Best Practice & Research Clinical Obstetrics and Gynaecology 71 (2021) 27e37

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Best Practice & Research Clinical

Obstetrics and Gynaecology
journal homepage: www.elsevier.com/locate/bpobgyn

Classification of deep endometriosis (DE)

including bowel endometriosis: From r-ASRM to
#Enzian-classification
€rg Keckstein, MD, Professor a, b, c, *,
Jo
Gernot Hudelist, MD, MSc a, d
a
Scientific Endometriosis Foundation (Stiftung Endometrioseforschung/ SEF), Westerstede, Germany
b
Endometriosis Centre, Clinic Dres. Keckstein, Villach, Austria
c
University Ulm, Germany
d
Department of Gynaecology, Centre for Endometriosis, Hospital St. John of God; Vienna, Austria

a b s t r a c t
Keywords:
Deep endometriosis (DE) Endometriotic lesions may affect peritoneal and ovarian tissues,
Bowel endometriosis cause secondary adhesions, and - in case of deep endometriosis
Enzian classification (DE), invade organs such as the urinary bladder, ureters, and
#Enzian classification bowel. Over decades, several classification systems have been
proposed with the rASRM score being the most widely accepted
one to date. However, the rASRM classification has certain limi-
tations regarding the description of DE. In contrast, the Enzian
classification, which has been updated and modified recently in
the form of the so-called #Enzian classification, has proved to be
the most suitable tool for staging DE and now also includes peri-
toneal or ovarian diseases as well as adhesions. In the ideal sce-
nario, a classification for endometriosis can be used with both
diagnostic and surgical methods. The present work discusses the
pros and cons of scores for endometriosis and highlights the need
for using one universal classification system.
© 2021 Elsevier Ltd. All rights reserved.

€ rg Keckstein, Endometriosis Clinic Dres. Keckstein, Richard Wagner Strasse 18, Villach, Austria.
* Corresponding author. Jo
E-mail address: joerg@keckstein.at (J. Keckstein).

https://doi.org/10.1016/j.bpobgyn.2020.11.004
1521-6934/© 2021 Elsevier Ltd. All rights reserved.
J. Keckstein, G. Hudelist Best Practice & Research Clinical Obstetrics and Gynaecology 71 (2021) 27e37

General issues

Because of the different manifestations and symptoms of endometriosis, the classification of this
disease is difficult. Many attempts have been made to describe and classify the disease into different
stages using various classifications systems. Within this, the WES (World Endometriosis Society)
consensus on the classification of endometriosis was held at the XII World Congress on Endometriosis
in Saeo Paulo, Brazil, in 2014. This included over 55 representatives of 29 national and international,
medical and non-medical organizations, and a statement was formed that “until better classification
systems are developed, we propose a classification toolbox” [1]. This toolbox includes the revised
American Society for Reproductive Medicine (rASRM) classification, the Enzian classification (Fig. 1),
and the endometriosis fertility index (EFI) (Fig. 2). Using the rASRM score, the disease is primarily
classified in the context of diagnostic laparoscopy [2,3]. The status of the peritoneum, tubes, and
ovaries is primarily considered concerning fertility issues describing the extent of pelvic adhesion
influencing the score grade, i.e., severity of the disease. This classification is intended mainly to be used
for those endometriosis patients consulting for infertility, but does not reflect DE. Endometriosis
proliferates into the genital and into extragenital anatomical structures such as the bowel, bladder,
rectovaginal septum (RVS) or ureters, as well as adenomyosis, which cannot be described adequately
when using the rASRM. The Enzian classification overcomes these issues and has been primarily
created to describe adenomyosis as well as DE using 3 planes or so-called pelvic compartments [4]
(Fig. 1) and can be used in addition to the rASRM. Finally, Adamson et al. introduced the EFI (Endo-
metriosis Fertility Index) in 2010 [5,6] that aims to provide the clinician with a prognostic picture of the
endometriosis-associated fertility status (Fig. 2).
DE and its surgical therapy confront the clinician with difficult decisions. Deep endometrial foci that
are sometimes not recognized before or during surgery may lead to a prolongation of the patient's
suffering and unnecessary further medical and surgical measures. To describe the full extent of
endometriosis, it is mandatory to identify the various locations of the implants precisely and classify
them accordingly.
The need for a universal classification system, particularly regarding DE is obvious but discussed
controversially [7e20]. Surgical procedures have developed enormously over recent years; thus, DE
can now be diagnosed or treated relatively safely in a minimally invasive manner. In addition,
noninvasive procedures such as transvaginal sonography (TVS) and magnetic resonance imaging (MRI)
have been established for the exact presurgical diagnosis of endometriosis, with TVS being proposed as
the first line tool to be used in the evaluation of women with suspected endometriosis [16,21e28].
Nevertheless, MRI also demonstrates high accuracy in the diagnosis of the locations of DE [29,30].

