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September 2016 · Volume 5 · Issue 9 Page 3202
International Journal of Reproduction, Contraception, Obstetrics and Gynecology
Chiantera V et al. Int J Reprod Contracept Obstet Gynecol. 2016 Sept;5(9):3202-3207
www.ijrcog.org
pISSN 2320-1770 | eISSN 2320-1789
Case Report
An atypical manifestation of inguinal endometriosis in the extra pelvic
part of the round ligament: a case report
Vito Chiantera1,2, Elene Abesadze2, Mohamed Gamal Ibrahim3,4, Anna Maria Dückelmann4,
Sylvia Mechsner2*
INTRODUCTION
Endometriosis is a common disease affecting millions of
women during the reproductive age.1,2 The typical
localisation of endometriosis is the intra-abdominal
cavity, with manifestation of endometriotic lesions in the
pelvis affecting genital organs (so-called endometriosis
genitalis externa and interna). Nevertheless, there are
extra-genital manifestations in 15% of the cases; for
example, in the bowel or the diaphragm.26,34 Most of
those lesions appear intra-abdominally and only 0.5-1%
extra-abdominally. There are descriptions of
endometriosis in scars after surgery, with secondary
dissemination of endometriotic tissue or primary and
secondary development of endometriosis in the
1Department of Gynecology, (UNIPA), University of Palermo, Palermo, Italy
2Charité University Hospital, Endometriosis Research Centre, Department of Gynaecology, Campus Benjamin
Franklin, Berlin, Germany
3The University of Münster, Clinic for obstetrics and gynecology, UKM Kinderwunschzentrum, Münster, Germany
4Charité University Hospital, Department of Gynaecology, Campus Benjamin Franklin, Berlin, Germany
Received: 28 June 2016
Accepted: 05 August 2016
*Correspondence:
Dr. Sylvia Mechsner,
E-mail: sylvia.mechsner@charite.de
Copyright: © the author(s), publisher and licensee Medip Academy. This is an open-access article distributed under
the terms of the Creative Commons Attribution Non-Commercial License, which permits unrestricted non-commercial
use, distribution, and reproduction in any medium, provided the original work is properly cited.
ABSTRACT
Establishing the diagnostic and surgical management of the inguinal Endometriosis, with further investigation of the
biological character. The imaging findings of CT and PET-CT, biopsy, ultrasound, open surgery of the inguinal
region with intraoperative cryosection, confirmation and evaluation of tissue infiltration by endometriosis,
laparoscopic removal of all endometriotic lesions, reconstruction of the groin. Based on the history of the 29-year-old
patient, suffering from a painful growing induration of the inguinal region. Immunohistochemistry performed, in
order to analyze the character of the inguinal endometriosis. CT, PET-CT and biopsy did not confirm the diagnosis of
endometriosis. Considering, the progressive symptoms of the patient, was performed the surgical intervention. Open
surgery of the inguinal region, with a preparation and separation of the groin fibrotic mass lead to the finding of an
affected extra-peritoneal portion of the round ligament. Intraoperative cryosection confirmed endometriosis.
Simultaneous laparoscopy showed peritoneal endometriosis (rASRM I) and an alteration of the inner round ligament,
involving the inner inguinal channel in this process. All endometriotic lesions were removed and the inguinal region
reconstructed. The immunohistochemical staining gave evidence of the endometriotic tissue, surrounded by smooth
muscle metaplasia. We consider that, reporting this rare case of endometriosis, based on a case report and a literature
review, affecting intra and extra peritoneal portion of the round ligament, is an important aid to avoid a wrong
diagnosis and method of therapy in future. Our data demonstrated the fully recovery of the patient, after surgical
treatment, reporting symptom-free status.
Keywords:
Extra genital endometriosis, Endometriosis, Affecting the intra and extra-peritoneal portion of the round
ligament, Inguinal endometriosis, Smooth muscle metaplasia
DOI: http://dx.doi.org/10.18203/2320-1770.ijrcog20163012
Chiantera V et al. Int J Reprod Contracept Obstet Gynecol. 2016 Sept;5(9):3202-3207
International Journal of Reproduction, Contraception, Obstetrics and Gynecology Volume 5 · Issue 9 Page 3203
umbilicus, in the lung, brain, or the inguinal
region.1,13,16,18,21,29 Remarkably, the establishment of
endometriosis in the extra-peritoneal part of the round
ligament was found to be 0.3-0.6% among the extra-
abdominal manifestation.1 In general, it seems to affect
only 0.07% of the patients with endometriosis.30 Inguinal
endometriosis is established rarely and so far, there
appears to be no evident based strategy available for
diagnostic or the therapeutic management.
