Human Reproduction, Vol.24, No.3 pp. 602 – 607, 2009
Advanced Access publication on December 17, 2008
Preoperative work-up for patients withdeeply inﬁltrating endometriosis:transvaginal ultrasonography mustdeﬁnitely be the ﬁrst-line imagingexamination
Mathilde Piketty1, Nicolas Chopin1, Bertrand Dousset2,Anne-Elodie Millischer-Bellaische3, Gilles Roseau1, Mahaut Leconte2,Bruno Borghese1,4,5, and Charles Chapron1,4,5,6
1Department of Gynecology, Obstetrics II and Reproductive Medicine, Universite´ Paris Descartes, Faculte´ de Me´decine, AssistancePublique – Hoˆpitaux de Paris (AP-HP), Groupe Hospitalier Universitaire (GHU) Ouest, Centre Hospitalier Universitaire (CHU) Cochin, SaintVincent de Paul, Pavillon Lelong, 82, Avenue Denfert Rochereau, 75014 Paris, France 2Department of Digestive and Endocrine, Universite´Paris Descartes, Faculte´ de Me´decine, Assistance Publique – Hoˆpitaux de Paris (AP-HP), Groupe Hospitalier Universitaire (GHU) Ouest,Centre Hospitalier Universitaire (CHU) Cochin, Saint Vincent de Paul, Paris, France 3Department of Radiology, Universite´ Paris Descartes,Faculte´ de Me´decine, Assistance Publique – Hoˆpitaux de Paris (AP-HP), Groupe Hospitalier Universitaire (GHU) Ouest, Centre HospitalierUniversitaire (CHU) Cochin, Saint Vincent de Paul, Paris, France 4Institut Cochin, Universite´ Paris Descartes, CNRS (UMR 8104), Paris,France 5Inserm, Unite´ de Recherche U567, Paris, France
6Correspondence address. Tel: þ33-1-58-41-19-14; Fax: þ33-1-58-41-18-70; E-mail: [email protected]
background: Transvaginal ultrasonography (TVUS) has important advantages compared with transrectal ultrasonography (TRUS): it isless invasive, is cost-effective, is a familiar and well-accepted approach, and anesthesia is not required. We compared the accuracy of TVUSand TRUS for diagnosing rectal wall involvement in patients presenting with histologically proved deeply inﬁltrating endometriosis (DIE).
methods: Prospective study of 134 patients with histologically proved DIE underwent preoperative investigations using both TVUS andTRUS. The radiologist (TVUS) and sonographer (TRUS) were unaware of the clinical ﬁndings but knew that DIE was suspected.
results: DIE was conﬁrmed histologically for all the patients. A rectal wall involvement was histologically proved for 75 patients (56%).
For the diagnosis of inﬁltration of the intestinal wall, TVUS and TRUS, respectively, had a sensitivity of 90.7% and 96.0%, a speciﬁcity of 96.5%and 100.0%, a positive predictive value of 97.1% and 100.0% and a negative predictive value of 88.9% and 95.2%.
conclusions: TVUS and TRUS have similar degrees of accuracy for predicting intestinal involvement. TVUS must be the ﬁrst-lineimaging process to perform for patients presenting with clinically suspected DIE. The question for the coming years is to deﬁne if it is necess-ary for TRUS to be carried out systematically in cases of clinically suspected DIE.
Key words: deep endometriosis / deeply inﬁltrating endometriosis / preoperative work-up / transvaginal ultrasonography / transrectalultrasonography
the type of pain is related to location of the DIE lesions (Fauconnieret al., 2002), whereas the severity is correlated to depth of the DIE
There are three types of endometriotic lesions: superﬁcial endome-
nodules (Koninckx et al., 1991; Porpora et al., 1999; Chapron et al.,
triosis (peritoneal and/or ovarian), ovarian endometriomas and
deeply inﬁltrating endometriosis (DIE). DIE is a speciﬁc entity, histo-
Management of DIE can be either medical (Igarashi et al., 1998;
logically deﬁned when endometriotic lesions penetrate more than
Fedele et al., 2000; Fedele et al., 2001; Heﬂer et al., 2005; Vercellini
5 mm under the peritoneum (Koninckx et al., 1991). DIE is respon-
et al., 2005; Razzi et al., 2007) or surgical (Urbach et al., 1998;
sible for pelvic pain symptoms (Fauconnier and Chapron, 2005), and
Chapron et al., 2003b; Darai et al., 2005; Vignali et al., 2005;
& The Author 2008. Published by Oxford University Press on behalf of the European Society of Human Reproduction and Embryology. All rights reserved.
