Introduction
Endometriosis is a chronic benign systemic
proinflammatory condition, which is characterized by the growth of
endometrium (glands and stroma) outside the uterus, mostly in the
ovaries, followed by the soft tissue, gastrointestinal and urinary
tract. Globally, it affects 7-10% of women with an incidence of 38%
in infertile women and 71-87% in women with chronic pelvic pain
(1,2). Histologically endometriosis is
classified as having a typical and atypical form. Atypical
endometriosis indicates a premalignant lesion and is characterized
by areas of marked cellular atypia with morphologic features
similar to those of clear cell carcinoma. By contrast, typical
endometriosis is a benign condition that involves endometrial-like
tissue growing outside the uterus (3,4).
Adenomyosis is a benign uterine condition, which is
characterized by the infiltration of ectopic endometrial tissue
(glands and stroma) within the underlying myometrium (5,6).
Depending on the distribution within the myometrium, adenomyoma can
be classified as focal, diffuse or polypoid adenomyoma (5,6).
Adenomyosis appears in late childbearing years (40-50 years of
age). It is accompanied by menorrhagia in 40-50% of cases, by
dysmenorrhoea that does not respond to the standard
anti-inflammatory treatment (such as non-steroidal
anti-inflammatory drugs) in 15-78% of cases and infertility in
11-12% of cases. The global prevalence of adenomyosis among
patients after a hysterectomy varies from 5-70 % (5,6).
However, European estimates using imaging (such as ultrasound and
MRI) suggest a prevalence of 20-35%, but the data are limited
(6). In 1927, the study by Sampson
(7) coined the term endometriosis.
Furthermore, in 1972, a study by Bird (8) defined adenomyosis as the benign
invasion of endometrium into the myometrium, surrounded by the
hypertrophic and hyperplastic myometrial tissue. Although,
adenomyosis was previously called ‘endometriosis interna’, a form
of endometriosis, it is well documented that both diseases are
distinct. Endometriosis is considered to form from the functional
endometrium and adenomyosis is considered to form from the basal
endometrium. Various etiological factors, such as genetic,
endocrine, autoimmune, environmental and anatomical factors, serve
a role in the development of both entities (1,2,6-9).
It is hypothesized that retrograde menstruation is the primary
mechanism for endometriosis and that local invasion, cellular
proliferation and angiogenesis are mechanisms for adenomyosis
(1,2,6,7,9).
Furthermore, patients with breast cancer that are treated with
tamoxifen are at a distinct risk of endometriosis, adenomyosis and
several other gynecological conditions such as endometrial polyps,
hyperplasia and uterine cancer (10).
Gynecological diseases such as adenomyosis,
leiomyomas, endometriosis, endometrial polyps, hyperplasia,
endometrial and ovarian cancer often coexist, which suggests that
they may share common pathogenic mechanisms such as the presence of
hyperestrogenism, inflammatory, environmental and genetic altered
features (1,5,11,12).
The aim of the present study was to determine the
histological frequency of various benign and malignant
gynecological diseases among women with endometriosis, adenomyosis
or both that underwent gynecological surgery.
Materials and methods
Patients
Women (aged ≥18 years) that underwent abdominal
hysterectomy with bilateral or unilateral salpingo-oophorectomy
with a clear medical record documentation, at the Department of
Obstetrics and Gynecology of Venizeleio General Hospital
(Heraklion, Greece) in January 2000 to December 2022 and the Third
Department of Obstetrics and Gynecology of Aristotle University of
Thessaloniki (Thessaloniki, Greece) in January 2009 to December
2019, were included in the present study. Data were collected
retrospectively and included the indication for gynecological
operation, age, clinical and histopathological findings.