This study will present the evidence of inguinal mass,
representing the methods of diagnosis and therapeutic
treatment.
CASE HISTORY
A 29 year-old nulliparous woman was presented to our
clinic, suffering from the swelling of a right inguinal area
over a two-year period. The complaints used to increase
cyclically, simultaneously to the menstrual bleeding. The
induration was very painful, especially during the
menstruation. Patient had regular menstrual cycle,
without endometriosis-related symptoms, like
dysmenorrhoea, pelvic pain, dyschezie or dyspareunia.
No surgical treatment was performed previously, as well.
Diagnostic findings
During medical examination, palpation showed a 2 x 2
cm diameter tumour disclosed in the right inguinal area,
laterally on the symphysis pubis. As concerning
underlying structures, they were relatively fixed and
immobile. The palpation was very painful, no evidence of
swelling in the contralateral side. Significant was, that the
gynaecological examination revealed no pathology in
pelvic area. Pelvic ultrasound was unremarkable, but an
inguinal ultrasound revealed a low echoic mass of more
than 2 cm diameter (Figure 1).
Within the medical history of the patient we could see,
that orthopaedics, in order to clarify and diagnose the
uncommon condition, performed a fine needle biopsy of
the inguinal mass. Histology revealed fibrosis. Further
imaging with CT scan and PET-CT gave no affect in
clarification of the uncommon mass.
Surgery
According to these complaints and findings, the patient
was considered to undergo an excision of the inguinal
mass, along with a laparoscopy. First step was an
inguinal excision, which revealed the 2 x 2 cm diameter
mass, attached to the extra-peritoneal part of the round
ligament, superolaterally to the right pubic tubercle. The
excised specimen sent to pathology indicated
endometriosis. The further preparation processed in the
direction of the deep inguinal ring and new frozen
sections justified endometriosis repeatedly. Subsequently,
the inguinal region was closed temporarily.
Second part of the surgery was performed
laparoscopically. Endometriosis was compatible to the
stage rASRM I. The intra-abdominal part of the round
ligament was infiltrated with endometriotic lesions,
therefore completely retracted into the right inguinal
channel; likewise, the uterus was shifted to the right
pelvic wall. On the left ovarian fossa and Sacrouterin
ligament were represented typical black cicatricle
endometriotic lesions, which were excised subsequently.
Considering wide infiltration approximately was resected
one-third of the abdominal part of the round ligament.
For further manipulation, laparoscopy and open surgery
have been combined, namely performed simultaneously.
The residual part of the round ligament, proximal to the
uterus, was embed medially to the superficial inguinal
ring and through the open groin connected to the superior
wall of the inguinal channel, followed by the fixation at
the transversal fascia.
As a final step, an inguinal channel was reconstructed for
a hernia prophylaxis, with a Vicryl mesh, followed by
consecutive closure of the epidermis the last laparoscopic
imaging showed mobile uterus, slightly shifted to the
dextra position. Essentially related to the normal
anatomic topography (Figure 2A-I).
Immunohistochemistry
Tissue preparation: All excised lesions were directly
fixed in 4% buffered formalin for 12h and then embedded
in paraffin. Serial sections (1-2 µm thick) were used for
haematoxylin-eosin staining and immunohistochemistry.
After deparaffinization in xylene (2 x 5 min at room
temperature) and rehydration (10 min in acetone and
acetone/Tris-buffered saline (TBS)) at a 1:1 ratio,
likewise only in TBS (at room temperature), the heat-
induced epitope retrieval (HIER) procedure was
performed by heating the specimens in citrate buffer (0.1
M citric acid and 0.1 M sodium citrate, pH 6.0 at 700 W
in a microwave oven for 17 min). Afterwards sections
were blocked with 10% foetal calf serum (FCS) for 30
min at room temperature.
