Human Reproduction, Vol.25, No.8 pp.

1949 1958, 2010

Advanced Access publication on June 13, 2010 doi:10.1093/humrep/deq135

ORIGINAL ARTICLE Gynaecology

Complications, pregnancy and

recurrence in a prospective series of
500 patients operated on by the
shaving technique for deep
rectovaginal endometriotic nodules
Department of Gynecology, Universite Catholique de Louvain, Cliniques Universitaires St Luc, 1200 Brussels, Belgium
*Correspondence address. Tel: +32-2-764-95-01; Fax: +32-2-764-95-07; E-mail: jacques.donnez@uclouvain.be

Submitted on March 17, 2010; resubmitted on April 30, 2010; accepted on May 7, 2010

background: The debate continues between advocates of the shaving technique and supporters of bowel resection in case of deep
endometriosis with rectal muscularis involvement, despite little evidence for better improvement with bowel resection.
methods: We analyzed complication, pregnancy and recurrence rates after deep endometriotic nodule excision by shaving surgery. This
is a prospective analysis of 500 cases (,40 years old) of deep endometriotic nodules.
results: Laparoscopic nodule resection was performed successfully in all cases. Major complications included: (i) rectal perforation in
seven cases (1.4%); (ii) ureteral injury in four cases (0.8%); (iii) blood loss .300 ml in one case (0.2%); and (iv) urinary retention in four
cases (0.8%). The median follow-up duration was 3.1 years (range 2 6 years). In our prospective series of 500 women, 388 wished to conceive. Of this number, 221 (57%) became pregnant naturally and 107 by means of IVF. In total, 328 women (84%) conceived. The recurrence
rate was 8% among these 500 women, and it was signicantly lower (P , 0.05) in women who became pregnant (3.6%) than in those
who did not (15%). In women who failed to conceive, or were not interested in conceiving, severe pelvic pain recurred in 16 20% of
patients.

conclusion: In young women, conservative surgery using the shaving technique preserves organs, nerves and the vascular blood
supply, yielding a high pregnancy rate and low complication and recurrence rates. There is a need, however, for further strong and energetic
debate to weigh up the benets of shaving (debulking surgery) versus rectal resection (radical surgery).
Key words: deep endometriosis / nodules / shaving technique / bowel resection

Introduction
In the pelvis, three different forms of endometriosis must be considered: (i) peritoneal endometriosis; (ii) ovarian endometriosis; and
(iii) deep rectovaginal endometriosis (Donnez et al., 1996; Nisolle
and Donnez, 1997).
The deep rectovaginal form of endometriosis has been dened as
deep endometriosis, rectovaginal endometriosis or adenomyosis of
the rectovaginal septum. In the literature, it is also called
deep-inltrating endometriosis or posterior deep-inltrating endometriosis. According to the magnetic resonance imaging (MRI) classication described by Squifet et al. (2002), most of these lesions
originate from the posterior part of the cervix and may inltrate the
anterior wall of the rectum.

Many different surgical techniques have been proposed and, surprisingly, the number of manuscripts advocating bowel resection has dramatically increased over recent years (Redwine and Wright, 2001;
Chapron et al., 2004; Dara et al., 2005a, b; Emmanuel and Davis,
2005; Fleisch et al., 2005; Ford et al., 2005; Keckstein and Wiesinger,
2006; Mereu et al., 2008; Meuleman et al., 2009), even if some authors
(Roman et al., 2010) have now started to question the advantages of
this approach.
Indeed, during meetings on this topic, the debate rages on
between advocates of the shaving technique and supporters of
bowel resection in case of deep endometriosis with rectal muscularis
involvement.
The goal of this manuscript is to present data from a prospective
series of 500 cases and discuss post-operative complications,

& The Author 2010. Published by Oxford University Press on behalf of the European Society of Human Reproduction and Embryology. All rights reserved.
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Jacques Donnez * and Jean Squifet

1950

Donnez and Squifet

Type II

296 (59.2%)

Surgery: the shaving technique

Type III

204 (40.8%)