Patients were divided into three groups, namely
group 1 (which included women with endometriosis), 2 (which
included women with adenomyosis) and 3 (which included patients
with both endometriosis and adenomyosis). All data were retrieved
from the medical records. Cases with inadequate medical records and
those lacking histological diagnoses were excluded. Patient consent
for participation was waived by the ethics committees due to the
retrospective nature of the present study. The Ethics Committees of
Venizeleio General Hospital (approval no. 124-17-18/12/2019;
Heraklion, Greece) and Aristotle University of Thessaloniki
(approval no. 1130-03/07/2020; Thessaloniki, Greece) both approved
the protocol of the present study.
Statistical analysis
The descriptive statistics are presented as mean ±
standard deviations or as frequencies and percentages. Associations
between categorical variables was estimated using the Chi-square
test of independence. The parameter ‘age’ was analyzed using
one-way ANOVA followed by Tukey's post hoc test. Multinomial
logistic regression was carried out to detect factors associated
with pathology. Statistical analysis was carried out using IBM SPSS
Statistics (version 25.0; IBM Corp.).
Results
Eligible population
In total, 3,511 women underwent abdominal
hysterectomy with bilateral or unilateral salpingo-oophorectomy at
the Department of Obstetrics and Gynecology of Venizeleio General
Hospital (Heraklion, Greece) and the Third Department of Obstetrics
and Gynecology of Aristotle University of Thessaloniki
(Thessaloniki, Greece) in the study period. However, of these 3,511
women, only 1,692 cases were eligible for inclusion in the present
study, having endometriosis, adenomyosis or both conditions. The
majority of cases had adenomyosis (n=1,096; 64.8%; group 2),
followed by endometriosis (n=495; 29.3%; group 1), while 101 cases
had both endometriosis and adenomyosis (6.0%; group 3). The mean
age of the total study population was 50.16±12.74 years (range,
16-85 years). However, the mean age of patients with adenomyosis
was significantly higher (55.34±10.21) compared with those of the
other two groups.
Reported pathologies among the
groups
In the total sample of 1,692 women, the most
commonly noted pathology was leiomyomas (43.3%), followed by
endometrial polyps (17.6%). Benign ovarian (12.2%) and paraovarian
cysts (13.7%), and cervical polyps (9.8%) were also frequently
observed. The occurrence of leiomyomas was significantly more
frequent in patients in group 3 (67.3%) compared with those in
groups 1 (24.2%) or 2 (49.6%). A similar result was observed for
the frequency of ovarian cysts, which were more common in the
patients in group 3 compared with those in groups 1 or 2 (Table I).
 | Table IFrequencies of various pathologies
among the patients. |
Table I
Frequencies of various pathologies
among the patients.
| Characteristic | Patients with
endometriosis (n=495) | Patients with
adenomyosis (n=1,096) | Patients with
endometriosis and adenomyosis (n=101) | P-value |
|---|
| Age, years (mean ±
SD) | 38.63±10.78 | 55.34±10.21 | 50.48±8.70 | <0.001 |
| Cervical polyps, N
(%) | 19 (3.8) | 130 (11.9) | 17 (16.8) | <0.001 |
| Endometrial polyps,
N (%) | 24 (4.8) | 261 (23.8) | 13 (12.9) | <0.001 |
| Endometrial
hyperplasia without atypia, N (%) | 6 (1.2) | 72 (6.6) | 4 (4.0) | <0.001 |
| Endometrial
hyperplasia with atypia, N (%) | 2 (0.4) | 39 (3.6) | 1 (1.0) | 0.001 |
| Leiomyomas, N
(%) | 120 (24.2) | 544 (49.6) | 68 (67.3) | <0.001 |
| Benign ovarian
cysts, N (%) | 36 (7.3) | 153 (14.0) | 17 (16.8) | <0.001 |
| Paraovarian cysts,
N (%) | 41 (8.3) | 169 (15.4) | 22 (21.8) | <0.001 |
| Cervical cancer, N
(%) | 11 (2.2) | 43 (3.9) | 0 (0.0) | 0.034 |
| Endometrial cancer,
N (%) | 8 (1.6) | 102 (9.3) | 4 (4.0) | <0.001 |
| Ovarian cancer, N
(%) | 1 (0.2) | 19 (1.7) | 0 (0.0) | 0.017 |
Among gynecological malignancies, endometrial cancer
was significantly more frequent in patients in group 2 (9.3%),
compared with those in groups 1 (1.6%) or 3 (4.0%) (Table I). However, further analysis with
multinomial logistic regression did not identify adenomyosis as a
factor associated with endometrial cancer (P=0.426).