Oestrogen receptor (ER) and progesterone receptor (PR)
were performed using the primary antibodies against ER
(clone 1D5, dilution 1:40) and PR (clone 1A6, 1:100)
obtained from DakoCytomation, Glostrup, Denmark. The
alkaline-phosphatase-anti-alkaline phosphatase complex
(APAAP) method was used for detection and analysed by
Fast Red as the chromogen.
Smooth muscle Actin (smActin) and desmin analysis:
The sections were incubated for 1 h at room temperature
with the monoclonal mouse anti-smActin or monoclonal
mouse anti-desmin antibody (dilution 1:50, Dako,
Hamburg, Germany), followed by incubation with a Cy2-
conjugated donkey anti-mouse antibody (dilution 1:100,
Dianova, Hamburg, Germany) for 45 min.
Chiantera V et al. Int J Reprod Contracept Obstet Gynecol. 2016 Sept;5(9):3202-3207
International Journal of Reproduction, Contraception, Obstetrics and Gynecology Volume 5 · Issue 9 Page 3204
There was used the uterine tissue as a positive control.
All negative control sections were processed by omitting
the primary antibody. Staining was detected using a
radiophoto microscope (Carl Zeiss, Göttingen, Germany).
Pictures were taken in different magnifications (40, 100
or 1000x) and further processed using the Adobe
Photoshop (Adobe Systems, Unterschleissheim,
Germany).
In order to investigate the biological character of inguinal
endometriosis, there was performed immune
histochemical analysis against ER and PR, likewise
smooth muscle differential markers: smooth muscle actin
and desmin.
Figure 1: Trans abdominal ultrasonography of right
inguinal region. Two solid hypoechoic round lesion of
2x1, 4 cm and 0, 9x0,7 cm, with irregular morphology
and blurred margins, which are located in the lower
right anterior abdominal wall.
The immune histochemical staining revealed typical
endometriotic lesions (epithelial and stromal cells)
(Figure 3). A strong expression of oestrogen and
progesterone receptors were detected in lesions (Figure
3A and B). Furthermore, the identification of the smooth
muscle actin, likewise desmin-positive cells in the
endometriotic associated surrounding tissue proves
evidence of smooth muscle metaplasia (Figure 3C and
D). Nonetheless, there was a divergence, between the
expression of smooth muscle actin (marker for
undifferentiated smooth muscle cells) and desmin (a
marker molecule for differentiated smooth muscle cells),
which is only expressed in mature smooth muscle cells.
Postoperative follow-up and management
After two-month postoperative period, the patient was
presented in our clinic, completely free from complaints:
no further cyclical painful irritations in the inguinal
region. Considering, patient’s actual seeking fertility,
shortly after discharge, no adjuvant hormonal treatment
was recommended.
DISCUSSION
Until today, approximately 100 cases of the round
ligament endometriosis are reported and further 150 case
reports, concerning inguinal endometriosis. Cullen
described the first case of ‘Adenomyom’ of the round
ligament in 1896. Throughout the following years,
eventually 20 similar cases were described, analysed and
interpreted by Robert Meyer.20 Although this
phenomenon had already been described in many
instances, inguinal endometriosis still stays a rare form of
extra-genital endometriosis, consequently standardized
treatment options are missing.
Figure 2 (A) (B): Laparoscopic part of the operation:
Status after inguinal excision, processed in the
direction of the deep inguinal ring, removal of 2 x 2
cm diameter mass, attached to the extra-peritoneal
part of the round ligament. Resection of the round
ligament, approximately one-third of the abdominal
part, considering the wide infiltration. (C)(D):
Combination of the laparoscopy and open surgery.
(E)(F): Fastening the residual part of the round
ligament, proximal to the uterus, medially to the
superficial inguinal ring and going through the open
groin, connected to the superior wall of the inguinal
channel, followed by the fixation at the transversal
fascia. (G) The last laparoscopic imaging showing
mobile uterus, slightly shifted to the dextra position,
related to the normal anatomic topography. (H)
Reconstruction of the inguinal channel as a hernia
prophylaxis, with a Vicryl mesh. (I) Followed by
consecutive closure of the epidermis.