How should we classify deep disease?

With a reproducible “picture “of the disease, appropriate decisions regarding diagnosis and therapy
can be made. This picture is drawn by using an accurate classification system for endometriosis.
However, rASRM stages have been demonstrated to poorly correlate with symptoms, which may be
explained by the unclear pathophysiological behavior of the disease itself or possibly also by the lack of
correct identification and complete classification of DE. Severe adhesions may hide the complex growth
pattern of the disease during diagnostic laparoscopy, especially in cases of DE. Consequently, the
comparison of clinical and scientific studies becomes much more difficult or even impossible when the
r-ASRM classification is the only instrument used to describe endometriosis. Therefore, several at-
tempts have been made to find a common “language” for the description of endometriosis. The ENZIAN
classification [4,31,32], the Visual Numeric Endometriosis Surgical Score (VNESS) system [33], and the
classification proposed by Chapron et al. and Adamyan [15,34] focus on DE. Each of these classification
systems has advantages and disadvantages with the Enzian classification being validated by several
studies in recent years.
In 2003 [4,35] and 2005 [31], the Scientific Endometriosis Foundation (Stiftung Endome-
trioseforschung/SEF) originally published the Enzian classification (http://www.endometriose-sef.de/
dateien/ENZIAN_2013_web.pdf) in order to complement the rASRM score. Apart from uterine
adenomyosis, the most common locations of DE are uterosacral ligaments (USL), vagina,

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J. Keckstein, G. Hudelist Best Practice & Research Clinical Obstetrics and Gynaecology 71 (2021) 27e37

Fig. 1. The Enzian classification version 2012. http://www.endometriose-sef.de/dateien/ENZIAN_2013_web.pdf.

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J. Keckstein, G. Hudelist Best Practice & Research Clinical Obstetrics and Gynaecology 71 (2021) 27e37

Fig. 2. The endometriosis fertility index (EFI).

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J. Keckstein, G. Hudelist Best Practice & Research Clinical Obstetrics and Gynaecology 71 (2021) 27e37

