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Human Reproduction Open, pp. 1–25, 2020
doi:10.1093/hropen/hoaa002
ESHRE PAGES
Recommendations for the surgical
treatment of endometriosis. Part 2:
deep endometriosis†‡¶
Working group of ESGE, ESHRE, and WES, Joerg Keckstein 1,*,
Christian M. Becker2, Michel Canis3,AnisFeki
4, Grigoris F. Grimbizis5,
Lone Hummelshoj6, Michelle Nisolle7, Horace Roman8,9,
Ertan Saridogan10, Vasilios Tanos11, Carla Tomassetti12,
Uwe A. Ulrich13, Nathalie Vermeulen 14, and
Rudy Leon De Wilde15
1Endometriosis Centre Dres. Keckstein, Richard-Wagner Strasse 18, 9500 Villach, Austria 2Nueld Department of Obstetrics and
Gynaecology, University of Oxford, John Radclie Hospital Womens Centre, OX3 9DU Oxford, UK 3Department of Gynaecological
Surgery, University Clermont Auvergne CHU, Estaing 1 Place Lucie Aubrac, 63000 Clermont-Ferrand, France 4Department of Obstetrics
and Gynecology, HFR Fribourg Hopital cantonal, 1708 Fribourg, Switzerland 51st Department of Obstetrics and Gynecology, Medical
School Aristotle University of Thessaloniki, Tsimiski 51 Street, 54623 Thessaloniki, Greece 6World Endometriosis Society, London N1 3JS,
UK 7Hôpital de la Citadelle, Department of Obstetrics & Gynecology, 4000 Liège, Belgium 8Endometriosis Centre, Clinic Tivoli-Ducos,
Bordeaux, France 9Department of Obstetrics and Gynaecology, Aarhus University Hospital, Aarhus, Denmark 10Reproductive Medicine
Unit, Elizabeth Garrett Anderson Wing Institute for Women’s Health, University College Hospital, NW1 2BU London, UK 11Department
of Obstetrics and Gynecology, Aretaeio Hospital, 2024 Nicosia, Cyprus 12Department of Obstetrics and Gynaecology, Leuven University
Fertility Centre, University Hospital Leuven, 3000 Leuven, Belgium 13 Department of Obstetrics and Gynaecology, Martin Luther Hospital,
14193 Berlin, Germany 14 ESHRE, Central oce - Meerstraat 60, BE 1852 Grimbergen, Belgium 15 University Hospital for Gynecology, Carl
von Ossietzky Universitat Oldenburg, 26129 Oldenburg, Germany
*Correspondence address. Endometriosis Centre Dres. Keckstein Villach, Richard-Wagner Strasse 18, 9500 Villach, Austria.
E-mail: joerg@keckstein.at; guidelines@eshre.eu https://orcid.org/0000-0002-3943-3300
Submitted on November 27, 2019; resubmitted on November 27, 2019; editorial decision on January 13, 2020
STUDY QUESTION: How should surgery for endometriosis be performed?
SUMMARY ANSWER: This document provides recommendations covering technical aspects of dierent methods of surgery for deep
endometriosis in women of reproductive age.
WHAT IS KNOWN ALREADY: Endometriosis is highly prevalent and often associated with severe symptoms. Yet compared to equally
prevalent conditions, it is poorly understood and a challenge to manage. Previously published guidelines have provided recommendations for
(surgical) treatment of deep endometriosis, based on the best available evidence, but without technical information and details on how to best
perform such treatment in order to be eective and safe.
STUDY DESIGN, SIZE, DURATION: A working group of the European Society for Gynaecological Endoscopy (ESGE), ESHRE and the
World Endometriosis Society (WES) collaborated on writing recommendations on the practical aspects of surgery for treatment of deep
endometriosis.
PARTICIPANTS/MATERIALS, SETTING, METHODS: This document focused on surgery for deep endometriosis and is complemen-
tary to a previous document in this series focusing on endometrioma surgery.
MAIN RESULTS AND THE ROLE OF CHANCE: The document presents general recommendations for surgery for deep endometriosis,
starting from preoperative assessments and first steps of surgery. Dierent approaches for surgical treatment are discussed and are respective
of location and extent of disease; uterosacral ligaments and rectovaginal septum with or without involvement of the rectum, urinary tract or
extrapelvic endometriosis. In addition, recommendations are provided on the treatment of frozen pelvis and on hysterectomy as a treatment
for deep endometriosis.
LIMITATIONS, REASONS FOR CAUTION: Owing to the limited evidence available, recommendations are mostly based on clinical
expertise. Where available, references of relevant studies were added.
WIDER IMPLICATIONS OF THE FINDINGS: These recommendations complement previous guidelines on management of endometrio-
sis and the recommendations for surgical treatment of ovarian endometrioma.
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2Working group of ESGE, ESHRE and WES et al.
STUDY FUNDING/COMPETING INTEREST(S): The meetings of the working group were funded by ESGE, ESHRE and WES. Dr
Roman reports personal fees from ETHICON, PLASMASURGICAL, OLYMPUS and NORDIC PHARMA, outside the submitted work; Dr
Becker reports grants from Bayer AG, Volition Rx, MDNA Life Sciences and Roche Diagnostics Inc. and other relationships or activities from
AbbVie Inc., and Myriad Inc, during the conduct of the study; Dr Tomassetti reports non-financial support from ESHRE, during the conduct
of the study; and non-financial support and other were from Lumenis, Gedeon-Richter, Ferring Pharmaceuticals and Merck SA, outside the
submitted work. The other authors had nothing to disclose.
TRIAL REGISTRATION NUMBER: na
Key words: endometriosis / laparoscopy / surgery / deep endometriosis / extrapelvic / frozen pelvis / hysterectomy / good practice
recommendations
†ESHRE Pages content is not externally peer reviewed. The manuscript has been approved by the Executive Committee of ESHRE.
‡This paper has been approved by the Executive Committees of the ESGE and WES.
¶This article has been co-published with permission in HROpen and FACTS, VIEWS & VISION in Obgyn.
WHAT DOES THIS MEAN FOR PATIENTS?
This paper was produced by a European working group looking at the dierent types of surgery for endometriosis, a common condition where
tissue, which is similar to the lining of the womb, is found elsewhere in the body. The working group looked specifically at how best to treat a
type of the disease, named deep endometriosis. Drug therapies may be used to treat endometriosis, but when endometriomas are found and
need treatment, surgery is often used. There are risks associated with surgery, and especially repeated surgery, including adhesions.
The working group looked at the main types of surgery which are used to treat deep endometriosis, focussing on the dierent locations in
the pelvis where the lesions can be found. The paper discusses in detail how dierent types of surgery should be performed, taking potential
risks into consideration, and stresses that careful planning and involving dierent surgeons specialising in bowel or bladder is essential to ensure
the best outcomes.
Introduction
Endometriosis is highly prevalent, yet compared to equally prevalent
conditions it is poorly understood and a challenge to manage. It has
been estimated that more than 176 million women worldwide suer
from endometriosis and its associated symptoms including infertility,
cyclical and non-cyclical abdominal pain, dysmenorrhea, dyspareunia,
dysuria and dyschezia (Adamson et al., 2010). It is generally accepted
that no correlation exists between the severity of such pain symptoms
and the extent of disease as characterised by the most commonly used
revised American Fertility Society/American Society for Reproductive
Medicine (rASRM) staging system (Vercellini et al., 2007); however,
with the use of other classification systems, such as ENZIAN, a correla-
tion with pain symptoms may exist (Montanari et al., 2019). It has been
shown that women with surgically verified endometriosis reported the
highest pain symptoms compared to women with other gynaecologic
pathology (Schliep et al., 2015). However, the correlation between
location and depth of endometriotic lesions and pain location is poor
(Hsu et al., 2011). Therefore, it could be relevant to include histology
when classifying the disease (Bouquet de Joliniere et al., 2019).
Endometriosis may be categorized into three entities: peritoneal
endometriosis, ovarian endometriotic cysts (endometrioma) and deep
endometriosis (DE) (previously known as deep infiltrating endometrio-
sis or DIE) (Nisolle and Donnez, 1997). In addition to medical therapy
with hormones and analgesics, surgery has been shown to significantly
improve endometriosis-associated symptoms (Duy et al., 2014;Byrne
et al., 2018). However, like medical intervention, surgery is not always
successful and is also associated with clinically relevant risks (Chapron
et al., 1998;Becker et al., 2017). Treatment failure can be partially
attributed to the heterogeneity of endometriosis and, in the case of
surgical intervention, is directly correlated with factors such as surgical
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experience, the complexity of each case and anatomical locations of
the disease.
A working group comprising members of the European Society
for Gynaecological Endoscopy (ESGE), ESHRE and the World
Endometriosis Society (WES) has set out to produce a series of
recommendations on the practical aspects of endometriosis surgery.
The first part of this series on endometrioma surgery was published
in 2017 (Working group of ESGE-ESHRE and WES et al., 2017).
This second part focuses on the surgical management of DE. After
general considerations, such as definition and anatomical specifications,
this publication concentrates on recommendations related to pre-
operative management and surgical technique respective of location
and extent of disease. Choices of dierent treatment options for
DE and the selection of patients that would benefit from surgery are
beyond the scope of this document. Conservative treatment, including
pain management, has to be considered thoroughly.
Materials and Methods
Previously published guidelines have provided recommendations on
the management of endometriosis, based on the best available evi-
dence (Johnson et al., 2013;Dunselman et al., 2014;Ulrich et al., 2014).
However, these guidelines were not intended to provide recommen-
dations on the technical details of surgical procedures.
Due to the scarcity of evidence on these technical details, the
current recommendations are primarily based on expert opinion on
best clinical practice. Studies and trials of these approaches have been
cited in the text, when available.
In addition to the recommendations, the working group has set
up a web platform with videos on the dierent options available for
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Surgical treatment of deep endometriosis 3
surgery of DE. The web platform is accessible through the following
link (https://www.eshre.eu/surendo) or via the ESGE, ESHRE or WES
websites.
(Results) Good Practice
Recommendations
Deep Endometriosis
Definition of DE
Rokitansky was probably the first to describe DE in the uterus (Roki-
tansky C., 1860;Hudelist et al., 2009;Tsui et al., 2015). Thomas
Cullen later described DE, although he described it as adenomyosis
of the round ligament (Cullen, 1896). In modern times, using laser
excision, Martin et al. described in a landmark study that the lesions in
approximately one-third of the women were penetrating more than
4 mm under the peritoneal surface (Martin et al., 1989). Cornillie
et al. then investigated the activity of endometriosis tissue at dierent
sub-peritoneal depths and suggested that DE was invasive (Cornillie
et al., 1990); however, clear evidence of infiltration is still missing.
Histologically, the investigators found active glandular and stromal
tissue as defined by the presence of mitoses and gl ycogen accumulation
5 mm below the peritoneal surface. Fibromuscular hyperplasia, cystic
transformation of the glands and perivascular mononuclear inflam-
matory cells were noted. Other definitions of DE have been used
related to the location of the disease including the involvement of
bowel, bladder, ureter, vagina, parametrium (cardinal ligament) and
diaphragm (Keckstein, 2017). Another definition by Bazot described
DE as a fibrous/muscular infiltration of organs and anatomical struc-
tures containing endometrial tissue below the peritoneum, regardless
of the depth of infiltration (Bazot and Darai, 2017).
For the purpose of this publication, and the surgical treatment of
the disease, the working group is defining DE as the involvement of
endometrial-like tissue with a depth of more than 5 mm (Koninckx
et al., 2012).
Morphological considerations
Infiltration of the abdominal and pelvic parietal peritoneum by
endometriotic tissue can lead to involvement of retroperitoneal
structures depending on the location and depth of the endometriotic
nodule. DE is often associated with fibrotic changes. Thus, retraction
of surrounding structures is common, and this is to be considered
during pre-operative and intra-operative planning and assessment of
the optimal surgical approach.
Surgeons must have a significant knowledge of pelvic anatomy in
order to have an approach to a grossly distorted surgical field. Thus,
pelvic anatomical landmarks represent essential points of reference to
start procedures such as mobilization of the pelvic viscera, wide peri-
toneal resections or the identification of further anatomical structures
to be preserved, such as bowel, ureter, vessels and parasympathetic
and orthosympathetic pelvic neural fibres in nerve-sparing procedures
(Ceccaroni et al., 2018). The preparation or dissection of specific
anatomical spaces (Latzko, Okabayashi, Yabuki), which have been
described by various authors, helps to identify these landmarks in order
to facilitate a complete and safe excision of the deep lesions (Yabuki
et al., 2005;Ceccaroni et al., 2018;Hudelist et al., 2018;Puntambekar
and Manchanda, 2018).
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The abdominal (upper third) part of the retroperitoneally located
ureter follows the ventral side of the psoas muscle. Entering the pelvis,
the ureter crosses dorsally to the ovarian artery and vein and then
ventrally to either the common (left side) or external (right side)
iliac artery. It then courses ventrally directly below the peritoneum
of the pelvic sidewall and runs antero-laterally from the uterosacral
ligament. Before entering the urinary bladder, the ureter crosses the
uterine artery caudally. Ureteral blood supply originates from the
renal artery (upper third), ovarian artery and abdominal aorta (middle
third) as well as the internal iliac arteries and smaller vessels (lower
third) and is usually located at the lateral side of the ureter. Plenty of
anastomoses of these blood vessels exist within the ureteral adventitia
where also the ureteral nerve plexus can be found. Anatomic variations
are common; for example, the prevalence of a duplex ureter has been
described in 0.5–6% of cases and has to be taken into consideration
when removing or ablating endometriotic lesions or nodules in the
pelvis (Phillips et al., 1987). In addition, the normal anatomical position
of the ureter can be altered significantly in the presence of DE, such
as medial displacement due to surrounding fibrosis and/or infiltration.
Ureteral stricture or complete obstruction may lead to hydro-ureter
and hydronephrosis (this is further discussed in the section on urinary
tract endometriosis).
The bilateral inferior hypogastric plexus supplies the pelvic organs,
such as the rectum, bladder and cervix, with sympathetic and parasym-
pathetic nerve fibres, and receives visceral aerent fibres. The sympa-
thetic nerve fibres come from the superior hypogastric plexus (L3–L4)
via the hypogastric nerve, which follows the common and the internal
iliac artery: they are found in the pararectal space medial and dorsal
to the ureter. The parasympathetic fibres originate from the pelvic and
sacral splanchnic nerves (S2–S4).
The intraperitoneally located sigmoid and the retroperitoneal
rectum are often involved in DE. Endometriotic nodules in the
recto-vaginal septum result in adherence of the recto-sigmoid to
the lower dorsal side of the uterus, cervix and vagina. The large
bowel wall consists of multiple layers, all of which can be invaded
by endometriotic tissue (Fig. 1). The sigmoid colon receives its blood
supply from multiple branches of the inferior mesenteric artery.
There exist anastomoses between the sigmoid arteries and the
superior rectal (superior haemorrhoidal) artery, itself a branch of the
inferior mesenteric artery, supplying the rectum and creating further
anastomoses with the middle rectal (middle haemorrhoidal) artery, a
branch of the inferior vesical artery which originates from the internal
iliac artery. Distally, the rectum receives some blood supply from the
inferior rectal (inferior haemorrhoidal) artery, which mainly supplies
the anal canal originating from the internal pudendal artery, another
branch of the internal iliac artery. Again, anastomoses exist between
the middle and inferior rectal arteries.