Discussion
The present study demonstrated that both
endometriosis and adenomyosis can co-exist with various benign,
premalignant or malignant gynecological diseases such as
leiomyomas, endometrial and cervical polyps, and benign ovarian and
paraovarian cysts. Regarding gynecological malignancy, adenomyosis
was more commonly associated with endometrial cancer compared with
cervical or ovarian cancer.
Uterine fibroids are mainly detected in women aged
30-50 years old and are due to the effects of estrogen and
progesterone levels and their metabolism. Under in vitro and
in vivo conditions, uterine fibroids and endometriotic
ectopic cells express aromatase, resulting in increased
concentrations of estrogen in the tissues (13). It is considered that an enlarged
fibroid mass can change the shape, size and location of the uterus
within the pelvic cavity and that this may result in retrograde
menstruation and endometriosis (14,15).
Our previous study confirms that fibroids coexist commonly with
endometriosis in perimenopausal women, whereas adenomyosis is more
prominent in postmenopausal women (16). In patients with leiomyomas, the
reported prevalence of adenomyosis varies from 15-60% in women
undergoing hysterectomy or another gynecological operation.
Furthermore, 70% of women in the general population will acquire
leiomyomas at any given point during their reproductive years, the
majority of which occur between the ages of 30-50 years (6,17).
In the present study, it was confirmed that cases of leiomyomas are
more common in patients with endometriosis and adenomyosis compared
with patients with endometriosis or adenomyosis.
According to the literature, endometrial hyperplasia
and polyps are mostly observed during reproductive years and in
perimenopause and result from hormonal alternations, overexpression
of aromatase, inflammation, gene mutations and monoclonal cell
hyperplasia (18,19). Women with a diagnosis of
pre-existing endometriosis (of at least 12 months), with no other
diagnosed pathology, were studied in a large population-based
observational study. The possible occurrence of endometrial cancer
or hyperplasia was studied with a mean follow-up of 6.4 years.
Women with endometriosis were at greater risk of developing
endometrial hyperplasia (1.85 times) and endometrial cancer (1.35
times) compared with women without endometriosis (20). Regarding polyps, a study by McBean
et al (21) was the first
to identify an association between endometriosis and polyps. A
study by Huang and Xiang (22)
suggests that endometrial polyps may be due to reactive endometrial
hyperplasia due to long-term repetitive mechanical stimulation and
the presence of biological inflammatory factors, such as VEGF and
TGFβ. In a study by Zhang et al (23), it is hypothesized that endometrial
inflammation indicates the common mechanism leading to the
coexistence of endometriosis with endometrial polyps. Additionally,
in the aforementioned meta-analysis it is observed that the risk of
coexistence is prominent in stages 2-4 of endometriosis. However, a
study by Zheng et al (24)
considers that the frequency of coexistence does not differ notably
according to the stage of endometriosis. Endometrial polyps were
found in 46.7% of cases with endometriosis and in 16.5% of the
control group (24). The study by
Kim et al (25), due to a
high risk of co-occurrence, recommends hysteroscopy in infertile
women with endometriosis, even if medical imaging is not suggestive
of endometrial polyps.
