a
low predictive value for the diagnosis of uterine sarcomas.[] In a retrospective study, Pessoa et al.[]
analyzed 893 women who underwent uterine curettage
and reported the risk of endometrial malignancy
significantly higher in women aged ≥50 years than
that younger women. The authors proposed routine
endometrial sampling in all patients 50 years of age or
older for those undergoing hysterectomy. Also, they
reported a significant association between irregular
uterine bleeding and the presence of endometrial malignancy.
In this current study, preoperative endometrial
sampling was performed in 1160 cases (71.16%)
and the proliferative endometrium was the most
common with 43.87%. On the other hand, occult
uterine malignancy was identified in seven (0.42%)
cases and ovarian malignancy was identified in five
(0.30%) cases in the final histopathological evaluation
of specimens. The incidence of unpredictable endometrial
cancer was 0.18%. Interestingly, all of the
malignant cases had preoperative endometrial sampling,
and the results were benign. In seven of these
malignant cases, endometrial biopsy was reported as
a proliferative endometrium. Our results are compatible
with the results of Yuk et al.'s study.[] They analyzed
12.850 women who underwent a hysterectomy
for benign conditions. In their study, the incidence
of unexpected uterine malignancy and endometrial
cancer after hysterectomy was reported as 0.19%
and 0.12%, respectively. In another study, Topdagi et
al.[] reported unexpected malignancy in 13 of the
1050 patients (1.23%) who underwent hysterectomy
for benign indications. In a recent study, Parsons et
al.[] performed a retrospective review of 6981 patients
underwent hysterectomy for benign reasons.
The incidence of unexpected endometrial carcinomas
was reported as 0.19%. In another study containing
a large sample group, Desai et al.[] identified
229.536 adult women who underwent hysterectomy
for benign indications during ten years. The incidence
of occult uterine cancer was 0.96%, including 0.75%
with endometrial carcinoma and 0.15% with uterine
leiomyosarcoma. Also, the incidence of occult ovarian
cancer was observed as 0.19% in their study. These
results are in line with our results.
Limitations of the Study
This present study revealed the possibility of malignant
outcomes in hysterectomies performed for benign indications.
This study is important for the literature in
terms of revealing data at a secondary referral center
during a ten-year period. Also, this study reveals the
importance of a detailed preoperative evaluation for
the early diagnosis of malignancies. However, there
is a limitation in our study. Unfortunately, we had no
information on patients" postoperative follow-up revealing
potentially results caused by delays in diagnosis
and treatment of occult malignancies. Since there
is no intensive care unit in our hospital, follow-up and
treatment of these patients were carried out in tertiary
referral centers. Multicentre studies involving a large
number and analyzing long-term follow-up data of patients
are required.
Conclusion
In conclusion, the unexpected malignancy rate in
women who underwent hysterectomies for benign indications
was 0.73%, and 58.33% of them were related
to the uterus, and 41.6% were related to ovarian tissues.
Occult uterine and ovarian malignancies may be observed
in hysterectomies performed for benign indications.
A detailed preoperative assessment should be
performed on all patients, considering potential occult
malignancies. Patients who are scheduled for hysterectomy
with benign indications should be informed in detail
preoperatively about the final pathology reports may
be malignant.
Peer-review: Externally peer-reviewed.
Conflict of Interest: The authors have no conflicts of interest
to declare.
Ethics Committee Approval: The study was approved by
the Ataturk University Faculty of Medicine Clinical Research
Ethics Committee (No: 13, Date: 07/05/2020).
Financial Support: The authors declared that this study has
received no financial support.
Authorship contributions: Concept - B.G.K., A.N.A.,
P.U., S.A.Ö., Ö.A.; Design - A.N.A., B.G.K.; Supervision -
S.A.Ö., Ö.A., P.U.; Funding - A.N.A., B.G.K.; Materials -
A.N.A., B.G.K.; Data collection and/or processing - B.G.K.,
A.N.A., P.U., S.A.Ö., Ö.A.; Data analysis and/or interpretation
- B.G.K., A.N.A., P.U., S.A.Ö., Ö.A.; Literature search
- B.G.K., A.N.A., P.U., S.A.Ö., Ö.A.; Writing - B.G.K.,
A.N.A., P.U., S.A.Ö., Ö.A.; Critical review - B.G.K., A.N.A.,
P.U., S.A.Ö., Ö.A.
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