Like any subperitoneal (deep) endometriosis, nodules in the vesico-
uterine pouch (ventral cul-de-sac) can involve or invade surrounding
structures, such as the underlying urinary bladder, eventually displacing
the round ligaments medially. The bladder wall consists of mucosa, a
submucosal layer (lamina propria) containing blood vessels and nerve
fibres, a muscularis propria (detrusor muscle) consisting of an inner
and outer longitudinal and a middle circular muscle layer, and either a
serosal layer or adventitia. The ureters, after passing about 1 to 2 cm
laterally to the uterine cervix and coursing ventral to the lateral border
of the vagina, enter the bladder postero-laterally in an oblique angle.
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4Working group of ESGE, ESHRE and WES et al.
Figure 1 The layers of the recto-sigmoid colon,as graphical representation (upper figure),in eosin-stained healthy recto-sigmoid
colon (lower left) and eosin-stained endometriosis-aected recto-sigmoid colon (lower right).1 serosa (sigmoid) or Adventitia (rectum);
2 subserosa; 3 tunica muscularis (outer longitudinal layer, inner circular layer) with plexus myentericus in between; 4 submucosa with plexus submucosus,
blood, and lymphatic vessels; 5 mucosa.
The urinary bladder receives its blood supply from the superior, middle
and inferior vesical arteries (branches of the internal iliac artery) as well
as the vaginal (branch of uterine artery) artery (see also Fig. 2).
Classification
The most commonly used classification system of endometriosis, the
rASRM classification, does not provide sucient information for DE;
correlation with symptoms is poor, and it does not predict surgical di-
culty level or outcome (Johnson et al., 2017). Several systems classifying
and documenting the extent of the DE have been developed, includ-
ing the ENZIAN classification (Keckstein et al., 2003b;Tuttlies et al.,
2005;Stiftung Endometriose Forschung (Foundation for Endometriosis
Research), 2011)(Fig. 3), the Visual Numeric Endometriosis Surgical
Score (VNESS) system (Abdalla AL and S., 2015) and those proposed
by Chapron et al. and Adamyan (Adamyan, 1993;Chapron et al.,
2003). The ENZIAN classification showed a significant correlation
between the extent of the disease, diculty and length of surgery and
symptoms (Haas et al., 2013a;Haas et al., 2013b;Haas et al., 2013c;
Morgan-Ortiz et al., 2019;Montanari et al., 2019). The dierent scor-
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ing systems with their advantages and disadvantages are summarised in
Table I.
In addition to classifying endometriosis, the documentation of sur-
gical findings, such as in Endometriosis Fertility Index (EFI), has been
found to have a prognostic value in infertile women (Adamson and
Pasta, 2010;Adamson, 2013).
The working group emphasises the importance of classification of
DE, but also the limitations of the existing systems, specifically with
regard to the scoring of the severity of disease. The ideal classification
system for DE should define accurately the anatomical location, size of
the lesions and level of involvement of the adjacent organs. It should
also be reproducible and should help the surgeon in the planning and
execution of surgery.
The working group recommends documenting the following
information:
•the location of DE lesions;
•uterosacral ligaments, including whether ureters are infiltrated;
•rectovaginal septum, including involvement of vaginal wall/mucosa;
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Surgical treatment of deep endometriosis 5
Figure 2 Anatomical landmarks in DE surgery (vessels,
nerves, ureter, bladder, bowel) which may be involved and
have to be respected carefully. DE: deep endometriosis. (Image
courtesy of Complete Anatomy (reprinted with permissions).)
•bowel, including involvement of muscularis layer;
•bladder, including involvement of muscularis and ureteral ostia;
•other sides in the pelvis;
•extrapelvic locations;
•involvement of the ovaries;
•the sizes of the lesions;
•the number of lesions;
•the degree of involvement of adjacent organs and structures.
The current paper is structured according to the dierent locations
of DE, with further subdivision on extent (where relevant).
Pre-operative assessment and preparation
for surgery
Pre-operative assessment of patients with suspected DE aims to estab-
lish a diagnosis, evaluate extent of disease and determine the optimal
surgical approach. This includes a thorough medical history, clinical
examination and imaging. When assessing the medical history and
symptoms, the focus should be directed on symptoms that could
indicate the presence of DE lesions in specific organs/locations. These
include, but are not limited to, cyclical haematuria and cyclical rec-
tal bleeding (Chattot et al., 2019). It is very important to record
co-morbidities and take them into consideration when deciding on
surgery.
It is helpful to use a validated symptom questionnaire for data
collection, for audit and comparison. Women’s symptoms, such as
pain, should be assessed, for instance using a visual analogue scale and
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general quality of life questionnaires (e.g. the World Endometriosis
Research Foundation (WERF) set up the Endometriosis Phenome
and Biobanking Harmonisation Project (EPHect) Endometriosis Patient
Questionnaire) (Vitonis et al., 2014;Bourdel et al., 2015;Vanhie et al.,
2016). Other questionnaires can be used to assess specific aspects of
endometriosis, including sexual function, urinary function, bowel func-
tion, recovery and depression and anxiety. These symptoms should be
assessed, taking into account uterine bleeding pattern and associated
dysmenorrhea, as painful symptoms associated with irregular periods
can be managed by starting and/or adapting a medical treatment.
Fertility plans and indications for surgery should be discussed before
the surgical procedure, for instance using the EFI (Adamson et al.,
2010). Choices of dierent treatment options (surgery, IVF) for DE and
the selection of patients that would benefit from surgery are beyond
the scope of this document. However, IVF could be proposed as the
first step in patients who have been operated previously, who have
a low ovarian reserve and/or when there is male factor infertility
(Dunselman et al., 2014). Oocyte freezing may also need to be dis-
cussed as an option in cases of coexistent ovarian endometrioma
(Working group of ESGE-ESHRE and WES et al., 2017).
A surgical history is essential. Previous operation reports should be
read in detail and any pictures/videos reviewed carefully. The surgeon
should know if the retroperitoneal space was opened and, if it was, its
side should be noted. It is also essential to know whether ureterolysis
and/or bowel dissection was performed. Extensive ureteral dissection
always impairs ureteral vessels, so that even a very cautious and
meticulous repeat ureterolysis may induce ureteral ischemia. Similarly,
previous bowel dissection, and/or previous rectal shavings, implies that
the bowel wall may be compromised by previous procedures, so the
risk of bowel injury and/or postoperative fistula may be increased.
As the risks of intra- and/or postoperative urinary or intestinal com-
plications are considered much higher in women who have under-
gone previous extensive procedures, this should be taken in account
during counselling the woman, decision-making and organisation of
the surgical team. History of previous ovarian cystectomy should be
taken into account when planning and performing surgery on ovarian
endometrioma in particular in women who may wish to conceive in the
future (Working group of ESGE-ESHRE and WES et al., 2017).
Clinical examination
Clinical examination in women with suspected DE includes not only
a physical examination of the pelvis but also the inspection and pal-
pation of the abdomen. The examination may need to be extended
beyond the pelvis, depending on the symptoms of the woman. Loca-
tion and extent of disease can sometimes be determined by clinical
examination (Ripps and Martin, 1992;Koninckx et al., 1996;Bazot
et al., 2009). There should be special emphasis on the visualization
of DE in the vagina by inspection of the dorsal fornix with a bivalved
speculum.
Vaginal examination can facilitate the detection of infiltration or
nodules of the vagina, uterosacral ligaments or pouch of Douglas. It
could also contribute to the assessment of the extent of disease to the
pelvic sidewall, which is important to evaluate the risk of trauma to the
hypogastric plexus and/or the ureter. Rectovaginal digital examination
may allow the detection of infiltration or mass involving the rectosig-
moid or adnexal masses (Ripps and Martin, 1992;Koninckx et al., 1996;
Eskenazi et al., 2001;Condous et al., 2007). Rectal examination is highly
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6Working group of ESGE, ESHRE and WES et al.
Tab le I Classification systems for deep endometriosis.
Classification system Scoring of compartments Scoring of severity Positive aspects Negative aspects
..............................................................................................................................................................................................................................................
ENZIAN Classification
(Keckstei n et al., 2003b)
(Tuttlies et al., 2005)(Stiftung
Endometriose Forschung
(Foundation for Endometriosis
Research), 2011)
Retroperitoneal structures are divided into the
following three compartments:
- A: rectovaginal septum and vagina
- B: Sacro uterine ligament to pelvic wall
- C: rectum and sigmoid colon
Retroperitoneal distant locations:
- FA: adenomyosis
- FB: involvement of the bladder
- FU: intrinsic involvement of the ureter
- FI: bowel disease cranial to the rectosigmoid
junction
- FO: other locations, such as abdominal wall
endometriosis
Severity is rated in the same way for all
compartments:
- Grade 1: invasion <1cm
- Grade 2: invasion 1–3 cm
- Grade 3: invasion >3cm
Relatively good morphological
description provided
Correlation between
symptoms and involved
compartments
Additional aspects can be
calculated (e.g. the anticipated
operating time, risk of
complication during and after
surgery)
International acceptance of the
classification is still
low—mostly used in Europe
Chapron
(Chapron et al., 2003)
Ventral DIE
- A1: Bladder
Dorsal DIE
- P1: Uterosacral ligament
-P2:Vagina
- P3: Intestine (solely -with or without vaginal
infiltration- or multiple intestinal location)
No scoring Linked to an operative
procedure
Reported in two publications
by the authors, no further
information
Not widely used
Adamyan
(Adamyan, 1993)
Adamyan Stage I: endometriotic lesions are
confined to the rectovaginal cellular tissue in the
area of the vaginal vault.
Adamyan Stage II: endometriotic tissue invades
the cervix and penetrates the vaginal wall,
causing fibrosis and small cyst formation.
Adamyan Stage Ill: lesions spread into the
sacro-uterine ligaments and the rectal serosa.
Adamyan Stage IV: the rectal wall, recto-sigmoid
zone, and rectouterine peritoneum are
completely involved, and the rectouterine pouch
is totally obliterated
No scoring Not published in peer
reviewed journal
Not widely used
Visual Numeric
Endometriosis Surgical Score
(VNESS)
(Abdalla AL and S., 2015)
Eight locations:
Left adnexa—Left pelvic sidewall - Left
uterosacral area/ventral compartment
(UVF)—dorsal compartment (POD)/right
uterosacral area—right pelvic sidewall—right
adnexa
For each location, a score between 0
and 4 representing the severity of
endometriosis
0: No visible endometriosis
1: Superficial endometriosis
2: DIE with no attachment to viscera
3: DIE loosely adherent to viscera
4: DIE densely adherent to viscera OR
invading muscularis OR kissing ovaries
Intuitive and easy to
remember.
Visually helpful
Not published in peer
reviewed journal
Not widely used
DIE; deep infiltrating endometriosis, UVF: Left uterosacral area/ventral compartment POD: Dorsal compartment
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Surgical treatment of deep endometriosis 7
Figure 3 Revised ENZIAN-classification for DE.The system classifies the clinical findings of endometriosis according to their localisation (com-
partment) and size (<1 cm, 1–3 cm, >3 cm). The ENZIAN classification focusses on the three dimensions (compartments) in the pelvis: A = craniocaudal
axis or compartment (rectovaginal space, vagina), B= laterodorsal axis (uterosacral and cardinal ligaments), C = dorsal axis (rectosigmoid). Other
localisations as uterus, bladder, ureter, other bowel involvement and extragenital localisations are respected as well and described with sux F). The
ENZIAN Classification is under revision (2019) again which is under publication.
recommended to assess the lateral and dorsal extension of the disease
allowing detection of the patients who are at risk of hypogastric vessels
injury and/or hypogastric plexus damage. It also allows the surgeon to
evaluate the mobility of the nodule of the dorsal cul-de-sac and thus
to predict how dicult the surgery may be.
Imaging and other investigations
The ESHRE Guideline on the Management of Endometriosis recom-
mends assessing the ureter, bladder and bowel involvement by addi-
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tional imaging, if there is a suspicion based on history or physical exam-
ination of DE, in preparation for further management (Dunselman
et al., 2014). Imaging for suspected involvement of bladder, bowel
and ureters may start with ultrasonography (US) (Guerriero et al.,
2016). Other imaging techniques, such as MRI (Fig. 4) including neuro
MRI, and computed tomography (CT) (only in selected cases as it is
associated with unacceptably high radiation exposure) (Exacoustos et al.,
2014;Guerriero et al., 2018) can also be used. Assessment of MRIs
should be performed using high-definition standards. Barium enema
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8Working group of ESGE, ESHRE and WES et al.
Figure 4 MRI picture of the pelvis. DE in the rectum with small,
dense adhesions between the posterior wall of the cervix and anterior
wall of the rectum (right circle) and adenomyosis (left circle).
and sigmoidoscopy may give additional information about stenosis of
the bowel. These investigations aim to determine the location, size
and number of DE lesions (nodules or plaques) as well as the level of
infiltration (depth of invasion, length of infiltration, stenosis) into the
organ/structure involved. Furthermore, the identification of lesions
on/in the pelvic wall (i.e. sacral root) and other extragenital localisation
(abdominal wall, inguinal canal, diaphragm, lung, etc.) with specific
imaging techniques is relevant, as it has an important impact on the
surgical treatment and its planning. Kidney sonography is mandatory
in every patient with DE potentially involving the ureters to prevent
overlooking silent hydronephrosis.
Bowel. Where appropriate, involvement of bowel muscularis and the
distance between the inferior border of the lowest bowel lesion and
the anal verge should be evaluated as these would be expected to have
an impact on the type of surgery that will be performed. Limitations of
the accuracy of these investigations should be kept in mind.
Colonoscopy identifies stenosis or intraluminal lesions, which are
rare, but unfortunately it does not give sucient information about
the presence, localisation and size of endometriosis in the bowel wall
(Fig. 5).
US is the first-line imaging modality for the assessment of pelvic
endometriosis. It has been demonstrated that most of the deep lesions
in the lower colon can be identified with a high sensitivity and specificity
(Hudelist et al., 2009;Hudelist et al., 2011;Exacoustos et al., 2017).
It may have limitations with respect to field of view and operator
dependence (Fig. 6).
Transrectal ultrasonography (TRUS) may be used for rectosigmoid
involvement but could not be adequately assessed for other anatomical
sites because of scant heterogeneous data.
MRI is usually performed as an additional examination in complex
cases or prior to surgery and is highly accurate in the evaluation of
endometriosis.
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Figure 5 Deep endometriosis of the rectosigmoid. The
extent of the white nodules (multifocal) which infiltrate the muscular
layer is not visible by colonoscopy and also dicult to identify com-
pletely by laparoscopy.
Figure 6 Transvaginal ultrasound of the rectosigmoid with
signs of infiltration of the muscular layer. Length >3cmEnzian
C3. Hypodense ultrasound pattern (halfmoon-shaped) represents the
hyperplasia of the lamina muscularis with inclusion of epithelium,
stroma and fibrosis.
Diagnostic accuracies were higher for transvaginal ultrasonography
(TVUS or TVS) with bowel preparation (TVUS-BP) and rectal water
contrast (RWC-TVS) and for 3.0 T MRI than for conventional methods,
although the paucity of studies precluded statistical evaluation (Nisen-
blat et al., 2016). TVUS for DE is highly dependent on the experience
of the operator and the quality of the US equipment. The additional
use of vaginal and rectal contrast US gel can further enhance the image
(Grammatico et al., 2017).
Multi-detector computed tomography enema (MDCT-e) is another
technique which might have a high diagnostic performance for rectosig-
moid and other bowel endometriosis (Ferrero et al., 2011).