Patients and methods

Five hundred patients under 40 years of age operated on for deep endometriotic nodules were included in this study from 2004 to 2008. This was
a prospective study, conducted with the approval of the Ethics Committee
of the Catholic University of Louvain. Prospective evaluation is the only
way to assess the recurrence rate, avoiding the bias of a retrospective
analysis (Table I).
Inclusion criteria were: (i) palpation of a nodule plus at least one
symptom of pain (dysmenorrhea, dyspareunia or rectal dyschezia) associated or not with infertility; (ii) type II or III nodules (Squifet et al., 2002);
(iii) no previous surgery for endometriosis; (iv) surgical procedure performed by one of the authors; and (v) consent to be followed every 6
months after surgery.
In this series of 500 patients, the main symptoms were pelvic pain and/
or dysmenorrhea observed in 95% of cases, deep dyspareunia in 86% of
cases and rectal dyschezia in 48% of cases (Table I).
Three hundred and twenty-four patients (64.8%) were suffering from
pelvic pain associated with infertility. In all cases of infertility, evaluation
of ovulation, cervical mucus sperm interaction (postcoital test) and
male factor (dened as ,15 million sperm/ml using a Makler counting
chamber) were undertaken. Six patients with ovulatory problems were
treated after surgery by clomiphene citrate or gonadotropins.
Careful clinical examination (Koninckx et al., 1996), transrectal ultrasonography (TRUS) (Ohba et al., 1992), rectal endoscopic sonography
(Abrao et al., 2007), transvaginal sonography (TVS), barium enema and
MRI (Squifet et al., 2002; Donnez and Squifet, 2004) have all been recommended to identify deep rectovaginal endometriotic lesions. All
patients in this prospective study underwent clinical examination, TVS,
TRUS, barium enema and MRI. In our series, examination with a speculum

Table I Characteristics of patients and incidence of

associated lesions.
Age (mean, range)
Nodules (n patients; %)

324 (64.8%)

There is no doubt that we should operate in case of symptomatic deep

nodular lesions, but surgical techniques have taken some considerable
time to evolve. However, all of them involve (i) separation of the anterior
rectum from the posterior vagina, (ii) excision or ablation of deep endometriosis after complete dissection of the nodule from the posterior
part of the cervix, systematically removing the posterior vaginal fornix
(Fig. 4) and (iii) vaginal closure.

None or minimal (one or two spots)

152 (30.4%)

Surgical procedure

Peritoneal (mild/moderate)

146 (29.2%)

Ovarian endometriosis (cyst . 2 cm)

352 (70.4%)

Symptoms (n patients; %)
Dysmenorrhea

476 (95.2%)

Deep dyspareunia

432 (86.4%)

Rectal dyschezia

241 (48.2%)

Associated infertility (n patients; %)

Associated endometriotic lesions (n patients; %)

Bladder nodules

38 (7.6%)

Ureteral lesions (substenosis/stenosis)

66 (13.2%)

Patients underwent surgery for deep rectovaginal endometriotic nodules using the
shaving technique.

In our department, all laparoscopic procedures are performed under

general anesthesia. A 12-mm operative laparoscope is inserted through
a vertical intraumbilical incision. Three other puncture sites are used: 2
3 cm above the pubis in the midline and in areas adjacent to the deep
inferior epigastric vessels, which are visualized directly.
Deep endometriotic nodules involving the cul-de-sac require excision of
the nodular tissue from the posterior vagina, rectum, posterior cervix and
uterosacral ligaments.

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26.1 (18 39 years)