A
B
C
F
E
D
I
H
G
Chiantera V et al. Int J Reprod Contracept Obstet Gynecol. 2016 Sept;5(9):3202-3207
International Journal of Reproduction, Contraception, Obstetrics and Gynecology Volume 5 · Issue 9 Page 3205
Figure 3: Immunohistochemical characterization of
the right inguinal endometriosis. When endometriotic
glands (arrow) and stroma express (A) oestrogen
receptor, only glandular epithelium expresses (B)
progesterone receptors. Smooth muscle metaplasia is
evident as endometriotic stromal cells express (C)
alpha smooth muscle actin. Furthermore, some
stroma cells are seen expressing (D) desmin as a
marker for differentiated smooth muscle cells; X200.
Interestingly, a retrospective analysis of women
undergoing laparoscopy for treatment of deep infiltrating
endometriosis (DIE) demonstrated a prevalence of
endometriosis of the round ligament of 13.8%.7 They still
removed the inner part of the round ligament, even for
cases of macroscopic alterations; such as shortening,
deviation or thickening for a histopathological analysis.
In the light of this, such an endometriosis manifestation
seems to be underestimated, and a rigorous evaluation of
the structure must now become part of the routine
surgical treatment of patients with endometriosis.7
The typical history of cyclical symptoms is the main
indication of endometriosis and leads to the correct
diagnosis. Patients were suffering from cyclical inguinal
swelling and catamenial pain. Sometimes the pain
changed into the permanent pain. CT and PET-CT
imaging, like wise fine needle biopsy resulted no
significant impact on diagnostic evaluation. Based on
other works, inguinal ultrasound appeared to be the most
profitable way to detect an echogen nodule, therefore
provides better opportunity to monitor the lesion.4,11
Furthermore, this method allows a differentiation from
other inguinal pathological findings, alike inguinal hernia
or enlarged lymph nodes. Additionally, in some selected
cases, magnet resonance imaging has been presented to
be particularly effective method in diagnosis of the extra-
peritoneal endometriosis.4,14,17,33 However, MRI is not
obligatory when the lesion is previously detectable by the
ultrasound. As a final consensus, it requires a surgical
excision and histological examination to give the
definitive diagnosis. The surgical treatment should
involve an adequate excision of the intra and extra-
peritoneal part of the round ligament to avoid disease
recurrence.10
It is remarkable, that in most cases of the inguinal
endometriosis extra-peritoneal part of the round ligament
is affected.6 Rarely, endometriosis also have been
observed in inguinal hernial sacs in lymph nodes, in canal
of Nuck or in regions associated with femoral vessels and
femoral hernia.2,3,24,27,28,32
Subsequent to extra-peritoneal manifestations of
endometriosis, a simultaneous laparoscopy is strongly
recommended, in order to exclude further expression of
intraperitoneal endometriosis. This case, based on the
example of our patient, is clear evidence of this theory.
Postoperative results were remarkably excellent. Patient
was free from previous complaints and from further
endometriosis-associated symptoms. The quality of life
was apparently improved. Generally, inguinal
endometriosis usually negate further endometriosis-
associated symptoms like dysmenorrhoea or pelvic pain.
In order to improve and investigate new methods of
treatment and be able to remove endometriotic lesions
totally, we had to find the right plain of endometriosis-
free tissue within the round ligament. Therefore,
intraoperatively frozen sections of endometriotic lesions
were sent to the pathology to explore the infiltration, in
order to come up with the right target. This concept
improves the possibility to excise the affected tissue
completely and avoid further recurrence.