Virtual colonoscopy may add new information to that provided by
MRI (Mehedintu et al., 2018). Virtual colonoscopy is a single non-
invasive short procedure. It provides information about lesions in the
whole length of the colon (esp. sigmoid, ileum, caecum) (van der Wat
et al., 2013). However, a dry bowel preparation is necessary, and the
risk of irradiation has to be considered, as with the MDCT-e scan.
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Surgical treatment of deep endometriosis 9
If rectal bleeding (haematochezia) is reported by the patient,
colonoscopy is indicated for dierential diagnosis of primary bowel
disease.
Bladder. TVS is sucient to diagnose bladder endometriosis in the
majority of cases. Typically, lesions are located at the dorsal wall or
the fundus of the bladder. They can extend into the vesico-cervical
space and the ventral wall of the uterus. A partially filled bladder
can optimize sonographic assessment, while a full bladder can make it
more challenging (Guerriero et al., 2018). MRI is often not necessary to
diagnose bladder endometriosis in addition to TVS, but it can be helpful
to identify the relation between the nodule and the ureteral ostia and if
additional complex rectovaginal endometriosis is suspected (Carfagna
et al., 2018;Aas-Eng et al., 2019).
Pre- or intra-operative cystoscopy is recommended for bladder
endometriosis as it allows visualization of the blueish, submucosally
protruding nodules. It is important to localize the lesion precisely
in relation to the ureterovesical junction (UVJ) (Collinet et al., 2006;
Fadhlaoui et al., 2015). Whilst the mucosa (urothelium) itself is rarely
infiltrated, the nodule usually protrudes into the bladder cavity and
may reach considerable size. Involvement of the outer layer of the
detrusor muscle cannot be excluded by cystoscopy. A biopsy is only
required for dierential diagnosis when other diseases are suspected,
such as urothelial carcinoma and/or interstitial cystitis. If surgery of
bladder endometriosis is planned, the placement of ureteral stents can
be advantageous.
Urodynamic evaluation to assess bladder function can be useful in
case of bladder problems. It may have a place in distinguishing pre-
existing bladder dysfunction from that developed postoperatively, as
surgery for DE may induce de novo dysfunction, potentially caused by
surgical nerve damage (de Lapasse et al., 2008). The use of a specific,
validated questionnaires, such as International Prostate Symptom Score
(I-PSS) (Barry et al., 1992) and Bristol Female Lower Urinary Tract
Scale (BFLUTS) (Jackson et al., 1996), may improve the preoperative
work-up.
Ureter and kidney. Assessment of the kidney is also necessary to rule
out asymptomatic hydronephrosis (Lusuardi et al., 2012). Endometrio-
sis of the ureter is very likely if hydronephrosis in women with
endometriosis is present, so abdominal ultrasound is the gold standard
in this situation. Hydronephrosis requires a functional work-up (side
separate clearance) in order to assess the renal function. Imaging,
including intravenous urography (IVU), high-resolution TVUS, mercap-
toacetyltriglycine (MAG3) renal scan (or radioisotope renography),
MRI and/or contrast CT, is usually performed according to local
protocols. Studies have shown the value of TV ultrasound scanning of
ureters in patients with DE; in about 50% of the cases with ureteral
involvement, obstruction can already be visualised by TVUS (cases lack-
ing hydronephrosis—early stage obstruction) (Carfagna et al., 2018).
In case of hydronephrosis, the function of the kidney has to be
checked before surgery.
Nerves. The involvement of nerves in DE is of great importance to
the patient as well as to the surgeon (Possover et al., 2011;Chiantera
et al., 2018).
Both the disease and radical removal of endometriosis may lead
to the destruction of the nerve fibres with corresponding symptoms,
which can be very debilitating for the patient.
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Endometriosis close to the sympathetic and parasympathetic nerve
fibres (hypogastric plexus and splanchnic nerves) can lead to a dys-
function of pelvic organs (e.g. dysfunction of the bladder as well as
disturbance of vaginal lubrication and intestinal dysfunction) (Possover,
2014).
Involvement of somatic nerves, such as the sacral plexus and
the sciatic nerve, leads to corresponding neurological symptoms or
deficits.
In recent years, neuropelveology (Possover et al., 2015), a new field,
has become established in endoscopy and gained great importance.
Laparoscopy provides an optimal surgical approach to the pelvic
somatic nerves and allows micro-neurosurgery as a therapeutic
approach. Both the exact pre-operative diagnosis in cases of suspected
nerve involvement and the specialized surgical techniques to protect
the nerves or even eliminate endometriosis close to the nerve are
reserved for specialists who have undergone appropriate training in
diagnosis and surgical treatment (Rabischong et al., 2018).
The current document draws particular attention to the importance
of these procedures. However, these interventions require special
training and detailed instructions on them would be the subject of
another publication.
Extrapelvic lesions. The diagnostic approach for extra-pelvic endometri-
otic lesions includes physical examination (palpation), MRI and US.
MRI can help to visualise the extent and to plan the surgery. A
complete diagnostic evaluation will minimise the risk of incomplete
resection.
Abdominal wall endometriosis including scars (secondary to Cae-
sarean sections or hysterectomy using open route), the umbilicus and
the inguinal region are thoroughly explored using either low depth
US or MRI examinations. The size and depth of nodules, and the
involvement of muscles or aponeurosis, should be checked before
the surgery in order to maximise the chances of a complete excision.
Large defects after excision have to be closed with the help of a
mesh.
MRI (especially high definition) may reveal endometriosis of the
diaphragm, usually when the lesions are larger than 5 mm, or when they
presented recent bleeding (T1 frontal, axial and sagittal views). How-
ever, small lesions may be overlooked during the pre-operative assess-
ment and may be only intra-operatively revealed. When laparoscopic
examination of the diaphragm is carried out using a trans-umbilical
endoscope, the surgeon should be aware that only the ventral part
of the diaphragm can be explored. However, lesions located behind
the liver in the hepatophrenic cul-de-sac are routinely associated with
visible satellite lesions spread on the ventral part of the diaphragm
(Ceccaroni et al., 2012).
Informed consent
Informed consent should be relevant to the patient and must cover
the extent of the surgery that may be performed and its potential
complications. Pros and cons of alternatives to the proposed treatment
must be presented (Bolton, 2015). Short- and long-term side eects
of surgery should be explained. The use of current patient information
leaflets or evidence-based online resources, with references/links to
best practice guidelines, should be considered to provide a sucient
source of information that the woman can review in her own time.
This may also be helpful as evidence of appropriate pre-operative
counselling.
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10 Working group of ESGE, ESHRE and WES et al.
Multidisciplinary surgical team
The surgical team should be organised according to the needs of the
planned or anticipated procedure(s). A bowel surgeon, a urologist, a
thoracic surgeon and even a plastic surgeon may need to be involved.
The gynaecologist should lead the team as his/her understanding of
endometriosis and the woman’s symptoms and needs is crucial in
planning the surgery. The gynaecologist advocates for the patient and
sets up a unique care plan, together with the team and patient, to
improve the woman’s pain, fertility and quality of life. Such a care
plan should consider input from other disciplines related to the tech-
nical aspect of procedures. A multidisciplinary team meeting before
the surgery may be helpful. The team should be informed well in
advance in order to plan the procedure and to organise their time
adequately.
If an ileostomy or a colostomy is planned, this should be discussed
extensively with the woman and the site of the stoma may be decided
and eventually drawn on the skin before the procedure.
Pre-operative strategies for a safe and complete excision of the
lesion
Bowel preparation. Dierent types of bowel lumen cleaning can be
helpful in cases of lesions in the dorsal compartment for the following
reasons:
•an empty bowel gives more space in the pelvis during the dissection;
•the use of rectal probes or manipulators in a clean bowel will cause
less contamination with faeces on the perineum, especially when the
vagina has to be opened;
•in the case of opening the bowel, it will minimise faecal soiling in the
abdomen.
According to the literature data on colorectal surgery, mechanical
bowel preparation and enemas are widely used (Guenaga et al., 2011;
Oliveira et al., 2016), though specific trials on the usefulness of bowel
preparation in endometriosis surgery (where the vaginal fornix dorsal
is often opened) are not available. Whereas none of these techniques
have a proven benefit on the reduction of postoperative complications
(Guenaga et al., 2011), in cases where a low anastomosis is expected
mechanical bowel preparation is better than an enema (Platell et al.,
2006). The use of intraluminal antibiotic decontamination of the bowel
to reduce clinically relevant anastomotic leakage can be considered
(McDermott FD et al., 2016).
Ureteral stenting. Pre-operative placement of ureteral stents is
suggested when: surgery of large bladder endometriosis is planned;
ureteral endometriosis is suspected pre-operatively; hydronephrosis
is present; or there is a history of previous ureteral surgery.
Uterine manipulator and rectal probe. The use of a uterine manipulator
achieves maximum mobility of the uterus, thereby improving visualiza-
tion and facilitating dissection. A rectal probe could also be helpful in
moving the bowel, although it could be hindered by stenosis due to a
deep nodule or severe bowel adhesions. Tactile feedback between the
dissecting instruments and the rectal and vaginal probes, handled by an
assistant, helps to identify the correct planes of cleavage. Bowel and
adnexal suspension can improve visualization and access to the pouch
of Douglas (Einarsson and Wattiez, 2016)(Figs 7 and 8).
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Figure 7 Deep endometriosis in the vagina, rectovaginal
septum and the anterior wall of the rectum (Enzian A, C
compartment). Two dierent ways to excise the nodule. A manipu-
lator and a sponge or rectal probe is in situ for a better presentation of
the nodule during the excision procedure. (Reprinted with permissions
from Keckstein and Hucke, 2000).
Figure 8 Frozen pelvis with invisible deep endometriosis
(bilateral ovary, left cardinal ligament, ureter left, anterior
wall of the rectum).
Strategy of the surgical intervention
Each surgeon needs a strategy for the operation, which is influenced by
many factors including the size, activity and localization of endometrio-
sis as well as the age and expectations of the patient, and the results of
previous interventions.
Advanced endometriosis in a young patient with a desire to have
children may be operated dierently than in a patient over 40 years of
age with pain as the main symptom.
The surgeon is often confronted with the conflict between complete
removal of endometriosis and the need for preservation of organs
aected by the disease.
Another challenge is tackling multi-organ involvement, which
requires a complex intervention possibly in a multidisciplinary setting.
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Surgical treatment of deep endometriosis 11
Tab le I I Principles for identifying and treating deep endometriotic lesions.
.........................................................................................................................................................................................
•Identify all important anatomical structures (ureters, colon, small bowel, major vessels, adnexae, uterus, bladder, nerves).
•Identify the lesions.
•Signs of deep endometriosis include:
•Fibrosis, with or without characteristic dark spots
•(Dense) adhesions
•Distortion of anatomical structures, infiltrations
•Reduced tissue elasticity
•Haemorrhagic cystic structures
•Perform easy steps first as this will facilitate dicult ones.
•Divide adhesions and restore pelvic anatomy in addition to complete excision of endometriosis.
•Free and isolate the lesions.
•Start the dissection in areas free of disease.
•Optimise exposure by using manipulators, ovariopexy and additional ports, if necessary.
•Aim for complete excision whenever reasonable and possible.∗
∗When deciding that a part of the disease may be left behind, the surgeon should remember that if an extensive dissection has been performed to access thispartof thedisease,
reoperation will be extremely dicult and sometimes almost impossible. If excision is considered to be too risky, it is likely to be even more dicult and dangerous if a reoperation is
needed due to recurrent pain or other severe symptoms (such as stenosis of the bowel or ureter). Ideally, surgeons would be prepared to manage all aspects of the disease.
An important limitation is the risk of postoperative complications.
For this reason, occasionally a limited radicality or surgery in several
steps may be chosen, for example simultaneous segmental resection of
intestinal endometriosis and ureteral re-implantation in hydronephrosis
may be avoided.
Decisions for the strategy before and during surgery depend in
particular on the situs and surgeon’s experience, and they have to be
made on a case-by-case basis.
Open versus endoscopic surgery (or robotic assisted)
Endoscopic access has become standard for the treatment of
endometriosis, including DE. It is obvious that the endoscopic
procedures are advantageous due to better views and access to
lesions in the depth of the pelvis, as well as lower postoperative
morbidity. Minimal trauma to the abdominal wall and the healthy
peritoneum, lack of dehydration and the use of microsurgical
techniques improve the outcome, especially in patients with infertility.
Furthermore, there are anatomical sites or endometriosis findings that
can exclusively be reached/treated only by an endoscopic procedure
(e.g. neuropelveology).
Endoscopic operations require special instruments and equipment
as well as a high level of training and experience of the surgeon. The
access route should be chosen according to the clinical findings and the
existing options.
However, a laparotomy (sometimes with midline incision) may occa-
sionally be more eective than several inadequate laparoscopies. The
advantage of a laparotomy for treatment of severe endometriosis to
identify and completely eliminate it lies in the ability of having a better
tactile feedback. In this situation, microsurgical operation techniques
should still be used.
Robot-assisted surgery has gained importance in the treatment of
endometriosis over the last 10 years. Special features of the instru-
ments may facilitate dicult steps of the procedures and some of the
benefits of laparotomy are thus incorporated into endoscopic surgery.
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Several studies have shown that the results of robot-assisted surgery
in DE are equivalent to those of conventional laparoscopy, but not
superior.
In the current document, particular attention is given to conventional
endoscopic procedures.
Initial steps of DE surgery—patient
positioning in view of anticipated long
duration of surgery
Prevent pressure sores and compartment syndrome by using:
•anti-embolism stockings for thromboprophylaxis, and additional
prophylaxis with postoperative low molecular weight heparin is
usually recommended after this type of pelvic surgery (follow local
guidelines);
•body warmer to maintain the core temperature;
•boots, lithotomy with soft stirrups, legs flat, intermittent pneumatic
compression devices.
The woman is placed in the modified dorsolithotomy position and
her legs are placed in surgical stirrups carefully avoiding trauma to the
leg nerves. As the surgery is often long, particularly in women with
previous multiple surgeries and/or in obese or moderately overweight
patients, mobilization and/or massage of the legs can be performed
every 2–4 h or between dierent surgical phases. Application of
intermittent pneumatic compression devices or sequential compres-
sion devices has been proposed to limit the risks of lower limb
compartment syndrome (Tomassetti et al., 2009;Gould et al., 2012).
Arms should be positioned carefully to avoid shoulder restraints or
pressure, especially in steep Trendelenburg position during surgery.
•Examination under anaesthesia is generally recommended for DE.
An additional rectovaginal exam under laparoscopic vision may be
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12 Working group of ESGE, ESHRE and WES et al.
Figure 9 DE involving the uterosacral ligament, vagina and
the rectum. The extent of the disease is not visible during diagnostic
laparoscopy. Spaces have to be opened in order to get access to the
entire lesion.
Figure 10 Dissection of the posterior compartment. Right
uterosacral ligament has already been resected, the vagina is partially
open with the manipulator in place.
beneficial particularly when rectovaginal nodules are not obviously
visible.
•Antibiotics can be used according to local guidelines.
•Systematic laparoscopic inspection and documentation is recom-
mended. After insertion of the laparoscope, the upper abdomen
including diaphragm and appendix/caecum should be inspected,
preferably prior to placing the patient in (adequate) Trendelenburg.
•The placement of secondary trocars for the various instruments
should be individualized according to the anatomical situation and
surgical needs.
The basic principles to identify and treat deep endometriotic lesions
are stated in Table II.
DE of the uterosacral ligaments and
rectovaginal septum with or without
involvement of the rectum
The extent of the surgical procedure is determined by the size of
the lesions, their location, their number (single or multifocal), and the
degree of infiltration (Figs 9 and 10).