rectovaginal space (RVS), the rectosigmoid, and the bladder [8
10], which are all mentioned in Enzian
classification. Furthermore, several studies have highlighted that there is a significant correlation
between the ENZIAN classification and the extent of the disease, difficulty and length of surgery as
well as severity of symptoms [36e40].
Dai et al. [41] demonstrated that DE lesions are associated with severe pain symptoms. Extensive
pain was also reported in patients with low rASRM scores demonstrating a lack of disease stage and
intensity of symptoms. In a study based on 63 patients with DE including recto-sigmoidal endome-
triosis, over 21% were found to have only stage 1 or 2 according to the rASRM scoring system [42]. In
contrast, the symptom severity appears to correlate with the extent of DE when classified by the Enzian
[43]. Mutuku et al. [44] demonstrated a clear correlation between the extent of DE and the degree of
dyspareunia. A recent study by Montanari and coworkers [40] showed that the disease extent depicted
by the Enzian classification was significantly correlated with the location and severity of different
preoperative pain symptoms.
In the ideal setting, a classification system should also be applicable using noninvasive methods
such as TVS and MRI, which accurately detect DE [25,26,40] [45,46], [36e38,43]. Within this, Di Paola
et al. [46] compared MRI-ENZIAN score and surgical ENZIAN score. The overall sensitivity, specificity,
accuracy, and positive and negative predictive values related to the presence/absence of DE were
calculated for each patient. The concordance between histopathological and MRI ENZIAN score was
excellent (k ¼ 0.824). MRI correlates with the surgical ENZIAN score and is highly accurate in the
detection and localization of DE, thus minimising false negative results (4%) and allowing correct
preoperative staging. Similarly, Thomassin-Naggara et al. recently showed that the Enzian is accu-
rate, reproducible and correlates with surgical findings and clinical parameters such as hospital stay.
Finally, Hudelist and coworkers demonstrated that TVS provides a valuable preoperative estimation
of DE localization and lesion size using the Enzian classification, especially for Enzian compartments
A, C and FB [47].
In addition, several studies have demonstrated that the Enzian classification, be it surgical or with
TVS/MRI, can be used to estimate operation time, help to choose adequate surgical
techniques preoperatively and to estimate the risk of associated complications [36]. Roman et al. [48]
compared the outcome after surgery for bowel endometriosis (according to the size of the nodule)
with two different surgical approaches. Following the division in three groups regarding bowel lesion
size (according to Enzian C 1e3), the authors concluded that shaving might also be possible in C2
lesions with lower complication rates, but a smaller effect on symptom relief [26]. Poupon et al. used a
nomogram based on three simple criteria e the age of the patient, previous surgery for DE and the
extent of disease described by the Enzian classification to evaluate the risk of severe postoperative
complications associated with the resection of DE without bowel involvement [49]. All factors were
significantly associated with the risk of postoperative complications and voiding dysfunction.
Consequently, several guidelines and recommendations [1,50e52] support the use of the Enzian
classification, which has also become mandatory for all certified endometriosis centers in Germany,
Switzerland, and Austria [53]. However, the Enzian classification has so far not included ovarian and
peritoneal endometriosis and has not allowed for the description of pelvic adhesions.

The Enzian classification

Enzian provides a morphologically descriptive classification of DE involving the vagina, USL,

bladder, ureter, bowel and uterus (adenomyosis), as well as other extragenital localizations (Fig. 1). The
description considers the different extent of the disease in terms of size (>5 mm ¼ DE) [54], site, and
different organ involvement. The idea of this classification is to divide the small pelvis into three
compartments (axis), with their anatomical correlates.
Compartment A (Fig. 3), which represents the cranio-caudal axis, comprises the rectovaginal space
and vagina.
Compartment B (Fig. 4), the medio-lateral axis, comprises the uterosacral ligaments, cardinal
ligaments, pelvic sidewall, and extrinsic ureteric obstruction.
Compartment C (Fig. 5a), the ventro-dorsal direction comprises the lower bowel (rectum and
sigmoid colon up to 16 cm from the anal verge).

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J. Keckstein, G. Hudelist Best Practice & Research Clinical Obstetrics and Gynaecology 71 (2021) 27e37

Fig. 3. Schematic image of the A compartment (craniocaudal axis).

Fig. 4. Schematic image of the B compartment (mediolateral axis) including the USL and cardinal ligament (green).