revealed either a normal vaginal mucosa or a protruded bluish nodule in

the posterior fornix. By palpation, the diameter of the lesion could be evaluated. Palpation is very often painful and the presence of a nodule
accounts for symptoms like deep dyspareunia and dysmenorrhea.
Preoperative radiography of the colon (barium enema) was systematically carried out in order to assess the involvement of the rectal surface
and its length. Prole radiography allows the best evaluation of inltration
of the anterior rectal wall (Fig. 1; Squifet et al., 2002).
According to Squifet et al. (2002), there are three types of deep endometriotic nodules (Fig. 2): (i) type I: rectovaginal septum lesions; (b) type II:
posterior vaginal fornix lesions; and (iii) type III: hourglass-shaped lesions.
Their prevalence is, respectively, 10, 58 and 32% of all deep nodular
lesions.
Type I nodules are pure rectovaginal septum lesions, situated far from
the cervix. They are more commonly considered as vaginal lesions and
their prevalence was only 10% in a previous study (Squifet et al., 2002;
Donnez and Squifet, 2004). These lesions were not included in the
present study, because they are never adherent to the rectum and do
not require the shaving technique.
Only patients with type II and III nodules according to the classication
of Squifet et al. (2002) were included in this series.
Type II nodules are lesions situated in the posterior vaginal fornix and
behind the cervix. Adamyan (1993) also clearly described, in her classication, endometriotic nodular lesions attached to the cervix and extending
to the rectovaginal septum and anterior part of the rectum.
Type III (hourglass-shaped) lesions (Fig. 3) occur when posterior fornix
lesions extend cranially to the anterior rectal wall. Clinical evaluation
usually reveals a larger lesion (more than 3 cm) and barium enema
always shows inltration and retraction of the rectal muscularis, known
as perivisceritis. This continuum between the rectal muscularis and the
cervix is found to obliterate the rectovaginal septum cranially. Type III
lesions always occur under the peritoneal fold of the recto-uterine
pouch of Douglas. Inltration of the rectal muscularis is consistently
observed in this subtype, as demonstrated by barium enema (prole
image; Fig. 1) and TRUS, but inltration is generally limited to the muscularis without mucosal involvement. These lesions may also extend laterally
and involve the ureter (Donnez et al., 2002; Jadoul et al., 2007). In case of
nodules 3 cm in size, intravenous pyelography (IVP) is systematically
carried out. In our series, ureteral involvement (deviation, stricture, substenosis or stenosis) was observed in 66 cases (13.2%).
In the present study, type II and III nodules were observed in, respectively, 59.2 and 40.8% of cases (Table I).

pregnancy and recurrence rates by analyzing the existing literature and

our own data. Pregnancy rate is an important outcome because pelvic
surgical procedures followed by complications (e.g. stula, abscess)
will often result in decreased fertility.

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Deep endometriotic nodules

Barium enema: prole radiography allows the best evaluation of inltration of the anterior rectal wall. Typical endometriotic inltration of the anterior rectal wall without
stenosis is clearly visible. No inltration of the mucosa is detected.

To determine the diagnosis of cul-de-sac obliteration during laparoscopy, a sponge on a ring forceps is inserted into the posterior vaginal
fornix. A dilator (Hegar 25) or rectal probe is systematically inserted
into the rectum (Donnez et al., 2007). In addition, a cannula is inserted
into the uterine cavity to markedly antevert the uterus. Complete obliteration is diagnosed when the outline of the posterior fornix cannot be seen
through the laparoscope.
Cul-de-sac obliteration is considered partial when rectal tenting is
visible, but a protrusion of the sponge into the posterior vaginal fornix is
identied between the rectum and the inverted U of the uterosacral ligaments. Sometimes, however, deep lesions of the rectovaginal septum are
only barely visible by laparoscopy.
As previously mentioned, surgical techniques all involve separation of
the anterior rectum from the posterior vagina and excision of the
nodule in that area. Aquadissection and CO2 laser are used.
In case of nodules with possible ureteral involvement [suspected by MRI
or IVP in 66 cases (13.2%) in our study], a JJ stent is inserted before starting the laparoscopic procedure and ureterolysis is then performed
(Donnez et al., 2002). The usefulness of JJ stents in preventing subsequent
complications was recently conrmed by Weingertner et al. (2008). The
group of Koninckx also published a large series of ureteral injuries (De
Cicco et al., 2009). They demonstrated that ureteral repair was often

possible by laparoscopy with excellent outcomes. Moreover, in case of

lateral extension, the uterine artery is often included in the brotic
process and needs to be clipped to prevent severe blood loss, whereas
associated bladder nodules require partial cystectomy (n 38; 7.6% in
our series) according to a previously described technique (Donnez
et al., 2000).
The follow-up duration in our series was 3.1 years (median, range 2 6
years).

Statistical analysis
The x2 test was used for statistical analysis. Values of at least P , 0.05
were considered statistically signicant.

Results
All 500 patients were treated by laparoscopy. No conversion to
laparotomy was required. Median lesion size was 3.4 cm (range 2
6 cm). Median operating time (including laparoscopy) was 78 min
(range 50 218 min). Surgery only exceeds 3 h when nodules are
removed from the bladder, ureter and bowel, sometimes including

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Figure 1 Radiograph of patient who will undergo surgery for deep endometriotic nodules.

1952

Donnez and Squifet

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Figure 2 Classication of deep endometriotic nodules.

BL, bladder; E, endometriotic lesion; R, rectum.