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Definitions of bowel infiltration and surgical procedures
The pre-operative clinical diagnostic workup including clinical exami-
nation (vaginal and rectal), TVUS, and an optional MRI is necessary in
order to identify the bowel wall infiltration pre-operatively. A negative
colonoscopy does not exclude the intramural presence of DE.
In case of muscularis infiltration by the nodule, the distance of the
inferior border of the most distal bowel lesion to the anal verge should
be evaluated, as this may impact on the type of surgery performed.
If the lesions are only located in or on the serosa without infiltration
of the muscularis layer, it can be treated with superficial resection
(serosal shaving) (Koninckx et al., 2012;Vanhie et al., 2016).
If deep (infiltrating) lesions involve the muscularis layer, sometimes
the submucosa and even the mucosa, partial or full thickness removal
by shaving, discoid or segmental bowel resection is necessary (Kon-
inckx et al., 2012;Donnez and Roman, 2017)(Figs 5 and 7).
First steps of surgery
Uterine, vaginal and rectal set up. A uterine manipulator is used to
improve exposure of the cul-de-sac, particularly in the presence of
an enlarged uterus due to fibroids and/or severe adenomyosis, which
makes the procedure more dicult. In some cases, a sponge can be
placed in the dorsal fornix of the vagina. A rectal probe should also
be available to mobilize the rectum in order to determine its position
and attachment to the vaginal wall and to evaluate the elasticity of
the tissue and degree of stenosis, taking care to avoid inadvertent
rectal laceration. During the surgery, these three manipulators can be
mobilized individually in order to clearly identify the limit between the
vagina, the rectal wall, and other pelvic structures (Figs 7, 9 and 10).
Preparing the operating field. Prior to starting the operation, a vagi-
nal exam using a bivalved speculum and digital (vaginal and rectal)
examination for the evaluation of the dorsal fornix (mucosa protru-
sion/retraction or invasion) and the extension to the pelvic sidewalls
is recommended.
The following steps may facilitate the surgical procedure: ovariolysis
and ovariopexy, sigmoid mobilization, ureterolysis, and the identifica-
tion of ligaments and rectosigmoid colon.
Ovariolysis The mobilization of fixed ovaries on the pelvic sidewall
improves the view of the operative field, particularly the lower struc-
tures in the cul-de-sac, which simplifies the identification of the ureters.
If present, endometrioma should be drained and managed according
to previous recommendations (Working group of ESGE-ESHRE and
WES et al., 2017). This may be done immediately after the drainage of
the cyst or after having removed all other deep lesions in the pelvis.
Endometriosis in the ovarian fossae should also be removed.
Temporary ovariopexy Suspension of the ovaries with sutures
(curved or straight needle through the abdominal wall) or special
devices can maximize access to the pelvic structures and especially the
pararectal spaces and the pelvic sidewalls.
Mobilisation of the sigmoid: (starting from the ‘white line of Toldt’)
Mobilize the sigmoid colon o its attachments to the abdominal wall
and pelvic sidewall to expose the left adnexa and underlying structures
such as the left pararectal space and ovarian fossa.
Ureterolysis It is advisable to identify the position of the ureter on the
pelvic rim or upper pelvic sidewall at the beginning of the procedure.
The ureter should be followed down to the cardinal ligament and the
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Surgical treatment of deep endometriosis 13
crossing with the uterine vessels. When covered with endometriotic
lesions, dissection of the ureter will be necessary to prevent inad-
vertent damage. The procedure can be simplified with the previously
performed ovariopexy.
Bowel adhesiolysis The approach to the dorsal compartment is
often hindered by dense adhesions between the rectum, uterosacral
ligaments, and the dorsal side of the uterus (Fig. 8). Even with the use
of manipulators it may be very dicult to identify the exact planes of
cleavage for the dissection procedure.
As the presence of dense adhesion between the rectum and other
structures may obscure the DE, complete dissection of these adhesions
is mandatory. Opening of the pararectal fossa—starting in healthy
tissue—will facilitate the excision of the nodule.
Adhesiolysis is performed with cold scissors, blunt dissection or
thermal instruments with minimal collateral thermal spread.
Aquadissection can be considered in special situations: injection of
Ringer’s lactate solution with or without diluted vasopressin may help
to identify the planes of cleavage and to separate vital structures,
such as the ureter or bowel, and may reduce bleeding (oozing). The
liquid can be injected with a spinal needle inserted individually and
directly through the abdominal wall, or with other instruments such
as suction/irrigation cannulas.
Second step of surgery for DE involving the rectovaginal space
DE involving the muscularis layer of the rectum with no vaginal infiltration.
In such cases, shaving consists of the separation of the DE nodule from
the ventral part of the rectum.
The aim of the procedure is to mobilize the ventral rectal wall from
the nodule until the rectum is free (first lateral then central dissection
until finally the distal border of the nodule is released) by means of
mechanical dissection (cold scissors) or low-thermic energy sources
(e.g. CO2laser, plasma).
Pararectal spaces are opened longitudinally, medially from the
uterosacral ligaments, and as close to the lateral side of the bowel
as possible in order to avoid injury to the hypogastric and splanchnic
nerves. Dissection is continued until the opening of the healthy
rectovaginal space. The use of a uterine manipulator and/or a vaginal
probe helps to identify the important structures, such as the vagina, the
cervix and the rectovaginal septum, by moving it in various directions.
Once the lateral sides of the rectum are freed, rectal shaving is
performed on the ventral wall of the rectum to remove the endometri-
otic lesion completely. Thus, the nodule is dissected away from the
rectal wall in an upward direction, resulting in the rectum falling back
dorsodorsally. The nodule is then dissected o the dorsal cervix, the
uterosacral ligaments and the vagina without opening the latter in the
absence of infiltration.
An alternative surgical technique named ‘the reverse technique’ can
also be applied, in which the DE lesion is separated first from the cervix
and the vagina and only in a second stage from the rectum (Kondo
et al., 2011;Bourdel et al., 2018). The removal of the nodule from the
mobilized rectum can be facilitated with a probe or sponge inserted
transanally into the lumen (Fig. 7).
The advantage of the reverse technique could be that any opening of
the intestinal lumen takes place very late and hence the contamination
time of the surgical field is shorter.
After the complete excision of the nodule from the wall of the bowel,
leaving soft tissue behind, it is always required to check the integrity
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of the bowel wall. This can be done by gently stretching the bowel
over the rectal manipulator to identify thinned areas. Another method
to detect leakage is to administer air into the rectal lumen while the
pelvis is filled with water or to fill the bowel with diluted methylene
blue. In the near future, the use of indocyanine green (often used by
general surgeons when assessing bowel anastomosis) will have to be
considered, adding an evaluation of the vascularisation of the bowel
wall to the identification of a leakage (Bar-Shavit et al., 2018;De Neef
et al., 2018;Seracchioli et al., 2018;Shen et al., 2018).
In the case that a muscularis/partial thickness defect is identified,
this can be sutured in one layer by using absorbable stitches starting
in healthy margins. In the case of a full thickness defect (opening of the
mucosa), a two-layer technique or a conversion to disc excision using
a transanal stapler, which provides a tight stapled line involving healthy
rectal wall, is suggested.
The disadvantage of the shaving technique in the infiltration of the
muscularis is that it may result in incomplete excision, which should be
considered in the pre-operative counselling of the woman.
DE involving the muscularis layer of the bowel and the vagina. In the case
of vaginal infiltration by the DE nodule, the first step of the procedure
is similar to that previously described (see DE involving the muscularis
layer of the rectum with no vaginal infiltration). The aim is to resect
the vaginal fornix adjacent to the uterine torus and to the ventral root
of the uterosacral ligaments (Fig. 7). This may be aided by the use
of a manipulator in the uterus and/or vagina (sponge, manipulator).
Where possible, preserve a rim of healthy vaginal mucosa attached to
the cervix in order to facilitate the vaginal closure. The DE nodule can
be extracted through the vaginal opening. Before starting to suture the
defect, the completeness of the excision should be checked by a vaginal
examination.
The excision of the vaginal nodule may also be done via the vaginal
route as a first surgical step under laparoscopic guidance (Possover
et al., 2000). The suturing of the vaginal defect can be performed
laparoscopically or vaginally by using running or interrupted sutures
(e.g. absorbable braided suture). When suturing laparoscopically, the
pneumoperitoneum can be maintained by inserting a roll of swabs
(potentially covered by a glove) into the vagina.
Second step of surgery for DE involving the uterosacral ligaments,
cardinal ligaments and pelvic sidewall
No infiltration of the ureters.
Uterosacral ligaments The operative treatment of lesions involving the
uterosacral ligaments depends on the extent of the disease and the
reactive alteration of the tissue. These lesions should be removed
completely with scissors or low thermal instruments, since coagulation
alone may not be deep enough and therefore incomplete. Prior to
the excision, it is advisable to identify the landmarks on the pelvic
wall, which are the ureter, bowel, nerves and pelvic vessels, and to
dissect these structures carefully if involved in the disease process.
The ureter usually runs closely to the lateral side of the uterosacral
ligament and can be densely adhered to it. Medially, mobilization of the
rectosigmoid will provide more space and preparation is carried out in
the direction from dorsal to ventral. Once the uterosacral ligament is
exposed dorsally, it can then be fully mobilized and excised towards the
uterus. An important aspect here is the proximity to the hypogastric
nerves, which should be avoided if not involved, or largely spared by
a meticulous dissection technique. In the case that hypogastric nerve
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14 Working group of ESGE, ESHRE and WES et al.
fibres are involved, a complete excision would include the resection
of these as well. In the case of bilateral involvement of the hypogastric
nerve, a more conservative approach should be considered to preserve
bladder and sexual function.
To protect the hypogastric nerves, it is advisable to prepare them
cranially in order to protect them in the area of the uterosacral
ligaments.
Cardinal ligaments If the parametrium is involved, the uterine vessels
and the splanchnic nerve fibres should be conserved accordingly.
The exposure of these structures can be achieved by dissection of
anatomical spaces such as the Latzko space, the Okabayashi space and
the Yabuki (Fourth) space.
The mobilization of the lesions usually starts cranially and laterally
in the parametrium, directed towards the medial side. In the case of
extensive involvement, it may occasionally be necessary to sacrifice
the uterine vessels, although the latter should be avoided in women
desiring pregnancy after surgery (especially bilateral); this may mean
that parametrial excision is incomplete.
The depth and the lateral extent of the preparation increases the risk
of harming the parasympathetic nerves significantly.
It may also be necessary to remove the insertion of the cardinal
ligaments at the outer part of the torus to complete the surgery.
This radical approach should be avoided in the instance of a bilateral
involvement of the parametria.
If the cardinal ligament involvement reaches the pelvic sidewall, the
dissection procedure should be started in healthy tissue close to the
internal iliac vessels, sacral root and (para)sympathetic nerves. In such
cases, neuropelveologic knowledge and advanced experience in radical
surgery in this area is mandatory.
Infiltration of the ureters. If the lateral parametrium/cardinal ligament
is involved, one strategy could be to remove the nodule in two parts
(transecting it): first the rectovaginal part, and secondly the parametrial
part since at that point the anatomy will have become clearer, especially
with regards to the view of the nerves and vessels.
The obstruction of the ureter with consecutive hydronephrosis
makes an intervention mandatory.
The ureter has to be freed completely by excision of pathologic
structures within the ligaments and connective structures lateral and
dorsal to the uterus. It is important to use either cold scissors or low
thermal energy sources (e.g. CO2laser, plasma) when dissecting the
ureter in order to minimize the risk of damage to its microvasculature.
However, in most cases, the ureter is narrower due to external
pressure from fibrotic tissue, in 2–5% of cases a true infiltration of the
intrinsic ureter wall is present and segmental resection with an end-
to-end anastomosis or re-implantation into the bladder may become
necessary (see also Urinary tract endometriosis).
Second step of surgery for DE involving the bowel
In the case of bowel infiltration, several procedures could be consid-
ered according to the consent of the woman (Keckstein et al., 2003a;
Tuttlies et al., 2005;Koninckx et al., 2012;Abrao et al., 2015;Roman
et al., 2016a;Abrao et al., 2017;Donnez and Roman, 2017)(Fig. 11).
Discoid excision. If the rectal wall is still infiltrated by implants of DE
after shaving, it will appear hollow, rigid and thickened when palpated
with a laparoscopic probe and/or a rectal probe.
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In these circumstances, to achieve a macroscopically complete exci-
sion, a full-thickness discoid excision of the shaved area may be
performed, followed by suturing the defect in one or two layers.
Before performing a discoid excision, the extent of the bowel circum-
ference involvement has to be evaluated. Indeed, there is a correlation
between the depth of bowel infiltration and the circumference of the
bowel aected by the disease.
Instead of suturing the defect in one or two layers, discoid excision
can also be performed by using transanal staplers (either semi-circular
or end-to-end circular staplers) (Figs 12, 13 and 14).
The semi-circular stapler allows large discoid excision (5–6-cm diam-
eter on average) when the shaved area is located between 8 and
10 cm above the anus. The end-to-end circular stapler can also be
used to remove discoids up to 3 cm in diameter located in the upper
rectum and rectosigmoid junction. Preliminary rectal shaving reduces
the thickness of the rectal patches, facilitating the excision (Roman,
2013).The rectal wall is pushed with a probe or pulled with threads
into the head of the open stapler, which is then closed. In case the
resection of the lesion was incomplete (owing to the size of the lesion
or incorrect placement of the stapler), a second full-thickness resection
is possible (to remove the residual lesion including also the first stapler
line) (Kondo et al., 2015;Trippia et al., 2016;Braunschmid et al., 2017).
Colorectal resection. Dissection is carried out through the rectovagi-
nal septum and follows the steps described above (Keckstein and
Wiesinger, 2005;Abrao et al., 2015;Bouquet de Joliniere et al., 2019)
(Fig. 15).
Mobilization of the rectum is carried out at least 20 mm below the
rectal nodule.
The proximal dissection line is close above the lesion. Mobilisation
and dissection of the bowel from the mesorectum and mesocolon are
performed in contact with the dorsal wall of the rectosigmoid, which
oers the possibility to preserve the mesorectum and mesosigma.
This technique is used especially for short segments and if no other
extraperitoneal structures are involved. When preparing the intestine
this way, care must be taken not to damage the microvasculature of
the intestinal wall due to thermal injury (Hudelist et al., 2018).
In the case of multiple rectosigmoid lesions, these may be removed
en bloc using a long segmental resection, or rectal discoid excision could
be associated with short segmental resection of the sigmoid colon in
Figure 11 Symptomatic DE of the sigmoid colon with
stenosis. Segmental resection is necessary.
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Surgical treatment of deep endometriosis 15
Figure 12 Disc resection of the anterior rectal wall with
the circular stapler. Specimen in the open stapling device.
Figure 13 Final view of the rectum with the lining of the
stapler in the anterior wall.
Figure 14 Rectoscopy with the view of the stapler lining in
the anterior rectal wall.
order to spare healthy bowel located between the nodules: the latter
technique requires a very careful check of the blood supply of the
bowel.
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Figure 15 DE of the rectosigmoid colon. Segmental resection
with linear stapler, resection of the segment outside of the abdominal
cavity is followed by the anastomosis with circular stapler (Reprinted
with permissions from Keckstein and Hucke, 2000).
The stapler is entered into the peritoneal cavity through one of
the inferior trocars and the rectum is then distally sectioned. A mini-
laparotomy of 4 cm is carried out in a transverse suprapubic fashion
(Pfannenstiel incision) or at the place of the inferior left or right
laparoscopic port site.
After the mobilized intestinal segment is pulled in front of the
abdominal wall, the resection of the involved part of the bowel takes
place, which is performed proximally close to the macroscopic nodule.