The grade of disease severity is identified for each compartment (thus excluding apparently minor
peritoneal lesions below 5mm invasion depth) as follows: grade 1 invasion <1 cm, grade 2 invasion
1e3 cm, and grade 3 invasion >3 cm. In compartment A, the DE is assessed in the area of the RVS, the
vagina, and the torus of the cervix (Fig. 3). Starting from the cervix, the uterosacral ligaments and
parametrical structures are assessed in the lateral and dorsolateral direction when describing the B
compartment (Fig. 4). Right and left sides are classified separately and considered when coding (B left/
right). The bowel section between the anus and rectosigmoid is assessed in the sagittal section
describing the C compartment (Fig. 5a and b). The infiltration of the rectum (anterior wall) is measured,
in particular the length of the lesion. Adenomyosis and other extragenital locations (F) are classified as
follows:

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J. Keckstein, G. Hudelist Best Practice & Research Clinical Obstetrics and Gynaecology 71 (2021) 27e37

Fig. 5. a): Schematic image of the C compartment (ventrodorsal axis). b): Surgical image showing DE in the right USL (2.5 cm), no
lesion in the left USL (B0/2) and rectum (3.9 cm) (C3) ¼ Enzian B0/2, C3. the full extent of the lump in the intestine was revealed only
after segment resection (however, this nodule was precisely identified preoperatively by sonography).

 Adenomyosis (FA)
 Bladder involvement (FB), the involvement of the muscle
 Ureteric involvement with signs of obstruction (FU)
 Bowel disease (FI) cranial to the rectosigmoid junction (>16 cm from the anal verge; upper sigmoid,
transverse colon, cecum, appendix, small bowel)
 Other locations (FO) such as the abdominal wall, diaphragm, and nerve or other localization.

The extent of endometriosis is coded separately for each compartment (Fig. 5b). The B compartment
includes the classification of both right and left sides. The individual stages (number 1-3) according to
the specification are depicted following the letter (A,B or C) directly after the letter: number 0 is used in
case of no involvement, i.e. lack of DE. A comma should be used between each individual compartment.
The B compartment includes the classification of both, right and left sides, using a slash sign (/) in order
to separate left/right.
Enzian summarized in the code (example):

 No lesion in the A compartment

 Deep endometriosis left USL < 1 cm, right USL >3 cm (B) ¼ B1/3
 Deep endometriosis in the rectum 4 cm (C) ¼ C3
 Hydroureter right (FU) ¼ FU(r)
 Deep Endometriosis in Ileum (FI) ¼ FI (Ileum)

Only affected compartments and organs should be listed:

Coding: Enzian B1/3, C3, FU(r), FI (Ileum).

#Enzian e a universal system applicable by all clinical specialties

Classifying endometriosis with different systems such as r-ASRM, EFI score [5,6,28], and Enzian
can lead to overlaps. It may be difficult and time-consuming in everyday clinical practice and
therefore gain fewer acceptance by the clinicians. Consequently, there is a need for a comprehensive
classification system that includes ovarian, peritoneal, and deep endometriosis as well as adhesions.
Recently, the #Enzian classification has been created by a group of experts in 2019 and 2020 [55,57].
It is applicable in both situations, surgical staging and diagnostic workup based on the fact that DE
can also be diagnosed with high accuracy using TVS and MRI (Fig. 6). Within this, the proposal of the
IDEA [24] (International Deep Endometriosis Analysis group) for the terms, definitions, and

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J. Keckstein, G. Hudelist Best Practice & Research Clinical Obstetrics and Gynaecology 71 (2021) 27e37

Fig. 6. Ultrasound image of rectal DE: Enzian C3.

Fig. 7. Surgical specimen of rectal DE corresponding to Fig. 6: Enzian C3. The specimen is cut lengthways. The layer of the mus-
cularis is thickened due to the infiltration of endometriosis associated with fibrosis and myohyperplasia.

Table 1
Comparison of the different classification systems, r-ASRM, EFI, and Enzian including its recently updated and proposed version
#Enzian.

r-ASRM EFI Enzian #Enzian

clinical acceptance þþþ þþ þþ u.i.

infertility (ovary, tubal adhesions) þþþ þþþ e þþþ
deep endometriosis (DE) þ þ þþþ þþþ
correlation with symptoms þ þ þþ u.i.
applicability TVS, MRI þ þ þþ u.i.
correlation with surgical complexity, complication rates þþ e þþþ u.i.