In terms of adenomyosis, a retrospective study by
Dayal and Nagrath (26), using 353
adenomyosis histological confirmed specimens, demonstrates the
co-existence of endometrial hyperplasia in 12.46% and uterine
polyps in 7.64% of cases. Additionally, a study by Tetikkurt et
al (27) confirmed 71 cases
with endometrial polyps, 9 cases with hyperplasia and concurrent
presence of endometrial polyps and hyperplasia in 6 women out of a
total of 319 cases with a histopathological diagnosis of
adenomyosis. However, a study by Bergholt et al (28) observes that the presence of
endometrial hyperplasia at the time of operation is the only
variable associated with adenomyosis, as was also demonstrated in
the present study. In a study by Baskin et al, six adult
female monkeys are ovariectomized and receive subcutaneous implants
containing 200 mg estradiol. The subsequent necropsy reveals the
coexistence of endometrial hyperplasia, polyps or adenomyosis;
thus, hyperestrogenism may result in various gynecological
conditions (29). In the present
study, endometrial and cervical polyps were significantly detected
in the patients with adenomyosis and the patients with both
endometriosis and adenomyosis, respectively.
With regards to benign ovarian growth, endometriosis
can coexist with various benign and premalignant ovarian masses
such as serous/mucinous cystadenomas, borderline ovarian tumors and
teratomas (11,30). A retrospective study by Oral et
al (31), using 530 cases with
ovarian cancer and 131 women with borderline ovarian cancer,
reveals that concomitant endometriosis occurs in 7.3% of cases.
However, our previous study recently concludes that further
research is required to investigate the pathway through which
ovarian teratomas are negatively associated with the risk of
developing endometriosis (32). A
previous case series study by Vercellini et al (33) confirms the coexistence of
adenomyosis and ovarian cysts in 21.4% of cases. Moreover, a
previous prospective cross-sectional study, out of 100 hysterectomy
cases, reveals the coexistence of adenomyosis with non-cancerous
ovarian cyst in 25% of cases (34). Our previous study retrospectively
investigates the medical records of 647 patients with adenomyosis
in order to examine a possible association between adenomyosis and
benign, premalignant and malignant gynecological diseases in women
who underwent gynecological surgery. The aforementioned study
demonstrates that adenomyosis co-exists with various gynecological
conditions, such as leiomyomas and endometrial polyps, but it did
not report a prominent association of adenomyosis with other
gynecological pathologies compared with the general population
(17). However, a paraovarian or
paratubal cyst (POC), a mass located in the broad ligament or the
mesosalpinx, has a high prevalence (5-20%) amongst the adnexal
masses. In the present study, benign ovarian cysts and POC were
prominent in group 3, followed by group 2. Due to hormonal
alternations, they are mainly found during reproductive age; thus,
they can coexist with endometriosis or adenomyosis (11,35).
POC can result in disturbed tubal mobility, a condition that may
result in the presence of endometriosis (36,37).
The present study found 101 cases with concurrent
endometriosis and adenomyosis. In 2018, a retrospective study,
including 1,000 cases with a histological confirmation of
endometriosis, concludes that women with endometriosis should
receive counseling regarding the risk of accompanying adenomyosis
(11). Moreover, in 2019, our
previous study retrospectively demonstrated the coexistence of
adenomyosis with endometriosis in 16% of women in perimenopause and
in 32.6% of women in postmenopause (16).
Although rarely, both endometriosis and adenomyosis
may exhibit cancerous behavior or coexist with gynecological
malignancy. Prolonged exposure to estrogens, genetic defects,
environmental factors, immune dysregulation and oxidative stress
are possible pathogenic mechanisms (38-41).
Sampson's criteria are used for both adenomyosis and endometriosis
malignant transformation (42,43).
Neoplasms that develop from endometrial ectopic implants in
endometriosis are divided into two categories; ovarian, which
accounts for 75% of the cases described in the literature and extra
ovarian such as endometrial, cervical and breast cancer (41). Cases of ovarian cancer due to
endometriosis have unique features, such as endometrioid carcinoma
or clear cell carcinoma, the diagnosis is usually made earlier
compared with other types of ovarian cancer and the prognosis is
better (44,45). Although malignant transformation
may occur in 1% of cases with ovarian endometriosis, there is a
strong link between endometriosis and ovarian cancer. In
particular, women with endometriosis have a 4.2-fold higher risk of
ovarian cancer compared with the general population. Therefore, it
is recommended to create screening and prevention programs for this
population in the future (46-48).