The extraction of the bowel through the opened vaginal vault during
hysterectomy, or an already opened vaginal fornix, is another option,
but this requires a long segment of the bowel to be mobilized. With
this technique, it should be noted that the farther cranial intesti-
nal sections are dicult to access by palpation, even with resection
techniques that are performed laparoscopically without the aid of a
mini-laparotomy. Therefore, there may be a risk of missing small or
additional ‘dicult-to-identify’ nodules and, consequently, leaving them
behind after surgery.
The transrectal extraction of the proximal segment has been
described by individual authors. However, this requires that the
intestinal lumen is open and thus also a higher risk of contamination
for the abdomen exists during this more complex procedure.
The anvil of the circular stapler is introduced into the stump of
the colon and fixed. After the stump has been brought back into the
pelvis, the anastomosis is performed by using end-to-end or end-to-
side anastomosis with circular transanal staplers.
Care should be taken to avoid tension on the anastomosis. Especially
in case several staple magazines have been used and thus staple lines
may overlap, the risk of a leakage increases. Sucient blood supply of
the bowel wall needs to be ensured (Braunschmid et al., 2017).
If the sigmoid alone is aected, and there is a dolichosigmoid (i.e.
elongated sigmoid), there is also the possibility to mobilize the intestine
and to exteriorise the aected segment through a mini laparotomy for
inspection and to perform segmental resection conventionally with a
hand-sewn anastomosis (Fig. 11).
With simultaneous resection of the dorsal vaginal fornix and intesti-
nal anastomosis, the application of an omentum flap may be consid-
ered, although the eect on postoperative infertility remains unclear.
At the end of the procedure, the rectal air test, or the injection of dye
(methylene blue) into the rectum may be used to control the quality
of colorectal suture and the absence of leakage.
A diverting stoma may temporarily be created in women with
concomitant rectal and vaginal sutures or with very deep anastomosis.
The use of a surgical drain close to the anastomosis is recommended.
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16 Working group of ESGE, ESHRE and WES et al.
Though a stoma does not always ensure primary healing, it reduces
the risk of a fistula formation with faecal peritonitis (Mabrouk et al.,
2015). An early closure of a stoma (4 weeks after surgery) is possible
in an uneventful postoperative process. However, performing a stoma
is related to specific complications and the need for additional proce-
dures to solve them (8.6% Clavien Dindo III complications in (Bonin
et al., 2019)); thus, the patients should be informed about these pre-
operatively.
Low anterior rectal resection. Before performing a colorectal resection,
the distance of the inferior border of the lowest bowel lesion to
the anal verge must be discussed pre-operatively. Indeed, the surgical
treatment of low rectal lesions (defined as 5–8 cm from the anal
verge) is associated with a higher risk of postoperative anastomotic
leaks (Ruo et al., 2010) and transient neurogenic bladder dysfunction
(Dousset et al., 2010). The patients should also be informed about the
risk of low anterior rectal resection syndrome (LARS) as this can have
significant negative consequences for gastrointestinal functioning and
overall postoperative quality of life.
A newer technique combining a laparoscopic and transanal approach
can be applied to remove the full thickness of the infiltrating endome-
trial nodules of the lower and middle rectum (Wolthuis et al., 2011;
Bridoux et al., 2012). This technique may reduce the risk of rectal
stenosis and denervation (Pronio et al., 2007;Goncalves et al., 2010;
Bridoux et al., 2012;Roman and Tuech, 2014).
Other intestinal interventions. Nodules involving the ileocecal valve, the
appendix, and the small intestine are often found next to rectosig-
moid lesions. Due to the multifocal and multicentric occurrence of
endometriosis, the entire intestine (appendix, small bowel, caecum and
ileocecal valve) should always be inspected.
The extent of this type of endometriosis is dicult to visualize
completely by laparoscopy. If suspected, mobilizing this entire intestinal
section will allow for it to be exteriorised through a mini-laparotomy
in the right lower abdomen or by extending the umbilical incision.
The resection is done conventionally (hand-sewn) or with stapler
technology.
Urinary tract endometriosis
Bladder endometriosis
DE of the bladder is often associated with an involvement of the
detrusor muscle and—rarely—infiltration of the mucosa (urothelium).
Involvement of the lower urinary tract is found in 0.2–2.5% of all DE
cases, although rates up to 52.6% have been reported (Knabben et al.,
2015;Acker et al., 2003;Le Tohic et al., 2009;Fadhlaoui et al., 2015).
Of these, bladder and ureteral lesions, respectively, occur in 25–85%
and 15–75% of the cases, while renal and urethral involvement is even
rarer (5%) (Acker et al., 2003;Carmignani et al., 2009;Fadhlaoui et al.,
2015;Badri et al., 2018).
Before starting surgery for bladder endometriosis, information on
the location of the lesion is important. The presence of hydronephrosis
provides additional information as to the potential involvement of the
ureters and the pelvic sidewall, respectively.
More details on imaging techniques and pre-operative procedures
are available in the section on pre-operative management. It must be
mentioned that, in a majority of cases, the pre-operative assessment
does not allow for accurate prediction of the feasibility of the ureterol-
ysis and the need for ureteral resection. Severe hydronephrosis with
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Figure 16 Deep endometriosis of the bladder.
Figure 17 DE of the bladder. The cystotomy was closed
transversally with 3–0 resorbable running suture. The nodule (3 cm
diameter) is presented with the forceps.
kidney atrophy may ultimately be due to ureteral extrinsic endometrio-
sis, which can be treated by ureterolysis.
Surgical management. The general initial steps of DE surgery also
apply for bladder endometriosis (Figs 16 and 17). The procedure
starts with the placement of a transurethral catheter. If cystoscopy
is not performed the day before surgery, the catheterization is
preceded by cystoscopy and the introduction of ureteral stents,
when needed. Bladder endometriosis is usually easily identifiable: the
bladder nodule may be immediately visible, or the round ligaments
may be pulled medially, obliterating the ventral compartment due to
fibrosis.
The dissection may start in the healthy peritoneum adjacent to the
nodule, either paravesically or between the bladder and the uterus,
depending on the size of the nodule or the adherence to the uterus
or round ligaments. However, the tissue planes may sometimes be
lost due to the disease, and the dissection may have to go through
fibrotic tissue. As with hysterectomy, the dorsal wall of the bladder
distally of the nodule needs to be found and dissected away from both
uterus and the ventral wall of the vagina, thus opening the vesico-vaginal
space. Special attention is needed if there is a history of Caesarean
section. Finally, a soft plane of connective tissue is reached indicating
the surgeon is distal of the nodule. The bladder is further mobilized
coming from both sides to ensure subsequent suturing without tension.
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Surgical treatment of deep endometriosis 17
Figure 18 Intrinsic endometriosis in the left ureter with
stenosis and hydronephrosis.
Figure 19 Segmental resection of the infiltrated part of
the ureter.
This step may be easier if the bladder is filled with at least 100 ml
sodium chloride solution (and methylene blue) as its contours become
more visible. When the nodule is isolated, and the bladder mobilized,
the nodule is grasped with traction and excised with macroscopically
free margins. It may be worth trying to resect the nodule from the
detrusor muscle, respecting the mucosa if the latter is not involved;
however, this is possible only in the minority of cases. On the other
hand, it is easier to control the dissection with an open bladder as
the definition of the resection margins from both inside and outside
is comfortable for the surgeon. Also, the trigone is directly visualized
to avoid ureteric damage in this manner.
After resection, the bladder defect is closed horizontally with a
running suture using 3–0 PDS, or another absorbable monofilament
material. There is no evidence for whether a mono- or double layer
suture results in a better outcome. If possible, only the detrusor is
sutured and the mucosa avoided. After the suture, the leak tightness of
the bladder is checked by filling it with 100 to 200 ml sodium chloride.
Leakages are managed by single stitches. After large bladder resection
the Retzius space may be opened to allow ‘a tension-free’ bladder
repair.
The complete resection of bladder lesions has its limitations when
the uterus is involved and has to be preserved for fertility. A Robinson-
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or easy-flow-drainage can be considered postoperatively for the first
24–48 h in order to have an early leakage detection.
In the case of bladder endometriosis close to the trigonum, ureteral
stents introduced before or during the procedure facilitate the excision
and closure procedure. A postoperative cystoscopy for inspection and
assessment of the suture after 10 days of drainage is recommended by
several authors (Rozsnyai et al., 2011;Antonelli, 2012;Maccagnano
et al., 2012;Darwish et al., 2017;Leone Roberti Maggiore et al.,
2017).
Traditionally, the transurethral resection with an electric loop of
intra-vesical endometriosis is performed by some urologists. However,
the disadvantage from our point of view is that only the tip of the
iceberg is removed while too large a part of the nodule remains
in situ. However, a cystoscopic approach may be combined with
the laparoscopic route, during the same procedure, in large bladder
nodules when limits are close to the ureter meatus in order to limit the
risk of an inadvertent injury to the intravesical segment of the ureter.
Postoperative management. If there is significant postoperative
haematuria, there may be a risk of catheter obstruction, and a
transurethral rinsing catheter can be placed for continuous rinsing.
If an intraperitoneal drainage was placed during the operation, it
should be removed on the first or second postoperative day.
The transurethral Foley catheter should remain in place for 8 to
10 days. Then, a radiological cystogram is highly recommended to
check the integrity of the suture. If the suture is sucient, the catheter
can be removed.
Before discharging the patient from hospital, the amount of post-
voiding urine is checked and an ultrasound of the kidneys is performed.
Ureteral stents can be removed after ∼6 weeks. Anticholinergic medi-
cation to reduce bladder irritability may be helpful while ureteric stents
remain in place. The management described (Ulrich and Schüller, 2018)
may especially be suitable for large resections. In patients with smaller
defects after resection (for example when the lesions are more distant
from the trigone or the ureteral ostia), the transurethral catheter can be
removed earlier, and the ureteral stents can be removed immediately
after suturing of the bladder, or not used at all.
Specific risks and complications of the resection of bladder endometriosis.
A typical risk of partial bladder resection is secondary haemorrhage
with bladder tamponade (i.e. large intravesical hematoma). This com-
plication can usually be managed by continuous irrigation through a
specific transurethral catheter, and a surgical revision is rarely required.
Following large partial bladder resection, a reduced bladder capacity
potentially aggravating the pre-existing problem may result.
In contrast to bowel surgery, insuciency of the suture with post-
operative leakage is less frequent in bladder surgery. This, however,
may lead to urinoma formation requiring drainage and surgical revision,
sometimes necessitating a long-lasting transurethral and/or suprapubic
catheter (and rarely a nephrostoma). Postoperative hydronephrosis
may occur by either accidental occlusion of the ureteral ostia (if the
suture was performed close to the ureteral ostia), or lack of proper
bladder emptying. This is usually prevented by the pre-operative place-
ment of ureteral stents (double J). The development of fistulas is
a complication of bladder and ureter surgery that can significantly
aect the quality of life. It is more likely if concomitant complex
urological, colorectal, and/or intestinal resections, or hysterectomies
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18 Working group of ESGE, ESHRE and WES et al.
Figure 20 Incision of the distal stump of the ureter in
order to increase the circumference in order to facilitate
the end to end anastomosis and to decrease the risk of a
post-operative stenosis formation.
are performed. The use of an omental flap can be considered in these
cases.
Ureteral endometriosis
Presentation and symptoms. Ureteral endometriosis is often the result
of pelvic sidewall endometriosis and is highly associated with DE
of the uterosacral ligaments. If the ureter is aected by endometri-
otic implants, fibrosis, and inflammatory reactions that are attached
to and consequently obstructing it from the outside, the situation
is referred to as extrinsic ureter endometriosis. The infiltration of
its muscular layer with or without reaching the lumen is defined as
intrinsic ureteral endometriosis. Either form may cause hydronephrosis
potentially leading to a complete loss of ipsilateral renal function.
Unfortunately, hydronephrosis is often undetected due to non-specific
or a lack of symptoms; only a minority of patients complain about
colic-like pain or discomfort of the flank (mostly with a left pre-
disposition) (Miranda-Mendoza et al., 2012). Hydronephrosis, due to
endometriosis-associated ureteral obstruction, is considered an abso-
lute indication for intervention if sucient kidney function still exists. If
kidney function is lost, however, nephrectomy is indicated. A multidis-
ciplinary review with the involvement of a urologist is recommended.
Surgical treatment. If ureteral endometriosis is already suspected pre-
operatively, and/or if hydronephrosis is present, a pre-operative trial
of ureteral stenting is recommended (Figs 18, 19, 20 and 21). During
any ureteral intervention, care should be taken to avoid damaging the
ureteral sheath within the vascular network (see the anatomy section).
Ureterolysis/Decompression In cases of extrinsic ureteral endo-
metriosis, ureterolysis is performed by freeing the ureter and excising
the surrounding fibrotic tissue. This may also be successful in cases with
the endometriosis reaching and infiltrating the adventitia—and even
the muscular layer if no relevant obstruction of the ureter is present.
Dissection of the ureter should be started in healthy tissue and not at
the aected location.
Segmental ureteral resection (end-to-end anastomosis) Segmental
resection with end-to-end anastomosis may be indicated—provided
that a tension-free anastomosis is possible—in cases after failed
ureterolysis or when an intrinsic ureteral lesion distant from the bladder
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Figure 21 Final view of the end-to-end anastomosis
(tension-free).
(i.e. in its upper sections) is present infiltrating the muscular layer with
obstruction of the lumen. Technically, complete mobilization of the
ends, spatulation and suturing over an introduced ureteral stent are
important for successful anastomosis. Interrupted sutures (e.g. 4–0
to 5–0, with monofilament material) are often used. The use of an
omental flap in order to protect the suture has been recommended
by some clinicians. In practice, this technique is feasible and safe
when the length of the ureter involved by the stenosis does not
exceed 1 cm: otherwise the tension-free anastomosis will not be
achievable.
Ureteral re-implantation (ureteroneocystostomy) Distal intrinsic
lesions close to the bladder, stenosis with a length exceeding 1 cm
or failed ureterolysis (i.e. hydronephrosis has recurred or is still
present after surgery) may require resection and re-implantation of
the proximal end of the ureter into the bladder. Most often, the
psoas-hitch technique is preferred. As with ureterolysis, mobilization
is started over the common iliac artery. Gentle dissection is continued
all the way down to the aected portion of the ureter in order to
protect the sheath with its blood supply. The ureter is transsected
above the lesion. The distal—now blind—end is tied and will stay in
situ. The bladder is mobilized entering the retropubic space (Retzius)
thus creating a flap-like side so that the bladder and the proximal end
of the ureter can be approximated. A cystotomy is performed at the
bladder dome. An oblique tunnel is created by introducing a clamp
into the bladder through that opening and advanced exactly to where
the ureter will be implanted, thus creating another small opening, and
the ureter will be pulled through that hole into the bladder. This is
often done submucosally. The ureter is stented and its end spatulated.
In the position described, the ureter is fixed to the bladder mucosa
with 4–0 monofilament single stitches. Finally, the bladder is closed
as previously described (see the bladder section) and a transurethral
and/or supra-pubic catheter placed. The ureteral pig-tail stent(s) will
be left in situ for ∼6 weeks (Ceccaroni et al., 2019). Whether a psoas
hitch or a Boari procedure is the best way of performing the ureteral re-
implantation (ureteroneocystostomy) may depend upon the situation
and the urologist’s preference.
After ureteral surgery for both intrinsic and extrinsic endometriosis,
or if conservati ve treatment is preferred while DE is suspected, patients
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Surgical treatment of deep endometriosis 19
should be monitored by kidney ultrasound every 6 months in order to
avoid overlooking silent hydronephrosis (Ulrich et al., 2014).