Figure 3 Hourglass-shaped deep lesions seen by magnetic resonance imaging: extension of posterior fornix lesion cranially to the anterior rectal wall.
This continuum between the rectal muscularis and the cervix is found to obliterate the rectovaginal septum cranially. (A) Sagittal view. (B) Transversal view.

laparoscopic nephrectomy (n 4 cases in this study) during the

same procedure, as described by Jadoul et al. (2007). In some
cases, type II nodules (,2 cm) could be removed in ,10 min,
particularly when they were not adherent to the rectum, the
vagina being sutured in 3 min. This explains why, in some cases,
the duration of surgery was so short.

Peri- and post-operative complications

In our series of 500 cases, laparoscopic rectal perforation occurred in
seven cases (1.4%) (Fig. 5A). In all these cases, barium enema had

detected muscularis involvement of more than 3 cm in length

(prole radiography; Table II). The rectum was always repaired by
laparoscopy (Fig. 5B and C).
Laparoscopic suture was carried out through a full-thickness layer
using Vicryl 2.0 (Ethicon, Johnson and Johnson, USA) with separate
stitches. The area was nally covered with brin glue (Tissucol,
Johnson and Johnson, USA; Fig. 5D). Among the seven cases,
neither stulas nor any other complications were observed. Rectal
muscle defects frequently arise during the shaving procedure and
are repaired by suturing. If the rectal lumen is not entered, it is
not considered a complication, just part of the procedure.

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Deep endometriotic nodules

Temporary urinary retention was observed in four cases (0.8%), but

normal micturition resumed within 2 weeks of surgery.

Pregnancy rates and recurrence

Four cases (0.8%) of ureteral injury were noted in our patients.

One case was diagnosed on the rst post-operative day by the
presence of abundant uid in the peritoneal cavity. High levels of
urea and creatinine in the peritoneal uid and IVP conrmed the
diagnosis of a lateral ureteral lesion. A JJ catheter was immediately
inserted and remained in place for 3 months. Hydronephrosis
was detected 1 month after removal of the JJ stent, and this
woman needed vesico-ureteral reimplantation for hydronephrosis
owing to brotic stenosis of the lower ureteral segment and
nephrostomy.
The remaining three cases of ureteral injury were the result of
thermal damage (bipolar coagulation). The patients presented 6 8
days after their initial surgery with diffuse abdominal pain and liquid
in the lower abdomen. Pyelography revealed lateral ureteral lesions.
They were treated by insertion of a JJ stent, which was removed
3 months later and the patients made a full recovery.

Discussion
Surgery for deep rectovaginal endometriosis was rst described by
Reich et al. (1991), and the rst two large series including 231 and
500 women, respectively, were published in 1995 and 1997
(Donnez et al., 1995, 1997).
Although these papers concluded that it is prudent to curtail rather
than encourage the widespread use of an aggressive and potentially
morbid procedure, increasingly aggressive surgery, including bowel

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Figure 4 (A) Shaving technique. (B) The deep nodule freed from
the rectum can then be dissected from the cervix.

The duration of follow-up was 26 years (median 3.1 years) (Fig. 6).
Among the 500 women, 388 (78%) wished to conceive (Fig. 6). Of this
number, 221 (57%) became pregnant naturally during follow-up.
After delivery, progestogens were administered, consistent with the
ndings of Vercellini et al. (2003, 2005), who proved that continuous
oral contraceptives and progestogens were effective at preventing
recurrence of symptoms. Progestogens [Primolut-Nor 5 mg (norethisterone), Bayer, Berlin, Germany] were continued until patients wished
to become pregnant again. In this subgroup of 221 women, recurrence
was noted in only four cases (2%).
Among the 388 women who wished to conceive, 167 (43%) underwent IVF procedures (from 1 to 6 attempts) because they failed to fall
pregnant naturally (after 1 year of regular sexual intercourse), or
because of severe male factor infertility (n 42; 25%), requiring
immediate IVF. In this subgroup, 107 patients became pregnant
(64%). The overall pregnancy rate (obtained naturally or after IVF)
was thus 84% (328 among 388 women wishing to conceive). Six
women experienced recurrence of pelvic pain during IVF and two
after delivery. Among these 107 women, the recurrence rate of
pelvic pain was therefore 7.4% (n 8). Among the 60 women who
failed to conceive, recurrence of severe pelvic pain was reported in
12 (20%), the majority of whom were then successfully treated with
progestogens [Primolut-Nor 5 mg (norethisterone), Bayer, Berlin,
Germany].
Of the 500 women in our series, 112 (22%) did not wish to conceive. Continuous progestogens or oral contraceptives (containing
20 mg of ethinylestradiol) were administered to all of these patients.
Recurrence of severe pelvic pain (severe dysmenorrhea and severe
deep dyspareunia according to Biberoglu and Berhman, 1981) was
noted in 15 cases (13%).
Repeat surgery was carried out for recurrence of severe pelvic pain
resistant to medical therapy in 12 women. Seven of them underwent
nodule resection, three underwent anterior segmental bowel resection, and two underwent large discoid resection (Fig. 7) because
recurrence was associated with bowel involvement, including the
mucosa, as conrmed by colonoscopy and biopsy. Surgery was performed by laparoscopy in all cases. Discoid bowel resection remains
a possibility (Fig. 7A D), even after the shaving technique.
Recurrence of pelvic pain was thus found to be signicantly lower
(P , 0.05) in women who became pregnant after surgery (12/328;
3.6%) than those who did not (27/172, 15.7%). If we analyze the recurrence rate among all 500 women, it gives a gure of 7.8% (39/500).