The study by Saavalainen et al (49) concludes that the type of
endometriosis a woman has may determine the risk of gynecological
cancer. The risk of ovarian cancer was highest among women with
ovarian endometriosis but low among cases with peritoneal and deep
infiltrating endometriosis (49).
Previously, a large retrospective study reports that endometrial
cancer with concomitant endometriosis is highly associated with
ovarian endometrioid carcinoma (50). Furthermore, epidemiological data
show that the risk of developing endometrioid carcinoma of the
endometrium doubles or even triples in cases with endometriosis
(51,52). However, a study by Poole et
al (53) demonstrates that
there is not a strong association between endometriosis and
endometrial cancer, and this indicates that both conditions follow
a different molecular pathogenesis. Our previous study
retrospectively confirms that women with cervical endometriosis are
at greater risk of developing ovarian, endometrial and cervical
cancer compared with women without endometriosis (54). Another large population-based
historical cohort study confirms that, compared with cases not
acquiring the conditions, patients with adenomyosis are at higher
risk of endometrial and thyroid cancer, while women with
endometriosis are at greater risk of endometrial and ovarian cancer
(55).
However, a large pilot study did not reveal a
notable difference in terms of epidemiologic, clinicopathologic and
prognostic characteristics in patients with endometrial cancer and
adenomyosis compared with patients with only endometrial cancer
(56). In addition, a systematic
review and meta-analysis by Raffone et al concludes that the
pathology of adenomyosis and endometrial cancer are two
unassociated entities (57).
Recently, for the first time, a large retrospective study by Yang
et al (58) describes a
possible protective mechanism of adenomyosis against cervical
cancer invasion, a phenomenon that is also previously discussed in
a study by Machida et al (39) for endometrial cancer. The findings
of the present study indicated endometrial cancer in patients with
adenomyosis; however, further analysis, with multinomial logistic
regression, did not identify adenomyosis as a factor associated
with endometrial cancer.
The present study had a number of limitations.
Firstly, there was a lack of long-term follow-up data, which meant
that distinguishing cases with concurrent gynecological malignancy
or malignant transformation of adenomyosis and/or endometriosis was
limited. Moreover, the retrospective aspect of the present study
was a limitation. However, strengths of the present study include
the histological confirmation of all cases and the large number of
patients that were included in the present study.
In conclusion, the present study demonstrated that
endometriosis, adenomyosis or the concomitant presence of both
conditions may coexist with various benign and malignant
gynecological diseases. Furthermore, patients with adenomyosis may
be associated with endometrial cancer. However, additional
longitudinal studies are required in order to generalize the
findings of the present study in other populations.
Acknowledgements
Not applicable.
Funding
Funding: No funding was received.
Availability of data and materials
The data generated in the present study may be
requested from the corresponding author.
Authors' contributions
MM, IK and CM conceived and designed the present
study and drafted the manuscript. MM, CM, IK and IT obtained the
data. MM, KK, CM, TD, AM, DAS and IK analyzed and interpreted the
data. DAS, KK, TD, AM and IT searched the literature for related
studies to be included in the manuscript. IK, DAS, AM, TD, KK and
IT critically revised the manuscript. All authors read and approved
the final version of the manuscript. MM and IK confirm the
authenticity of all the raw data.
Ethics approval and consent to
participate
The Ethics Committees of Venizeleio General Hospital
(approval no. 124-17-18/12/2019; Heraklion, Greece) and Aristotle
University of Thessaloniki (approval no. 1130-03/07/2020;
Thessaloniki, Greece) approved the protocol of the present
study.
Patient consent for publication
Not applicable.
Competing interests
MM, IT, CM, KK, TD, AM and IK declare that they have
no competing interests. DS is the Managing Editor of the journal,
but had no personal involvement in the reviewing process, or any
influence in terms of adjudicating on the final decision, for this
article.
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