DE of the diaphragm
Techniques used
Superficial lesions can be coagulated or ablated with dierent types of
low-energy sources. The presence of larger lesions may afterwards be
associated with diaphragmatic fenestrations and therefore should be
managed by a multidisciplinary team (Roman et al., 2008). It should
be taken into account that only the ventral part of the diaphragm is
visible by laparoscopy performed in dorsal lithotomy position. The
left lateral decubitus position helps to have complete exposure of the
right diaphragmatic muscle and endometriosis (Bourdel et al., 2019).
The diaphragmatic fenestrations are usually present in the tendinous
(central) part of the diaphragm. These openings can lead to secondary
pneumothorax, serous or bloody pleural eusions or partial herniation
of the liver into the chest.
In the case of catamenial pneumothorax, video-assisted thoraco-
scopic surgery (VATS) is the approach of choice for diagnosis and
surgical treatment (Nezhat et al., 2007). In the case of lesions close
to the phrenic nerve, a mini-thoracotomy can be considered (Alifano
et al., 2007). Small fenestrations in the diaphragm can be closed with
staples or interrupted stitches, while bigger defects should be excised
and stitched. Especially in cases with large defects after resection, the
thoracoscopic suturing by a thoracic surgeon is preferable. Plication or
insertion of a mesh may be necessary in rare cases of larger diaphrag-
matic defects. ‘Blind’ pleurodesis with talc without diagnosing diaphrag-
matic fenestrations can later lead to entrapped lung and isolated basal
pneumothorax with persistent symptoms. Pleurodesis without excision
of the endometriotic nodules is followed by continued pain during
menstruation (Bagan et al., 2003). In a porous diaphragm, a polyglactin
mesh implantation improves the outcome (Bagan et al., 2003). If deep
lesions have been diagnosed without catamenial pneumothorax, a
laparoscopic approach is a viable alternative. A surgeon with thoracic
qualifications on standby is an essential prerequisite (Nezhat et al.,
1998;Nezhat et al., 2007). Women who complain of catamenial pain in
the (right) shoulder have diaphragmatic lesions until otherwise proven
by thoracoscopy and laparoscopy performed in left lateral decubitus
position. At thoracoscopy, only full thickness lesions are visible and
some infiltrative lesions are not visible from the thoracoscopic side.
Risks and complications
The diaphragm is very thin, and care should be taken to reduce the
possibility of entering the thoracic cavity, particularly on the left side
because of the proximity of the pericardium. Arrangements should
be in place to manage a pneumothorax and other complications.
Intra-operative placement of a pleural drain can solve the problem.
Risks of VATS include postoperative pneumothorax, damage to the
phrenic nerve, recurrences, postoperative haemothorax and necessity
for additional surgery due to concurrent pelvic endometriosis. The risks
and complications of laparoscopy are identical in the case of additional
VATS.
Prevention of complications
To limit the risk of pneumothorax, double lumen intubation is preferred
over single lumen intubation (Alifano et al., 2007;Ciriaco et al., 2009).
Intra-operative deflation after single lumen intubation has been used
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as an alternative; no comparative studies on this topic are available,
however. A chest tube should be left in situ for 2–6 days. When surgery
next to the phrenic nerve is necessary, a mini-thoracotomy can be
helpful (Alifano et al., 2007;Roman et al., 2016b). Recurrences can
be reduced through the use of a polyglactin mesh implantation and
postoperative GnRH analogue treatment (Bagan et al., 2003;Ciriaco
et al., 2009). If diaphragmatic endometriosis is found as the reason for
catamenial pneumothorax, pelvic endometriosis must be investigated
and excised.
When a patient does not want to have surgery or only incomplete
resection is possible, in case of catamenial pneumothorax, a bilateral
salpingo-oophorectomy may be considered if future fertility is not
desired.
DE of the abdominal wall including scars, the
umbilicus, and the inguinal region
Endometriosis can be found in the abdominal wall, especially in scars,
the umbilicus or the inguinal region. These lesions may be misinter-
preted as tumourous growths or keloids.
In abdominal scar endometriosis following laparotomy (fx. Cae-
sarean section) or laparoscopy (fx. trocar insertion sites), the preferred
method is wide excision.
A multidisciplinary approach may be required if a large defect needs
to be repaired following excision. The use of a polypropylene mesh can
be considered (Khan et al., 2017;Pas et al., 2017).
For umbilical endometriosis, a similar approach can be applied taking
into account cosmetic consequences (Siddiqui et al., 2017).
In endometriosis of the inguinal region, the proximity to other
structures (e.g. nerves and femoral vessels) should be considered and
a multidisciplinary approach is advised.
Risks and complications
Incomplete excision and herniation through the fascia or rectus muscle
have been reported. Women should be counselled about possible
unavoidable and undesirable cosmetic consequences.
Side eects from mesh cannot be excluded.
Nerve damage and pain after resection of inguinal endometriosis is
a risk.
Frozen pelvis and endometriosis
A frozen pelvis is considered the ultimate stage of deep endometriotic
lesions with fibrosis, severe adhesions and abnormal tissue replacing
pelvic soft tissue. It is defined as the presence of extensive dense
adhesions at one or both adnexae with complete dorsal cul-de-sac
obliteration. This definition may also include patients with severe
peritoneal adhesions only.
The surgical management of these patients remains a challenge, as
the risk of complications may be increased.
The basic principles of dissection are similar to those described
for bowel endometriosis, even though there may not be true bowel
endometriosis. For dicult cases and frozen pelvis, the general
principles as described in Table II apply, in addition to the following
principles:
•Try to mobilise the sigmoid colon.
•Identify the ureters and dissect if necessary.
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20 Working group of ESGE, ESHRE and WES et al.
•Follow the principles described in the specific chapters for the
treatment of the uterosacral ligaments and rectovaginal septum, or
urinary tract involvement.
Hysterectomy in women with severe DE
Hysterectomy together with removal of endometriotic lesions, with
or without oophorectomy, in women who have completed their family
and/or have no desire to become pregnant, may be indicated in certain
circumstances (Dunselman et al., 2014). Women should be carefully
counselled about this irreversible decision to have a healthy organ
removed, as well as the risks associated with a hysterectomy with
oophorectomy, including a higher risk of coronary heart disease (Mu
et al., 2016), congestive heart failure, obesity and high blood pressure
(Laughlin-Tommaso et al., 2018) as well as dementia (Rocca et al.,
2012). Furthermore, they should be informed that hysterectomy will
not necessarily cure the symptoms or the disease.
Hysterectomy for endometriosis is usually performed by the
abdominal route (laparoscopy or laparotomy) depending on the extent
of the disease. The laparoscopic route has the advantage of better
access, identification, division of adhesions and removal of non-uterine
endometriotic lesions. It may also facilitate vaginal hysterectomy
(LAVH) and ensure complete removal of all endometriotic lesions.
The general principles of laparoscopic hysterectomy should be
applied in women with DE (Einarsson and Suzuki, 2009), with some
specific recommendations.
Technical considerations
The principles of approach to deep endometriotic lesions should be
followed, as described in the previous sections.
It is usually easier to leave the uterus until the endometriotic
lesions are isolated or removed, but in certain situations performing
hysterectomy first may facilitate access to the lesions and their excision.
Sometimes an initial supracervical hysterectomy can precede the
removal of the cervix in case of, for example, a large uterus, or
to approach deep lesions. Treatment of the dorsal compartment
and hysterectomy should be performed carefully. The plane used to
excise the dorsal disease are the planes used in type B or C radical
hysterectomy (Querleu et al., 2017) whereas in most patients without
cardinal ligament involvement an intrafascial approach may be used to
remove an adenomyotic uterus.
Ligation of the uterine arteries. In the case of an enlarged uterus or
severe adhesions, consideration should be given to ligation of the
uterine arteries at their origin as this may reduce bleeding and be helpful
in the dissection of the ureter.
Treatment of rectal lesions. In the case of hysterectomy combined
with resection of bowel endometriosis (anastomosis or full thickness
resection), a temporary stoma can be considered.
Hysterectomy and bladder opening. In the case of the opening of the
bladder or resection of a bladder nodule, it is necessary to close the
wound with a tension-free suture and avoid apposition of the bladder
and vaginal vault by sucient mobilisation of the bladder wall. The
bladder should be drained with a catheter for 5 to 10 days.
Extraction of the uterus. If it is dicult to evacuate the uterus vagi-
nally, morcellation in a bag can be considered, to prevent parasitic
endometriosis.
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Ureteral stenting. In the case of parametrial involvement at hysterec-
tomy, the use of a stent may be helpful.
Caution of complications with hysterectomy in DE
Hysterectomy in the case of DE may be extremely challenging and
is known to be associated with intra-operative complications (4-fold
higher compared to normal hysterectomy): increased intra and postop-
erative risk of haemorrhage, and direct injuries (bowel, bladder, ureter)
due to dicult adhesiolysis (Uccella et al., 2016;Surrey et al., 2017).
It is particularly important to check the bowel and bladder integrity at
the end of the procedure in dicult cases where extensive dissection is
required. Adhesion prevention is to be considered in cases of extensive
dissection; hyalobarrier gel and other anti-adhesion agents can be used.
Conclusion
Surgery is an important treatment option for women with DE.
However, like medical intervention, surgery is not always successful
and is also associated with clinically relevant risks (Chapron et al.,
1998;Becker et al., 2017). Surgical treatment failure can be partially
attributed to the heterogeneity of endometriosis, but it is also
correlated with factors such as surgical experience, the complexity
of each case, and anatomical locations of the disease.
The principles for identifying and treating deep endometriotic lesions
(Table II) and the good practice recommendations in the text aim to
support clinicians and surgeons is counselling and treating (or referring)
women presenting with DE.
Supplementary data
Supplementary data are available at Human Reproduction Open online.
Acknowledgements
The working group would like to acknowledge the input of Prof. Dirk
Van Raemdonck, thoracic surgeon at University Hospitals Leuven (Bel-
gium) on the section on endometriosis of the diaphragm. Furthermore,
the working group would like to thank the experts that participated in
the stakeholder review for their valuable comments (list of experts
provided in Supplementary Table SI).
Authors’ roles
The working group was led by J.K. N.V. provided technical and admin-
istrative support. All other authors contributed equally in writing the
text, attending the meetings and discussing the content until there was
agreement within the group. All authors reviewed and approved of the
final version.
Funding
ESGE; ESHRE; WES.
Conict of interest
Dr Roman reports personal fees from ETHICON, PLASMASURGI-
CAL, OLYMPUS and NORDIC PHARMA, outside the submitted
work; Dr Becker reports grants from Bayer AG, Volition Rx, MDNA
Downloaded from https://academic.oup.com/hropen/article-abstract/2020/1/hoaa002/5733057 by guest on 12 February 2020
Surgical treatment of deep endometriosis 21
Life Sciences and Roche Diagnostics Inc., and other relationships or
activities from AbbVie Inc., and Myriad Inc., during the conduct of the
study; and Dr Tomassetti reports non-financial support from ESHRE,
during the conduct of the study and non-financial support and other
from Lumenis, Gedeon-Richter, Ferring Phar maceuticals and Merck SA,
outside the submitted work. The other authors had nothing to disclose.
References
Aas-Eng K, Salama M, Sevelda U, Ruesch C, Nemeth Z, Hudelist
G. Learning curve for detection of the distal part of ureters by
transvaginal sonography (TVS): a feasibility study. Ultrasound Obstet
Gynecol 2019.
Abdalla AL. S. K. Development and Validation of a New Visual Numeric
Endometriosis Surgical Score for Assessment of Pelvic Endometriosis
Using Videotaped Laparoscopic Procedures [Thesis]. UK: University of
Surrey, 2015.
Abrao MS, Borrelli GM, Clarizia R, Kho RM, Ceccaroni M. Strategies
for Management of Colorectal Endometriosis. Semin Reprod Med
2017;35:65–71.
Abrao MS, Petraglia F, Falcone T, Keckstein J, Osuga Y, Chapron
C. Deep endometriosis infiltrating the recto-sigmoid: critical fac-
tors to consider before management. Hum Reprod Update 2015;
21:329–339.
Acker O, Robert Y, Carpentier F, Vinatier D, Cosson M. Symptomatic
bladder or ureteral endometriosis: report of 8 cases and review of
the literature. Ann Chir 2003;128:34–39.
Adamson GD. Endometriosis Fertility Index: is it better than the
present staging systems? Curr Opin Obstet Gynecol 2013;25:186–192.
Adamson GD, Kennedy SH, Hummelshoj L. Creating solutions in
endometriosis: global collaboration through the World Endometrio-
sis Research Foundation. J Endometriosis 2010;2:4–6.
Adamson GD, Pasta DJ. Endometriosis fertility index: the new,
validated endometriosis staging system. Fertil Steril 2010;94:
1609–1615.
Adamyan L. Additional international perspectives. In: Dh N (ed).
Gynecologic and Obstetric Surgery. St. Louis: Mosby Year Book, 1993,
1167–1182.
Alifano M, Jablonski C, Kadiri H, Falcoz P, Gompel A, Camilleri-Broet S,
Regnard JF. Catamenial and noncatamenial, endometriosis-related or
nonendometriosis-related pneumothorax referred for surgery. Am J
Respir Crit Care Med 2007;176:1048–1053.
Antonelli A. Urinary tract endometriosis. Urologia 2012;79:167–170.
Badri AV, Jennings R, Patel P, Eun DD. Renal endometriosis: the case
of an endometrial implant mimicking a renal mass. J Endourol Case
Rep 2018;4:176–178.
Bagan P, Le Pimpec Barthes F, Assouad J, Souilamas R, Riquet M. Cata-
menial pneumothorax: retrospective study of surgical treatment. Ann
Thorac Surg 2003;75:378–381 discusssion 381.
Bar-Shavit Y, Jaillet L, Chauvet P, Canis M, Bourdel N. Use of
indocyanine green in endometriosis surgery. Fertil Steril 2018;109:
1136–1137.
Barry MJ, Fowler FJ, O’Leary MP, Bruskewitz RC, Holtgrewe HL,
Mebust WK, Cockett AT. Association∗MCotAU. The American
Urological Association symptom index for benign prostatic hyper-
plasia. J Urol 1992;148:1549–1557.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
Bazot M, Darai E. Diagnosis of deep endometriosis: clinical exam-
ination, ultrasonography, magnetic resonance imaging, and other
techniques. Fertil Steril 2017;108:886–894.
Bazot M, Lafont C, Rouzier R, Roseau G, Thomassin-Naggara I,
Darai E. Diagnostic accuracy of physical examination, transvagi-
nal sonography, rectal endoscopic sonography, and magnetic reso-
nance imaging to diagnose deep infiltrating endometriosis. Fertil Steril
2009;92:1825–1833.
Becker CM, Gattrell WT, Gude K, Singh SS. Reevaluating response and
failure of medical treatment of endometriosis: a systematic review.
Fertil Steril 2017;108:125–136.
Bolton H. The Montgomery ruling extends patient autonomy. BJOG
2015;122:1273.
Bonin E, Bridoux V, Chati R, Kermiche S, Coget J, Tuech JJ,
Roman H. Diverting stoma-related complications following colorec-
tal endometriosis surgery: a 163-patient cohort. Eur J Obstet Gynecol
Reprod Biol 2019;232:46–53.