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Work-up for rectal wall involvement in deep endometriosis
Ribeiro et al., 2006; Seracchioli et al., 2007). Success of surgery is cor-
experienced radiologist (A.E.M.B.). Routine analysis of uterus and ovaries
related with the radicality of the exeresis (Chopin et al., 2005). A sat-
took place ﬁrst. Moreover, the protocol included the study of the peritoneal
isfactory work-up (questioning, clinical examination, imaging) is
surfaces (pouch of Douglas, vesicouterine pouch) and the retroperitoneal
necessary preoperatively to establish the map of DIE lesions and to
space (i.e. USL, torus uterinum and posterior fornix of the vagina). Theprobe was ﬁrst positioned in the lower vagina in front of the anal canal.
obtain the patient’s consent (Chapron et al., 2004a).
The probe was moved slowly down and up to the posterior fornix of the
Preoperative knowledge about intestinal inﬁltration is essential
vagina. By moving the probe, all the anterior rectosigmoid space could be
because, if surgery is decided, a speciﬁc intestinal surgical procedure
analyzed. The normal aspect of the rectum/sigmoid colon muscularis
will be necessary (Chapron et al., 2003b). In these situations, patients
propria is hypoechoic and thin (,3 mm). Intestinal DIE was deﬁned as an
must be informed preoperatively concerning the surgical risks (Landi
irregular hypoechoic mass, with or without hypo/hyperechoic foci involving
et al., 2006; Dubernard et al., 2008). Because clinical examination is
the rectum/sigmoid colon muscularis propria (Bazot et al., 2007b). Particu-
of limited use for establishing the extent of the DIE lesions
lar attention was paid to the appendix and small. The aspect of torus uter-
(Chapron et al., 2002; Abrao et al., 2007), it is necessary to use non-
inum and USL was observed at the same time with sagittal and parasagittal
invasive imaging processes prior to surgery. Transrectal ultrasonogra-
views of hypoechoic and irregular nodules.
phy (TRUS) was demonstrated to be efﬁcient for the diagnosis ofrectal wall inﬁltration by DIE lesions (Chapron et al., 1998; Fedele
et al., 1998; Delpy et al., 2005; Bazot et al., 2007a). Magnetic reson-
TRUS was performed with an Olympus UM 160 Echoendoscope (SCOP
ance imaging (MRI), also proposed, presents the great advantage of
Medecine Olympus, 94150 Rungis, France) by a single examiner (G.R.). It
offering the possibility of obtaining a complete pelvic evaluation with
was carried out without sedation, 2 h after a rectal enema. Endoscopic
a single imaging procedure (Siegelman et al., 1994; Kinkel et al.,
examination of the rectum and the distal sigmoid colon was ﬁrst performed,
1999; Bazot et al., 2004; Chapron et al., 2004b; Kataoka et al.,
placing the probe in the sigmoid colon, over the aortic bifurcation and/or
2005; Abrao et al., 2007). More recently, transvaginal ultrasonography
the upper part of the body of the uterus. The probe was then slowly with-
(TVUS), which is the imaging method of choice for diagnosis of endo-
drawn allowing optimum imaging of rectal and sigmoid colon walls, withinstillation of water into the intestinal lumen and alternating use of 5, 7.5
metriomas (Mais et al., 1993; Guerriero et al., 1995), was proposed
and 12 MHz frequencies. Normal intestinal wal s usually appear as a ﬁve-
for the diagnosis of DIE (Gorell et al., 1989; Bazot et al., 2003;
layer structure: the fourth hypoechoic layer corresponds to the muscularis
Koga et al., 2003). This method of investigation offers the advantages
propria. The surrounding areas were also imaged, with particular attention
of accessibility and cost-effectiveness when compared with MRI and
paid to the ovaries, cervix and body of the uterus, pouch of douglas, USL
tolerability when compared with TRUS.