1954

Donnez and Squifet

Table II A series of 500 cases of deep endometriosis

treated by the laparoscopic shaving technique without
segmental resection.
Laparoscopic shaving surgery (n 500)
Lesion size (cm)
Duration of surgery (min)
Post-operative hospitalization (days)

3.4 (2 6)
78 (50218)
1.5 (1 7)

Complications, n (%)
Rectal perforation

7 (1.4%)

Ureteral injury

4 (0.8%)

Urinary retention

4 (0.8%)

Blood loss . 300 ml

1 (0.2%)

resection, is still systematically proposed in case of deep endometriosis with muscularis involvement, even in the absence of mucosal involvement (Redwine and Wright, 2001; Chapron et al., 2002; 2004;
2006; Dara et al., 2005a; Emmanuel and Davis, 2005; Fleisch et al.,
2005; Ford et al., 2005; Abrao et al., 2007; Meuleman et al., 2009).
All these studies are retrospective and non-randomized, however,
and do not evaluate the long-term outcome of this surgery compared
with shaving surgery. The lack of evidence of better improvement in
case of bowel resection was recently underlined by Vercellini et al.
(2009).

Complications
We conducted a review of complication rates encountered after
bowel resection for deep nodular endometriosis (Table III)
(Redwine and Wright, 2001; Duepree et al., 2002; Chapron et al.,

2004; Dara et al., 2005a, b; Emmanuel and Davis, 2005; Fleisch

et al., 2005; Ford et al., 2005; Seracchioli et al., 2005; Keckstein and
Wiesinger, 2006; Mereu et al., 2008; Meuleman et al., 2009). Unfortunately, much of the recent literature appears to encourage very invasive techniques, including bowel resection in case of rectal muscularis
involvement. Our review of recent publications (see above) reporting
the results and complications of laparoscopy-assisted bowel resection
for deep endometriotic nodules reveals a relatively high complication
rate compared with the shaving technique. Indeed, rates of urinary
retention (35%), ureteral lesions (24%), fecal peritonitis (35%),
severe anastomotic stenosis (3%), rectovaginal stulas (6 9%) and
pelvic abscesses (2 4%) were found to be higher than with the
shaving technique. A possible bias could have been the relatively
small number of patients involved in some series (Seracchioli et al.,
2005), but it should be pointed out that, even in very experienced
hands (Dara et al., 2005b; Keckstein and Wiesinger, 2006), the rate
of severe complications (rectovaginal stulas, abscesses, stenosis,
fecal peritonitis) can be more than 10%.
Very recently, Meuleman et al. (2009) reported an 11% rate of
severe complications, some of which resulted from the duration of
surgery (mean over 7 h). Indeed, lower leg compartment syndrome
was observed in three cases (3/56), requiring fasciotomy. It is important to note that there was no mucosal inltration of the rectum in this
series. This relatively high rate of severe complications was encountered despite a multidisciplinary approach including a urologist and
digestive surgeon. In this series, the median operating time was 7 h
16 min (range 180780 min). The duration is also related to costs
for the hospital (operating room, nurses, anesthetist, etc.).
It should also be pointed out that colorectal segmental resection is a
complex procedure, sometimes resulting in pelvic nerve damage and
unpleasant urinary and digestive symptoms (Slack et al., 2007;
Roman and Bourdel, 2009; Vercellini et al., 2009; Roman et al., 2010).