Bouquet de Joliniere J, Major A, Ayoubi JM, Cabry R, Khomsi F, Lesec
G, Frydman R, Feki A. It is necessary to purpose an add-on to
the American classification of endometriosis? This disease can be
compared to a malignant proliferation while remaining benign in most
cases. EndoGram(R) is a new profile witness of its evolutionary
potential. Front Surg 2019;6:27.
Bourdel N, Alves J, Pickering G, Ramilo I, Roman H, Canis M. System-
atic review of endometriosis pain assessment: how to choose a scale?
Hum Reprod Update 2015;21:136–152.
Bourdel N, Comptour A, Bouchet P, Gremeau AS, Pouly JL, Slim K,
Pereira B, Canis M. Long-term evaluation of painful symptoms and
fertility after surgery for large rectovaginal endometriosis nodule: a
retrospective study. Acta Obstet Gynecol Scand 2018;97:158–167.
Bourdel N, Fava V, Budianu MA, Chauvet P, Canis M, Chadeyras JB.
Laparoscopic resection of diaphragmatic endometriosis in 10 steps.
J Minim Invasive Gynecol 2019;26:1224–1225.
Braunschmid T, Hartig N, Baumann L, Dauser B, Herbst F. Influence
of multiple stapler firings used for rectal division on colorectal
anastomotic leak rate. Surg Endosc 2017;31:5318–5326.
Bridoux V, Roman H, Kianifard B, Vassilie M, Marpeau L, Michot F,
Tuech JJ. Combined transanal and laparoscopic approach for the
treatment of deep endometriosis infiltrating the rectum. Hum Reprod
2012;27:418–426.
Byrne D, Curnow T, Smith P, Cutner A, Saridogan E, Clark TJ, Cen-
tres BE. Laparoscopic excision of deep rectovaginal endometriosis
in BSGE endometriosis centres: a multicentre prospective cohort
study. BMJ Open 2018;8:e018924.
Carfagna P, De Cicco Nardone C, De Cicco Nardone A, Testa AC,
Scambia G, Marana R, De Cicco Nardone F. Role of transvaginal
ultrasound in evaluation of ureteral involvement in deep infiltrating
endometriosis. Ultrasound Obstet Gynecol 2018;51:550–555.
Carmignani L, Ronchetti A, Amicarelli F, Vercellini P, Spinelli M, Fedele
L. Bladder psoas hitch in hydronephrosis due to pelvic endometrio-
sis: outcome of urodynamic parameters. Fertil Steril 2009;92:
35–40.
Ceccaroni M, Ceccarello M, Cale G, Clarizia R, Scarperi S, Pastorello
M, Molinari A, Ruo G, Cavalleri S. Total laparoscopic uretero-
neocystostomy for ureteral endometriosis: a single-center experi-
ence of 160 consecutive patients. J Minim Invasive Gynecol 2019;26:
78–86.
Downloaded from https://academic.oup.com/hropen/article-abstract/2020/1/hoaa002/5733057 by guest on 12 February 2020
22 Working group of ESGE, ESHRE and WES et al.
Ceccaroni M, Roviglione G, Giampaolino P, Clarizia R, Bruni F, Ruo G,
Patrelli TS, De Placido G, Minelli L. Laparoscopic surgical treatment
of diaphragmatic endometriosis: a 7-year single-institution retro-
spective review. Surg Endosc 2012;27:625–632.
Ceccaroni M, Roviglione G, Mautone D, Clarizia R. Anatomical land-
marks in deep endometriosis surgery. In: Minimally Invasive Gynecol-
ogy. Springer, 2018,45–59.
Chapron C, Fauconnier A, Vieira M, Barakat H, Dousset B, Pansini V,
Vacher-Lavenu MC, Dubuisson JB. Anatomical distribution of deeply
infiltrating endometriosis: surgical implications and proposition for a
classification. Hum Reprod 2003;18:157–161.
Chapron C, Querleu D, Bruhat MA, Madelenat P, Fernandez H, Pierre
F, Dubuisson JB. Surgical complications of diagnostic and operative
gynaecological laparoscopy: a series of 29,966 cases. Hum Reprod
1998;13:867–872.
Chattot C, Huchon C, Paternostre A, Du Cheyron J, Chouillard E,
Fauconnier A. ENDORECT: a preoperative score to accurately
predict rectosigmoid involvement in patients with endometriosis.
Hum Reprod Open 2019;2019: hoz007.
Chiantera V, Petrillo M, Abesadze E, Sozzi G, Dessole M, Catello Di
Donna M, Scambia G, Sehouli J, Mechsner S. Laparoscopic neuron-
avigation for deep lateral pelvic endometriosis: clinical and surgical
implications. J Minim Invasive Gynecol 2018;25:1217–1223.
Ciriaco P, Negri G, Libretti L, Carretta A, Melloni G, Casiraghi M,
Bandiera A, Zannini P. Surgical treatment of catamenial pneumotho-
rax: a single centre experience. Interact Cardiovasc Thorac Surg 2009;
8:349–352.
Collinet P, Marcelli F, Villers A, Regis C, Lucot JP, Cosson M, Vinatier
D. Management of endometriosis of the urinary tract. Gynecol Obstet
Fertil 2006;34:347–352.
Condous G, Van Calster B, Van Huel S, Lam A. What is the value
of preoperative bimanual pelvic examination in women undergoing
laparoscopic total hysterectomy? J Minim Invasive Gynecol 2007;
14:334–338.
Cornillie FJ, Oosterlynck D, Lauweryns JM, Koninckx PR. Deeply
infiltrating pelvic endometriosis: histology and clinical significance.
Fertil Steril 1990;53:978–983.
Cullen TS. Adenomyoma of the round ligament. Bull Johns Hopkins
Hosp 1896;7:112–114.
Darwish B, Stochino-Loi E, Pasquier G, Dugardin F, Defortescu G,
Abo C, Roman H. Surgical outcomes of urinary tract deep infiltrating
endometriosis. J Minim Invasive Gynecol 2017;24:998–1006.
de Lapasse C, Renouvel F, Chis C, Grosdemouge I, Panel P. Urinary
functional and urodynamic preoperative evaluation of patients with
deep pelvic surgical endometriosis: about 12 cases. Gynecol Obstet
Fertil 2008;36:272–277.
De Neef A, Cadiere GB, Bourgeois P, Barbieux R, Dapri G, Fastrez
M. Fluorescence of deep infiltrating endometriosis during laparo-
scopic surgery: a preliminary report on 6 cases. Surg Innov 2018;
25:450–454.
Donnez O, Roman H. Choosing the right surgical technique for deep
endometriosis: shaving, disc excision, or bowel resection? Fertil Steril
2017;108:931–942.
Dousset B, Leconte M, Borghese B, Millischer AE, Roseau G, Ark-
wright S, Chapron C. Complete surgery for low rectal endometrio-
sis: long-term results of a 100-case prospective study. Ann Surg
2010;251:887–895.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
Duy JM, Arambage K, Correa FJ, Olive D, Farquhar C, Garry R,
Barlow DH, Jacobson TZ. Laparoscopic surgery for endometriosis.
Cochrane Database Syst Rev 2014;CD011031.
Dunselman GA, Vermeulen N, Becker C, Calhaz-Jorge C, D’Hooghe T,
De Bie B, Heikinheimo O, Horne AW, Kiesel L, Nap A et al. ESHRE
guideline: management of women with endometriosis. Hum Reprod
2014;29:400–412.
Einarsson JI, Suzuki Y. Total laparoscopic hysterectomy: 10 steps
toward a successful procedure. Rev Obstet Gynecol 2009;2:
57–64.
Einarsson JI, Wattiez A. Minimally Invasive Gynecologic Surgery: Evidence-
Based Laparoscopic, Hysteroscopic & Robotic Surgeries, 2016, JP Medi-
cal Ltd.
Eskenazi B, Warner M, Bonsignore L, Olive D, Samuels S, Vercellini
P. Validation study of nonsurgical diagnosis of endometriosis. Fertil
Steril 2001;76:929–935.
Exacoustos C, Malzoni M, Di Giovanni A, Lazzeri L, Tosti C, Petraglia F,
Zupi E. Ultrasound mapping system for the surgical management of
deep infiltrating endometriosis. Fertil Steril 2014;102:143–150 e142.
Exacoustos C, Zupi E, Piccione E. Ultrasound imaging for ovarian and
deep infiltrating endometriosis. Semin Reprod Med 2017;35:5–24.
Fadhlaoui A, Gillon T, Lebbi I, Bouquet de Joliniere J, Feki A.
Endometriosis and vesico-sphincteral disorders. Front Surg 2015;
2:23.
Ferrero S, Biscaldi E, Morotti M, Venturini PL, Remorgida V, Rollandi
GA, Valenzano Menada M. Multidetector computerized tomography
enteroclysis vs. rectal water contrast transvaginal ultrasonography
in determining the presence and extent of bowel endometriosis.
Ultrasound Obstet Gynecol 2011;37:603–613.
Goncalves MO, Podgaec S, Dias JA Jr, Gonzalez M, Abrao MS.
Transvaginal ultrasonography with bowel preparation is able to
predict the number of lesions and rectosigmoid layers aected in
cases of deep endometriosis, defining surgical strategy. Hum Reprod
2010;25:665–671.
Gould MK, Garcia DA, Wren SM, Karanicolas PJ, Arcelus JI, Heit JA,
Samama CM. Prevention of VTE in nonorthopedic surgical patients:
antithrombotic therapy and prevention of thrombosis, 9th ed: Amer-
ican College of Chest Physicians Evidence-Based Clinical Practice
Guidelines. Chest 2012;141:e227S–e277S.
Grammatico D, Gonzalez A, Nicholson R, Rolla E. Endometrio-
sis: a correlation between high resolution nuclear magnetic reso-
nance and laparoscopic findings. In: 13TH WORLD CONGRESS on
ENDOMETRIOSIS, 2017.
Guenaga KF, Matos D, Wille-Jorgensen P. Mechanical bowel prepara-
tion for elective colorectal surgery. Cochrane Database Syst Rev 2011;
Cd001544.
Guerriero S, Condous G, van den Bosch T, Valentin L, Leone FP, Van
Schoubroeck D, Exacoustos C, Installe AJ, Martins WP, Abrao MS
et al. Systematic approach to sonographic evaluation of the pelvis
in women with suspected endometriosis, including terms, definitions
and measurements: a consensus opinion from the International Deep
Endometriosis Analysis (IDEA) group. Ultrasound Obstet Gynecol
2016;48:318–332.
Guerriero S, Saba L, Pascual MA, Ajossa S, Rodriguez I, Mais V,
Alcazar JL. Transvaginal ultrasound vs magnetic resonance imaging
for diagnosing deep infiltrating endometriosis: systematic review and
meta-analysis. Ultrasound Obstet Gynecol 2018;51:586–595.
Downloaded from https://academic.oup.com/hropen/article-abstract/2020/1/hoaa002/5733057 by guest on 12 February 2020
Surgical treatment of deep endometriosis 23
Haas D, Chvatal R, Habelsberger A, Schimetta W, Wayand W,
Shamiyeh A, Oppelt P. Preoperative planning of surgery for deeply
infiltrating endometriosis using the ENZIAN classification. Eur J
Obstet Gynecol Reprod Biol 2013a;166:99–103.
Haas D, Shebl O, Shamiyeh A, Oppelt P. The rASRM score and the
Enzian classification for endometriosis: their strengths and weak-
nesses. Acta Obstet Gynecol Scand 2013b;92:3–7.
Haas D, Wurm P, Shamiyeh A, Shebl O, Chvatal R, Oppelt P. Ecacy
of the revised Enzian classification: a retrospective analysis. Does the
revised Enzian classification solve the problem of duplicate classifica-
tion in rASRM and Enzian? Arch Gynecol Obstet 2013c;287:941–945.
Hsu AL, Sinaii N, Segars J, Nieman LK, Stratton P. Relating pelvic
pain location to surgical findings of endometriosis. Obstet Gynecol
2011;118:223–230.
Hudelist G, Aas-Eng MK, Birsan T, Berger F, Sevelda U, Kirchner L,
Salama M, Dauser B. Pain and fertility outcomes of nerve-sparing,
full-thickness disk or segmental bowel resection for deep infiltrating
endometriosis-a prospective cohort study. Acta Obstet Gynecol Scand
2018;97:1438–1446.
Hudelist G, English J, Thomas AE, Tinelli A, Singer CF, Keckstein
J. Diagnostic accuracy of transvaginal ultrasound for non-invasive
diagnosis of bowel endometriosis: systematic review and meta-
analysis. Ultrasound Obstet Gynecol 2011;37:257–263.
Hudelist G, Tuttlies F, Rauter G, Pucher S, Keckstein J. Can transvaginal
sonography predict infiltration depth in patients with deep infiltrating
endometriosis of the rectum? Hum Reprod 2009;24:1012–1017.
Jackson S, Donovan J, Brookes S, Eckford S, Swithinbank L, Abrams
P. The Bristol female lower urinary tract symptoms questionnaire:
development and psychometric testing. Br J Urol 1996;77:805–812.
Johnson NP, Hummelshoj L, Adamson GD, Keckstein J, Taylor HS,
Abrao MS, Bush D, Kiesel L, Tamimi R, Sharpe-Timms KL et al.
World Endometriosis Society consensus on the classification of
endometriosis. Hum Reprod 2017;32:315–324.
Johnson NP, Hummelshoj L. World Endometriosis Society Montpel-
lier C. Consensus on current management of endometriosis. Hum
Reprod 2013;28:1552–1568.
Keckstein J. The ENZIAN Classification of Deep Infiltrating
Endometriosis. In: Liselotte Mettler IA, Keckstein J, Meinhold-
Heerlein I (eds). Endometriosis: A Concise Practical Guide to Current
Diagnosis and Treatment. Tuttlingen: EndoPress, 2017,44–56.
Keckstein J, Hucke J. Die endoskopischen Operationen in der Gynäkologie,
1st edn. Urban & Fischer Verlag/Elsevier GmbH, munich, 2000.
Keckstein J, Ulrich U, Kandolf O, Wiesinger H, Wustlich M. Laparo-
scopic therapy of intestinal endometriosis and the ranking of drug
treatment. Zentralbl Gynakol 2003a;125:259–266.
Keckstein J, Ulrich U, Possover M, Schweppe KW. ENZIAN-
Klassifikation der tief infiltrierenden Endometriose. Zentralblatt fur
Gynakologie 2003b;125:291.
Keckstein J, Wiesinger H. "Deep endometriosis, including intestinal
involvement–the interdisciplinary approach.". Minim Invasive Ther
Allied Technol 2005;14:160–166.
Khan Z, Zanfagnin V, El-Nashar SA, Famuyide AO, Daftary GS,
Hopkins MR. Risk factors, clinical presentation, and outcomes
for abdominal wall endometriosis. J Minim Invasive Gynecol
2017;24:478–484.
Knabben L, Imboden S, Fellmann B, Nirgianakis K, Kuhn A, Mueller
MD. Urinary tract endometriosis in patients with deep infiltrating
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
endometriosis: prevalence, symptoms, management, and proposal
for a new clinical classification. Fertil Steril 2015;103:147–152.
Kondo W, Bourdel N, Jardon K, Tamburro S, Cavoli D, Matsuzaki S,
Botchorishvili R, Rabischong B, Pouly JL, Mage G et al. Comparison
between standard and reverse laparoscopic techniques for rectovagi-
nal endometriosis. Surg Endosc 2011;25:2711–2717.
Kondo W, Ribeiro R, Zomer MT, Hayashi R. Laparoscopic double
discoid resection with a circular stapler for bowel endometriosis.
J Minim Invasive Gynecol 2015;22:929–931.