areas and torus uterinum. DIE showed up as hypoechoic peri-digestive
The aim of this study is to compare the results of TVUS with those
nodules of rounded or roughly triangular shape. A diagnosis of digestive
of TRUS, which is the investigation of choice for the diagnosis of rectal
tract inﬁltration was conﬁrmed when a hypoechoic thickening of the muscu-
wall inﬁltration, and to clarify whether there are limits for TVUS.
laris propria was demonstrated at ultrasound (Chapron et al., 1998), eitherisolated or involved in an adjacent pelvic location.
Between January 2005 and July 2007, we performed a prospective study
For each imaging process (TVUS and TRUS), sensitivity, speciﬁcity, positive
during which time patients suffering from pelvic pain (alone or associated
and negative predictive value (PPV and NPV), 95% conﬁdence intervals
with infertility) underwent complete surgical exeresis of DIE lesions
and kappa test of concordance in the diagnosis of rectal wall involvement
(Chapron et al., 2003b). DIE was suspected in all cases preoperatively
for patients presenting histologically proved DIE were calculated (McKen-
(questioning, clinical examination, imaging). Diagnosis of DIE was histologi-
zie et al., 1997). Data are presented as mean + SD.
cally proven for each patient. DIE lesions were classiﬁed in ﬁve locations(bladder, uterosacral ligament(s) (USL), vagina, intestine, ureter) accordingto a previous classiﬁcation (Chapron et al., 2006). For each patient, data
were collected: (i) general patients’ characteristics (age, gravidity, parity,height, weight); (ii) history of previous medical and/or surgical treatment
During the study period, 134 patients were enrolled. Patients’ charac-
for endometriosis; (iii) preoperative painful symptoms scores (dysmenor-
teristics are presented in Table I. Four hundred and ten (n ¼ 410) his-
rhea, deep dyspareunia, non-cyclic chronic pelvic pain, gastrointestinal and
tologically proved DIE lesions were removed during complete DIE
lower urinary tract symptoms) according to visual analogue scale; (iv) stage
surgical exeresis: USL (132 lesions; 32.2%); vagina (80 lesions;
of the disease and mean revised American Fertility Society (AFS) scores
19.5%); bladder (22 lesions; 5.4%); intestine (163 lesions; 39.7%)
(total, implant, adhesion) according to the AFS (AFS, 1985); (v) number
and ureter (13 lesions; 3.2%). The mean number of DIE lesions per
and location of DIE lesions (bladder, USL, vagina, intestine, ureter); (vi)
patient was 3.1 + 2.1 (range 1 – 10). Fifty-one patients (n ¼ 51;
existence of associated ovarian endometrioma.
38.1%) had an ovarian endometrioma associated with the DIE lesions.
All women underwent both TVUS and TRUS prior to surgery. The radi-
Patient distribution, according to the main location of the DIE
ologist (for the TVUS) and the sonographer (TRUS) were informed thatDIE was suspected but were blinded to the results of clinical ﬁndings
Classiﬁcation (Chapron et al., 2006), was as follows: USL 25 patients
and previous imaging examinations. They were asked whether there was
(18.7%); vagina 23 patients (17.2%); bladder 11 patients (8.2%); intes-
tine 66 patients (49.2%); and ureter 9 patients (6.7%) (Table II). Atotal of 75 patients (56.0%) presented with histologically proved intes-
tinal involvement (the 66 patients classiﬁed as ‘intestine’ and 9 as
TVUS was performed with a Toshiba ultrasound machine, using a 5 –9 MHz
‘ureter’) (Table II). The mean number of intestinal DIE lesions per
transducer. TVUS was performed without bowel preparation by a single
patient was 2.7 + 1.5 (range 1 – 9). For 70 patients (93.3%), the
rectal and/or sigmoid DIE lesion. Ninety-six percent (96.0%; 72
Table I Characteristics of patients with DIE in the
cases) of the patients presented a rectal wall inﬁltration. Appendix
(n ¼ 8 patients) and omentum (n ¼ 3 patients) DIE lesions werenever isolated and always associated with rectal and/or sigmoid DIE
Among the patients with intestinal DIE lesions (n ¼ 75), only 34
patients (45.3%) presented a single intestinal lesion (not taking
omentum and appendix DIE lesions into account). Among the 41
patients with more than one intestinal DIE lesions (not takingomentum and appendix DIE lesions into account), 21 patients pre-
sented, associated with the rectal and/or sigmoid DIE lesions, a
‘right intestinal DIE lesion’ located at the cecum and/or ileum
(cecum: n ¼ 4 patients; ileum: n ¼ 13 patients; cecum and ileum: 4
patients). So, for patients with rectal and/or sigmoid DIE lesions
(n ¼ 75), the rate of associated ‘right intestinal involvement’ (ileum
Preoperative painful symptoms scoresa,b,c
and/or cecum) was 28% (n ¼ 21 patients) (Fig. 1).