The pathway, mentioned above, is the direct extension
along the round ligament from the pre-existing
endometriosis in the pelvis.6 In our case, infiltration of
the intraabdominal part was accompanying the round
ligament into the inguinal canal, involving the extra-
peritoneal part. In 32% of the described cases, infiltration
affected an inguinal hernia, occasionally, even after
excluding the intraperitoneal endometriosis
laparoscopically.6,25 Nonetheless, in previous six cases
the initial tentative diagnosis of inguinal hernia were
reported, the confirmation of this diagnosis throughout
the surgery was missing.5 In all of these women, the
endometriotic lesions were located in the extra-peritoneal
portion of the round ligament, without any apparent
spatial communication with the pelvis. Consequently, the
statement of Meyer in 1930, about the embryological
development of the round ligament, can be considered
very interesting. It declares that the second pathway is a
reason of endometriosis dissemination, according to the
lymphatic spread. Recently Moore, J. G have suggested
the theory considering that retroperitoneal endometriotic
lesions are probably associated with a lymphatic spread
of endometrial cells.23 This could be lymphatic vessels,
which have originated in the uterus and run along the
round ligament.15 Accordingly, this could be a possible
explanation of endometriosis in the extra-peritoneal part
of the round ligament, whereas the intraperitoneal
endometriosisis is not emerged. In case of intraperitoneal
endometriosis, a crossing of the endometriotic cells
through the peritoneal mesothelium into the lymphatic
and venous system of the round ligament seems to be
possible.10 Although it has been confirmed that a
Chiantera V et al. Int J Reprod Contracept Obstet Gynecol. 2016 Sept;5(9):3202-3207
International Journal of Reproduction, Contraception, Obstetrics and Gynecology Volume 5 · Issue 9 Page 3206
lymphatic spread in retroperitoneal deep infiltrating
endometriosis is in fact a frequent phenomenon, the
inguinal endometriosis is not typically localised in the
inguinal lymph nodes but rather in the round ligament.19
In the literature, it has also been reported that in 90% of
the cases preferred manifestation of inguinal
endometriosis involves the right groin.6 Why this
affection involves predominantly the right side of the
groin is still undefinable. Furthermore, usually we inspect
more right sided affection of the diaphragmatic
endometriosis. The intraperitoneal circulation of the fluid
could explain this, assuming that endometriotic cells
(from transtubal flow or pelvic endometriosis) remain in
the region of the right round ligament for a longer period,
than in the left side. In addition, the sigmoid seems to
protect the left round ligament. Therefore, the persistence
of such cells in the right deep inguinal ring and the
inferior epigastric vessels could favour the passage of
these cells across the mesothelium into the lymph system
of the right round ligament resulting in a consecutive
development of endometriosis.5
Based on the long-term follow-up, there were observed
late complications - the malignant transformation under
oestrogen replacement therapy, especially in case of
hysterectomy, while Patients were taking oestrogen
replacement monotherapy for the menopausal
syndrome.9,22 Regarding such complications, it is very
important to remove the inguinal mass totally.
For further analysis, were performed the biological
properties of this inguinal endometriosis,
immunohistochemical examinations. Absolutely all
epithelial and stromal cells express an oestrogen and
progesterone receptor, proving a high hormonal
sensitivity of the endometriotic lesion. Besides the
hormonal sensitivity, there is also a high COX-2
expression, which reflects the high activity of inguinal
lesions.31 Another famous factor, associated with the
activity of endometriotic lesions is the metaplasia
process.18 In this context, we analyzed character of the
rarely found inguinal endometriotic lesion.
However, in the endometriotic lesion was a high
expression of smooth muscle actin, a general marker
molecule for smooth muscle cells and myofibroblasts,
indicating a high content of smooth muscle cells.18 In
serial sections, was expressed desmin (a marker molecule
for differentiated smooth muscle cells) in corresponding
with smooth muscle cells (Figure 3). However, on
another hand, discrepancy was detected, between the
expression of smooth muscle actin and desmin, expressed
only in mature smooth muscle cells. This discovery
indicates, that the smooth muscle cells were of new origin
in the differentiation process.8,18
In summary, transvaginal and inguinal ultrasound was the
method of choice to investigate the extension of an
inguinal endometriosis. The laparoscopy should be
performed, in order to exclude or treat a pelvic
endometriosis. Recurrence is definitely rare after a
complete and adequate surgical treatment (including the
intra and extra-peritoneal part of the round ligament).
However, in context with the biological properties of the
inguinal endometriotic lesion, a postoperative endocrine
treatment can be discussed for recurrence prevention or in
a case of recurrent disease.5
CONCLUSION
We consider that, reporting this rare case of
endometriosis, based on a case report and a literature
review, affecting intra and extra peritoneal portion of the
round ligament, is an important aid to avoid a wrong
diagnosis and method of therapy in future. Our data
demonstrated the fully recovery of the patient, after
surgical treatment, reporting symptom-free status.
Funding: No funding sources
Conflict of interest: None declared
Ethical approval: The study was approved by the IRB of
Charité ethics committee (EA)
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Cite this article as: Chiantera V, Abesadze E,
Ibrahim MG, Dückelmann AM, Mechsner S. An
atypical manifestation of inguinal endometriosis in
the extra pelvic part of the round ligament: a case
report. Int J Reprod Contracept Obstet Gynecol
2016;5:3202-7.