Koninckx PR, Meuleman C, Oosterlynck D, Cornillie FJ. Diagnosis of
deep endometriosis by clinical examination during menstruation and
plasma CA-125 concentration. Fertil Steril 1996;65:280–287.
Koninckx PR, Ussia A, Adamyan L, Wattiez A, Donnez J. Deep
endometriosis: definition, diagnosis, and treatment. Fertil Steril 2012;
98:564–571.
Laughlin-Tommaso SK, Khan Z, Weaver AL, Smith CY, Rocca WA,
Stewart EA. Cardiovascular and metabolic morbidity after hysterec-
tomy with ovarian conservation: a cohort study. Menopause (New
York, NY) 2018;25:483–492.
Le Tohic A, Chis C, Yazbeck C, Koskas M, Madelenat P, Panel P. Bladder
endometriosis: diagnosis and treatment. A series of 24 patients.
Gynecol Obstet Fertil 2009;37:216–221.
Leone Roberti Maggiore U, Ferrero S, Candiani M, Somigliana E,
Vigano P, Vercellini P. Bladder endometriosis: a systematic review
of pathogenesis, diagnosis, treatment, impact on fertility, and risk of
malignant transformation. Eur Urol 2017;71:790–807.
Lusuardi L, Hager M, Sieberer M, Schatz T, Kloss B, Hruby S, Jeschke
S, Janetschek G. Laparoscopic treatment of intrinsic endometriosis
of the urinary tract and proposal of a treatment scheme for ureteral
endometriosis. Urology 2012;80:1033–1038.
Mabrouk M, Clarizia R, Grassi T, Ruo G, Roviglione G, Bruni F,
Pontrelli G, Scarperi S, Rettore L, Rossini R. Protective ileostomy in
colorectal resection for endometriosis: is it truly protective? J Minim
Invasive Gynecol 2015;22:S177.
Maccagnano C, Pellucchi F, Rocchini L, Ghezzi M, Scattoni V, Mon-
torsi F, Rigatti P, Colombo R. Diagnosis and treatment of bladder
endometriosis: state of the art. Urol Int 2012;89:249–258.
Martin DC, Hubert GD, Levy B. Depth of infiltration of endometriosis.
J Gynecol Surg 1989;5:55–59.
McDermott FD, Arora S, Smith J, Steele RJC, Carlson GL, Winter DC,
(on behalf of the joint ASGBI/ACPGBI Anastomotic Leakage Work-
ing Group). PREVENTION, DIAGNOSIS AND MANAGEMENT
OF COLORECTAL ANASTOMOTIC LEAKAGE. 2016.
Mehedintu C, Brinduse LA, Bratila E, Monroc M, Lemercier E, Suaud O,
Collet-Savoye C, Roman H. Does computed tomography-based vir-
tual colonoscopy improve the accuracy of preoperative assessment
based on magnetic resonance imaging in women managed for col-
orectal endometriosis? J Minim Invasive Gynecol 2018;25:1009–1017.
Miranda-Mendoza I, Kovoor E, Nassif J, Ferreira H, Wattiez A. Laparo-
scopic surgery for severe ureteric endometriosis. Eur J Obstet Gynecol
Reprod Biol 2012;165:275–279.
Montanari E, Dauser B, Keckstein J, Kirchner E, Nemeth Z, Hudelist G.
Association between disease extent and pain symptoms in patients
with deep infiltrating endometriosis. Reprod Biomed Online 2019;
39:845–851.
Morgan-Ortiz F, Lopez-de la Torre MA, Lopez-Zepeda MA, Morgan-
Ruiz FV, Ortiz-Bojorquez JC, Bolivar-Rodriguez MA. Clinical char-
Downloaded from https://academic.oup.com/hropen/article-abstract/2020/1/hoaa002/5733057 by guest on 12 February 2020
24 Working group of ESGE, ESHRE and WES et al.
acteristics and location of lesions in patients with deep infiltrating
endometriosis using the revised Enzian classification. J Turk Ger
Gynecol Assoc 2019;20:133–137.
Mu F, Rich-Edwards J, Rimm EB, Spiegelman D, Missmer SA.
Endometriosis and risk of coronary heart disease. Circ Cardiovasc
Qual Outcomes 2016;9:257–264.
Nezhat C, Nezhat C, Seidman D, Berker B, Nezhat F. An expert forum
for the histology of endometriomas. Fertil Steril 2007;88:1017–1018
author reply 1018-1019.
Nezhat C, Seidman DS, Nezhat F, Nezhat C. Laparoscopic surgi-
cal management of diaphragmatic endometriosis. Fertil Steril 1998;
69:1048–1055.
Nisenblat V, Bossuyt PM, Farquhar C, Johnson N, Hull ML. Imaging
modalities for the non-invasive diagnosis of endometriosis. Cochrane
Database Syst Rev 2016;2:CD009591.
Nisolle M, Donnez J. Peritoneal endometriosis, ovarian endometriosis,
and adenomyotic nodules of the rectovaginal septum are three
dierent entities. Fertil Steril 1997;68:585–596.
Oliveira MA, Pereira TR, Gilbert A, Tulandi T, de Oliveira HC, De
Wilde RL. Bowel complications in endometriosis surgery. Best Pract
Res Clin Obstet Gynaecol 2016;35:51–62.
Pas K, Joanna SM, Renata R, Skret A, Barnas E. Prospective study
concerning 71 cases of caesarean scar endometriosis (CSE). J Obstet
Gynaecol 2017;37:775–778.
Phillips DI, Divall JM, Maskell RM, Barker DJ. A geographical focus of
duplex ureter. Br J Urol 1987;60:329–331.
Platell C, Barwood N, Makin G. Randomized clinical trial of bowel
preparation with a single phosphate enema or polyethylene glycol
before elective colorectal surgery. Br J Surg 2006;93:427–433.
Possover M. Pathophysiologic explanation for bladder retention in
patients after laparoscopic surgery for deeply infiltrating rectovaginal
and/or parametric endometriosis. Fertil Steril 2014;101:754–758.
Possover M, Diebolder H, Plaul K, Schneider A. Laparascopically
assisted vaginal resection of rectovaginal endometriosis. Obstet
Gynecol 2000;96:304–307.
Possover M, Forman A, Rabischong B, Lemos N, Chiantera V. Neu-
ropelveology: new groundbreaking discipline in medicine. J Minim
Invasive Gynecol 2015;22:1140–1141.
Possover M, Schneider T, Henle KP. Laparoscopic therapy for
endometriosis and vascular entrapment of sacral plexus. Fertil Steril
2011;95:756–758.
Pronio A, Di Filippo A, Narilli P, Mancini B, Caporilli D, Piroli S, Vestri A,
Montesani C. Anastomotic dehiscence in colorectal surgery. Analysis
of 1290 patients. Chir Ital 2007;59:599–609.
Puntambekar S, Manchanda R. Surgical pelvic anatomy in gynecologic
oncology. Int J Gynaecol Obstet 2018;143:86–92.
Querleu D, Cibula D, Abu-Rustum NR. 2017 update on the Quer-
leu–Morrow classification of radical hysterectomy. Ann Surg Oncol
2017;24:3406–3412.
Rabischong B, Botchorishvili R, Bourdel N, Curinier S, Campagne-
Loiseau S, Pouly JL, Canis M. Nerve sparing techniques in deep
endometriosis surgery to prevent urinary or digestive functional dis-
orders: techniques and results: CNGOF-HAS Endometriosis Guide-
lines. Gynecol Obstet Fertil Senol 2018;46:309–313.
Ripps BA, Martin DC. Correlation of focal pelvic tenderness with
implant dimension and stage of endometriosis. J Reprod Med 1992;
37:620–624.
.
.
.
.
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.
.
Rocca WA, Grossardt BR, Shuster LT, Stewart EA. Hysterectomy,
oophorectomy, estrogen, and the risk of dementia. Neurodegener Dis
2012;10:175–178.
Rokitansky C. Über Uterusdrüsen-Neubildungen in uterus- und Ovar-
ial Sarcomen. Zeitschrift der Kaiserlich Koenigl Gesellschaft der Aerzte
zu Wien 1860;37:577–581.
Roman H. Rectal shaving using PlasmaJet in deep endometriosis of the
rectum. Fertil Steril 2013;100:e33.
Roman H, Abo C, Huet E, Tuech JJ. Deep shaving and transanal disc
excision in large endometriosis of mid and lower rectum: the Rouen
technique. Surg Endosc 2016a;30:2626–2627.
Roman H, Chanavaz-Lacheray I, Scotté M, Marpeau L. Laparoscopic
management of diaphragm endometriosis. J Minim Invasive Gynecol
2008;15:151S.
Roman H, Darwish B, Provost D, Baste JM. Laparoscopic management
of diaphragmatic endometriosis by three dierent approaches. Fertil
Steril 2016b;106:e1.
Roman H, Tuech JJ. New disc excision procedure for low and mid rectal
endometriosis nodules using combined transanal and laparoscopic
approach. Colorectal Dis 2014;16:O253–O256.
Rozsnyai F, Roman H, Resch B, Dugardin F, Berrocal J, Descargues
G, Schmied R, Boukerrou M, Marpeau L, Group CS. Outcomes of
surgical management of deep infiltrating endometriosis of the ureter
and urinary bladder. JSLS 2011;15:439–447.
Ruo G, Scopelliti F, Scioscia M, Ceccaroni M, Mainardi P, Minelli L.
Laparoscopic colorectal resection for deep infiltrating endometriosis:
analysis of 436 cases. Surg Endosc 2010;24:63–67.
Schliep KC, Mumford SL, Peterson CM, Chen Z, Johnstone EB,
Sharp HT, Stanford JB, Hammoud AO, Sun L, Buck Louis GM.
Pain typology and incident endometriosis. Hum Reprod 2015;30:
2427–2438.
Seracchioli R, Raimondo D, Arena A, Zanello M, Mabrouk M. Clinical
use of endovenous indocyanine green during rectosigmoid segmen-
tal resection for endometriosis. Fertil Steril 2018;109:1135.
Shen R, Zhang Y, Wang T. Indocyanine green fluorescence angiog-
raphy and the incidence of anastomotic leak after colorectal
resection for colorectal cancer: a meta-analysis. Dis Colon Rectum
2018;61:1228–1234.
Siddiqui ZA, Husain F, Siddiqui Z, Siddiqui M. Port site endometrioma:
a rare cause of abdominal wall pain following laparoscopic surgery.
BMJ Case Rep 2017;2017.
Stiftung Endometriose Forschung (Foundation for Endometriosis
Research). The revised Enzian classification. Consensus meeting, 7th
Conference of the Stiftung Endometriose Forschung (Foundation
for Endometriosis Research), Hotel Enzian, Weissensee, Austria.
In: Weissensee, Austria: Stiftung Endometriose Forschung (SEF), 2011,
2011.
Surrey ES, Soliman AM, Yang H, Du EX, Su B. Treatment patterns, com-
plications, and health care utilization among endometriosis patients
undergoing a laparoscopy or a hysterectomy: a retrospective claims
analysis. Adv Ther 2017;34:2436–2451.
Tomassetti C, Meuleman C, Vanacker B, D’Hooghe T. Lower limb
compartment syndrome as a complication of laparoscopic laser
surgery for severe endometriosis. Fertil Steril 2009;2038:e2039–
e2012.
Trippia CH, Zomer MT, Terazaki CR, Martin RL, Ribeiro R, Kondo
W. Relevance of imaging examinations in the surgical planning of
Downloaded from https://academic.oup.com/hropen/article-abstract/2020/1/hoaa002/5733057 by guest on 12 February 2020
Surgical treatment of deep endometriosis 25
patients with bowel endometriosis. Clin Med Insights Reprod Health
2016;10:1–8.
Tsui KH, Lee FK, Seow KM, Chang WC, Wang JW, Chen SU, Chao
HT, Yen MS, Wang PH. Conservative surgical treatment of adeno-
myosis to improve fertility: controversial values, indications, compli-
cations, and pregnancy outcomes. Taiwan J Obstet Gynecol 2015;54:
635–640.
Tuttlies F, Keckstein J, Ulrich U, Possover M, Schweppe KW, Wustlich
M, Buchweitz O, Greb R, Kandolf O, Mangold R et al. ENZIAN-
score, a classification of deep infiltrating endometriosis. Zentralblatt
fur Gynakologie 2005;127:275–281.
Uccella S, Marconi N, Casarin J, Ceccaroni M, Boni L, Sturla D, Serati M,
Carollo S, Podesta’ Alluvion C, Ghezzi F. Impact of endometriosis on
surgical outcomes and complications of total laparoscopic hysterec-
tomy. Arch Gynecol Obstet 2016;294:771–778.
Ulrich U, Buchweitz O, Greb R, Keckstein J, von Leern I, Oppelt P,
Renner SP, Sillem M, Stummvoll W, De Wilde RL et al. National
German Guideline (S2k): guideline for the diagnosis and treatment
of endometriosis: long version - AWMF registry no. 015-045.
Geburtshilfe Frauenheilkd 2014;74:1104–1118.
Ulrich UA, Schüller J. Tief infiltrierende Endometriose: Blase. In: Solo-
mayer EF, Juhasz-Böss I (eds). Kursbuch Gynäkologische Endoskopie.
Georg Thieme Verlag KG Stuttgart, New York, 2018.
van der Wat J, Kaplan MD, Roman H, Da Costa C. The
use of modified virtual colonoscopy to structure a descriptive
imaging classification with implied severity for rectogenital and
disseminated endometriosis. J Minim Invasive Gynecol 2013;20:
543–546.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
Vanhie A, Meuleman C, Tomassetti C, Timmerman D, D’Hoore A,
Wolthuis A, Van Cleynenbreugel B, Dancet E, Van den Broeck U,
Tsaltas J et al. Consensus on recording deep endometriosis surgery:
the CORDES statement. Hum Reprod 2016;31:1219–1223.
Vercellini P, Fedele L, Aimi G, Pietropaolo G, Consonni D, Crosignani
PG. Association between endometriosis stage, lesion type, patient
characteristics and severity of pelvic pain symptoms: a multivariate
analysis of over 1000 patients. Hum Reprod 2007;22:266–271.
Vitonis AF, Vincent K, Rahmioglu N, Fassbender A, Buck Louis GM,
Hummelshoj L, Giudice LC, Stratton P, Adamson GD, Becker CM
et al. World Endometriosis Research Foundation Endometriosis
Phenome and Biobanking Harmonization Project: II. Clinical and
covariate phenotype data collection in endometriosis research. Fertil
Steril 2014;102:1223–1232.
Wolthuis AM, Meuleman C, Tomassetti C, D’Hooghe T, Fieuws S,
Penninckx F, D’Hoore A. Laparoscopic sigmoid resection with tran-
srectal specimen extraction: a novel technique for the treatment of
bowel endometriosis. Hum Reprod 2011;26:1348–1355.
Working group of ESGE-ESHRE and WES, Saridogan E, Becker
CM, Feki A, Grimbizis GF, Hummelshoj L, Keckstein J, Nisolle
M, Tanos V, Ulrich UA et al. Recommendations for the surgical
treatment of endometriosis-part 1: ovarian endometrioma. Gynecol
Surg 2017;14:27 simultaneous publication in Human Reproduction
Open.
Yabuki Y, Sasaki H, Hatakeyama N, Murakami G. Discrepancies
between classic anatomy and modern gynecologic surgery on pelvic
connective tissue structure: harmonization of those concepts by col-
laborative cadaver dissection. Am J Obstet Gynecol 2005;193:7–15.
Downloaded from https://academic.oup.com/hropen/article-abstract/2020/1/hoaa002/5733057 by guest on 12 February 2020