The sensitivity, speciﬁcity, PPV and NPV of TVUS and TRUS for the
diagnosis of rectal wall involvement are presented in Table IV. TVUS
and TRUS yielded a diagnosis of deep rectal endometriosis in 68
(90.7%) and 72 patients (96.0%), respectively. The kappa test of con-
cordance was 0.86 for TVUS and 0.96 for TRUS.
This prospective study demonstrates two points: ﬁrst, TVUS is accu-
rate to diagnose intestinal wall involvement for patients with DIE
and results are similar than those observed with TRUS; second, in
cases of rectal DIE lesions, there are associated cecum and/or
ileum DIE lesions in 28% of the cases.
bSometimes more than one for the same patient.
It is essential that these results, which agree with the conclusions of
dScore according to the revised American Fertility Society Classiﬁcation (AFS, 1985).
two recent studies (Abrao et al., 2007; Bazot et al., 2007b), should betaken into consideration when treating DIE patients. If surgery isdecided, the DIE lesions must all be totally excised (Chapron et al.,
intestinal DIE lesions were associated with other DIE lesions (USL,
2003b; Chopin et al., 2005; Fedele et al., 2005; Vignali et al., 2005).
Consequently, if there is any deep intestinal inﬁltration, a speciﬁc seg-
The anatomic distribution of intestinal DIE lesions (163 lesions for
mental intestinal resection procedure is required (Remorgida et al.,
75 patients) is presented in Table III. All the patients presented a
2005; Abrao et al., 2008). Bowel segmental resection is by no
Table II Distribution of patients according to main location of the DIE
Values in parentheses are percentages.
aAccording to a previously published surgical classiﬁcation for DIE (Chapron et al., 2006).
bNumber of patients.
cNumber of histologically proven DIE lesions.
dEach lesion of bilateral pair counted as part of pair, so total number of individual lesions ¼ 212.
Bl, bladder; USL, uterosacral ligament; Va, vagina; Bl, bladder; Ur, ureter; In, intestine; R, right; L, left; B, bilateral.
Work-up for rectal wall involvement in deep endometriosis
to establish a good basis for deciding on the treatment strategy in
Table III Anatomic distribution of intestinal DIE
Apart from its excellent diagnostic efﬁciency, TVUS has important
advantages compared with TRUS. It is a less invasive means of inves-
tigation than TRUS, is cost-effective, familiar and well accepted by
patients in obstetrics and gynecology, and can be used in all cases
without anesthesia. Unlike TRUS, TVUS performs well for diagnosis
of ovarian endometriomas (Bazot et al., 2007b), which are often
associated with DIE lesions and must be considered as a marker for
severity of the disease (Chapron et al., 2008). Furthermore, DIE
lesions are frequently multifocal (Chapron et al., 2003b). In our experi-
ence, intestinal DIE lesions are associated with other DIE locations
(USL, vagina, bladder, ureter) in 93% of cases. TVUS gives better
results than TRUS for the diagnosis of these associated DIE lesions,
notably when there is inﬁltration of the USL and bladder (Bazot
Some patients presented several intestinal DIE lesions.