The advantages and disadvantages of the systems are compared (- not suitable, þ little, þþ moderately, and þþþ well suitable, u.i.,
under investigation).

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J. Keckstein, G. Hudelist Best Practice & Research Clinical Obstetrics and Gynaecology 71 (2021) 27e37

measurements that precisely describes typical sonographic features of the different phenotypes of
DE is also considered.
In the age of digital recording and web-based documentation, a web-based application tool for
classification of endometriosis should be mentioned e the so-called EQUSUM (www.equsum.org).
Named after the QUSUM (QUality indication for SUrgical performance in Minimally invasive
surgery), it was developed to provide electronic synoptic operative reporting (E-SOR) and easy
staging/classification using 3 commonly known classification tools - rASRM, Enzian and the EFI
(which is incorporated for fertility advice after surgery (Table 1). The tool aims to simplify correct
and automatic endometriosis classification/scoring and surgical registration by using infographics. The
collection of standardized data with the EQUSUM could improve endometriosis reporting and increase
the uniformity of scientific output. Because classification is subject to constant change and new ver-
sions, one digital system might facilitate to update the system with current developments and evo-
lutions such as #Enzian classification [56].

Summary

The exact and reproducible classification of endometriosis including DE is of great importance for
both the clinician and the patient. The 3 main classification and recording tools that are currently used
are the r-ASRM, Enzian, and EFI. An updated version of the Enzian, the so-called #Enzian classification
now also includes peritoneal and ovarian disease as well as adhesions. It may be also used with TVS and
MRI. Future studies are needed to test its accuracy and reproducibility. The combination of different
classifications such as r ASRM, Enzian, and EFI is pivotal for recording the disease adequately, planning
therapeutic measures and evaluating results. However, the complexity of the various systems and their
combination can be cumbersome and hinder general acceptance. The development of a comprehensive
classification as #Enzian classification and the possibility of classifying digitally (web-based) with
EQUSUM may simplify the application of the classifications and offers a large potential in the near
future.

Declaration of competing interest

The authors have no conflicts of interest.

Practice points:

 Correct staging of endometriosis is of great importance for both diagnosis and therapy.
 The application of the Enzian classification shows high clinical applicability and accuracy,
especially for DE and can also be used noninvasively with TVS and MRI.
 A universally useable system such as the updated #Enzian system may allow for complete
classification of endometriosis using noninvasive and invasive techniques

Research agenda:

 Accuracy and reproducibility of a universal classification system - #Enzian

 Fertility outcomes following surgery when DE is described by #Enzian
 Outcomes regarding pain and complication rates using different classification systems.

Acknowledgements

This work was supported by the Scientific Endometriosis Foundation /Stiftung Endometriose For-
schung SEF. The creation of the Enzian classification was initiated and further developed by the

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J. Keckstein, G. Hudelist Best Practice & Research Clinical Obstetrics and Gynaecology 71 (2021) 27e37

Scientific Endometriosis Foundation, SEF in 2002. The following experts were primarily involved in the
design of the classification in the following years during several Weissensee meetings: J. Keckstein, G.
Hudelist, K.W.Schweppe, H. Tinneberg, U. Ulrich, M. Sillem, P. Oppelt, K. Bühler, S. Mechsner, S. Renner,
L. Mettler, A. Schindler, M. Possover, O. Buchweitz, R. Mangold, E. Janschek, F. Tuttlies, R. Greb, D. Barisic,
S. Keckstein.
The following international experts have also significantly contributed to the improvement of the
Enzian classification through intensive discussions and active cooperation in recent years: C. Exa-
coustos, E. Saridogan, M. Malzoni, A. Di Giovanni, H. Roman.

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