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Figure 5 (A) Laparoscopic rectal perforation occurring during the shaving procedure. (B and C) The defect is sutured using one layer of separate
stitches of 2.0 Vicryl (Ethicon, USA). (D) Once the suture is complete, it is covered with brin glue (Tissucol).

1955

Deep endometriotic nodules

Analysis at 3 years of follow-up.

Care must always be taken to preserve the pelvic autonomic

nerves, as they are the pathway for the neurogenic control of rectal,
bladder and sexual arousal function (Maas et al., 1999; Possover
et al., 2000; Landi et al., 2006). The shaving technique allows preservation of the nerves by avoiding deep lateral rectal dissection (necessary for rectosigmoid resection). Indeed, lateral dissection is mandatory
only in case of lateral extension of the disease with ureteral involvement (Donnez et al., 2002) and, even in this case, it rarely involves dissection of the posterolateral compartment of the rectum.
Removing part of the rectum increases the risk of complications.
Furthermore, no randomized studies performed to date have been
able to prove that it is any more effective than the shaving technique.
Very recently, Landi et al. (2006) reported that full-thickness disc excision using a circular stapler could prevent the potential morbidity
associated with low anastomosis. As only a few months earlier the
same group (Mereu et al., 2008) reported a major complication rate
that required repeat operations in 20 among 192 cases (10.4%),
they are now probably evaluating a less aggressive surgical technique
than bowel resection (Landi et al., 2006). The same trend away
from bowel resection toward a less aggressive approach has recently
been described by Slack et al. (2007) and Roman et al. (2010).

In our hands, the shaving approach has proved to be adequate. In

most cases, muscularis inltration observed in all cases of type III
lesions may be left in place, at least partially, since the shaving technique already removes what is necessary. Residual lesions in the muscularis of the rectum do not evolve and remain constant for a long
time (Donnez and Squifet, 2004). The argument used by some gynecologists and surgeons to defend bowel resection is that this procedure is more radical. This is simply not true. Indeed, even with
bowel resection, the margins are not free of disease in more than
10% of cases (Anaf et al., 2009; Roman et al., 2010), so their argument
is not borne out.

Recurrence and pregnancy rates

In our series, the recurrence rate of symptoms (severe dysmenorrhea,
severe dyspareunia and severe pelvic pain) evaluated prospectively
was 7% after shaving surgery. The rate of recurrent pain observed
in this large series is therefore no higher than the rate encountered
after more aggressive surgery, including bowel resection. In the
majority of series reporting data on bowel resection, the recurrence
rate of severe pelvic pain is evaluated to be between 6 and 20%

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Figure 6 A series of 500 cases of type II and III nodules.

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Donnez and Squifet

(A) Preoperative barium enema. (B) Laparoscopic rectal discoid resection. A rectal dilator (yellow) is introduced into the rectum. (C) Laparoscopic closure. (D) Postoperative barium enema conrms complete healing.

(Redwine and Wright, 2001; Duepree et al., 2002; Chapron et al.,

2004; Dara et al., 2005a, b; Emmanuel and Davis, 2005; Fleisch
et al., 2005; Ford et al., 2005; Seracchioli et al., 2005; Keckstein and
Wiesinger, 2006; Mereu et al., 2008; Meuleman et al., 2009).
However, in these studies, it is difcult to gauge the proportion of
women suffering from pelvic pain linked to a genuine recurrence of
endometriosis, and those with post-operative adhesions related to
severe complications, such as pelvic abscesses or peritonitis.
The favorable results observed in our study in terms of pelvic pain
recurrence may be explained by the almost complete resection of
deep nodular endometriosis, which is innervated abundantly by
sensory C cholinergic and adrenergic nerve bers, as recently demonstrated by Wang (2009). Even if some residual endometriotic foci
remain in the bowel muscularis, they are not related to pelvic pain persistence. On the other hand, as stated above, even when bowel resection is carried out, the margins are not free of disease in around 10%
of cases (Roman et al., 2007, 2010; Anaf et al., 2009).