et al., 2007b). Further work is required to establish whether TVUSshould be systematically combined in the future with water-contrastin the rectal lumen (Valenzano Menada et al., 2008) or saline solutionin the vagina (Dessole et al., 2003) and whether the use of ultrasoundtransmission gel improves the diagnosis accuracy (Guerriero et al.,2007). While, like others (Bazot et al., 2007b), we performed TVUSwithout bowel preparation, further studies will be necessary to ﬁndout if mechanical lower bowel cleansing using a rectal enema priorto the examination (Abrao et al., 2007) will improve TVUS accuracy.
Although TVUS is efﬁcient for the diagnosis of rectal involvement,
this technique raises two controversial points. First, TVUS is anoperator-dependent procedure. Speciﬁc training for the practitionersis essential to understand the DIE TVUS imaging semiology. Sinceour radiologists came to the operating room to ﬁnd out for themselveswhat the problems facing us are and to understand the anatomy of theposterior pelvic compartment, we have seen better accuracy forthe imaging results. Second, intestinal DIE lesions are multifocal inthe digestive wall in almost one case out of two (Chapron et al.,
Figure 1 Intestinal endometriosis: the anatomic distribution oflesions in 134 patients with DIE.
2003b). In our experience, rectal lesions are associated with asecond intestinal lesion in 54.6% of cases (41/75) (Fig. 1). Similarly,rectosigmoid lesions are associated with ileo-cecum DIE lesions
means an innocuous surgical procedure and presents a real risk of
(cecum and/or terminal ileum) in 28% of cases (Fig. 1). These ‘high
complications (Darai et al., 2007). This point is essential insofar as
sigmoid’ and/or ‘right bowel lesions’ (cecum and/[E1]or ileum) will
the patients concerned are young (32.1 + 5.0 years in this study)
be more difﬁcult to diagnose with TVUS. Their frequency justiﬁes car-
and present painful functional symptoms without any question of
rying out a systematic complete intestinal work-up, since the number
malignancy. Preoperative knowledge of the existence of intestinal inﬁl-
and location of intestinal lesions governs the choice of surgical pro-
tration is important in order to be able to inform the patient about the
cedure. In case of a single intestinal lesion, and especially when it is
various treatment possibilities together with their respective risks and
isolated (without other associated DIE lesions in the bladder, the
Table IV Sensitivity, speciﬁcity, positive and negative predictive value of TVUS and TRUS in the diagnosis of rectalinvolvement for patients presenting with DIE (n 5 134)
PPV, positive predictive value; NPV, negative predictive value.
vagina or the ureter), laparoscopic surgery is the preferred operating
technique (Possover et al., 2000; Duepree et al., 2002; Darai et al.,2005; Jatan et al., 2006; Ribeiro et al., 2006). In case of multiple intes-
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Comparison between clinical examination, transvaginal sonography andmagnetic resonance imaging for the diagnosis of deep endometriosis.
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required given that in these situations, two bowel resections will be
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necessary to carry out complete exeresis during the same operation.
Endometriosis lesions that compromise the rectum deeper than the
To the best of our knowledge, our study is the ﬁrst to underline the
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CURRICULUM VITAE Dott. Ing. Antonella Bogoni CNIT head of research area Via Moruzzi 1 56124 Pisa Italy Tel. +39 050 5492221 Fax. +39 050 5492194 e-mail: antonella. [email protected] CNIT (Consorzio Nazionale Interuniversitario per le Telecomunicazioni) head of research area (digital and microwave photonics) at the Integrated Research Center for Photonic Networks and Technologie
Journal of Magnetic Resonance 149, 196–203 (2001) doi:10.1006/jmre.2001.2298, available online at http://www.idealibrary.com on A Q-Band Pulse EPR/ENDOR Spectrometer and the Implementationof Advanced One- and Two-Dimensional Pulse EPR MethodologyI. Gromov,∗ , 1 J. Shane,∗ J. Forrer,∗ R. Rakhmatoullin, † Yu. Rozentzwaig, † and A. Schweiger∗∗ Laboratory of Physical Chemis