The high pregnancy rate observed after surgery for deep lesions in
our study could be explained by three possible factors:
(i) Lesions are resected without extension or lateral dissection, frequently associated with subsequent adhesions in case of bowel
resection (Pachler and Wille-Jrgensen, 2005).
(ii) In almost 30% of cases, as described both previously (Nisolle and
Donnez, 1997) and in the present study, nodules are not associated with severe peritoneal endometriosis or ovarian
endometriomas.
(iii) When ovarian endometriotic lesions are present, use of the combined technique (Donnez et al., 2010) avoids removal of primordial follicles together with the endometrioma capsule, as
demonstrated by Muzii et al. (2005).
As vigorously discussed at the last World Endometriosis Society Congress in Melbourne (Donnez, 2008), it is time to discourage very
aggressive surgery under the false pretenses that a more radical

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Figure 7 A case of recurrence with bowel involvement, including the rectal mucosa, operated on by large discoid resection.

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Deep endometriotic nodules

Table III Complication rate after surgery for deep rectovaginal endometriotic nodules using the shaving technique
compared with bowel resection (selected systematic review).
Shaving technique
(data from present study)
(n 5 500)

Rectal resection (selected systematic review; Redwine and

Wright, 2001; Duepree et al., 2002; Chapron et al., 2004;
Dara et al., 2005a, b; Emmanuel and Davis, 2005; Fleisch
et al., 2005; Ford et al., 2005; Seracchioli et al., 2005;
Keckstein et al., 2006; Mereu et al., 2008; Meuleman et al.,
2009)

.............................................................................................................................................................................................
Laparoconversion

0%

5 11%

Repeat surgery

,0.1%

10%

Urinary retention

0.8% (n 4)

3 5%

Ureteral lesions (uroperitoneum)

0.8% (n 4)

2 4%

Fecal peritonitis, anastomotic leakage

0%

3 5%

Severe anastomotic stenosis

3%

Occlusion

0%

1%

0%

2 4%

0%

6 9%

Rectal perforation upon shaving (diagnosed and

repaired during surgery, no further
complications)

1.4% (n 7)

approach is more effective. It is certainly not true of endometriosis,

which is a benign disease. Women want to be free of symptoms,
have normal bladder and digestive function, and enjoy a normal sex
life. They do not necessarily want to be completely free of endometriosis. Indeed, as stated by Vercellini et al. (2003, 2005), the overall
extent of disease correlates neither with the frequency or severity
of symptoms, nor with the long-term prognosis in terms of conception
or pain recurrence.
In 2009, we can no longer accept Redwine and Wrights claim
(2001) that the success of surgical treatment is determined by how
much disease remains after operative intervention. Indeed, we
should bear in mind that radical bowel surgery is associated with longterm morbidity and, as previously reported in a Cochrane Review
(Pachler and Wille-Jrgensen, 2005), quality of life is signicantly
impaired following rectal resection.

Conclusion
Endometriosis is not cancer and does not require the same treatment
approach. Conservative surgery of deep endometriosis in young
women means preservation of organs, nerves and the vascular
blood supply. There is therefore a need for further strong and energetic debate to weigh up the benets of shaving (debulking surgery)
versus rectal resection (radical surgery). Feasibility is not always synonymous with efcacy.

Authors roles
J.D. rst described the shaving technique in 1995, performed surgery
in a large number of cases and wrote the manuscript. J.S. performed
surgery, established the MRI classication and participated in discussions about the manuscript.

References
Abrao MS, Goncalves MO, Dias JA Jr, Podgaec S, Chamie LP, Blasbalg R.
Comparison between clinical examination, transvaginal sonography and
magnetic resonance imaging for the diagnosis of deep endometriosis.
Hum Reprod 2007;22:3092 3097.
Adamyan L. Additional international perspectives. In: Nichols DH (ed).
Gynecologic and Obstetric Surgery. St. Louis: Mosby-Year Book, 1993,
1167 1182.
Anaf V, El Nakadi I, De Moor V, Coppens E, Zaeleman M, Noel JC.
Anatomic signicance of a positive barium enema in deep inltrating
endometriosis of the large bowel. World J Surg 2009;33:822 827.
Biberoglu KO, Berhrman SJ. Dosage aspects of danazol therapy in
endometriosis: short-term and long-term effectiveness. Am J Obstet
Gynecol 1981;136:645 654.
Chapron C, Liaras E, Fayet P, Hoeffel C, Fauconnier A, Vieira M,
Barakat H, Dousset B, Legmann P, Bonnin A et al. Magnetic
resonance imaging and endometriosis: deeply inltrating endometriosis
does not originate from the rectovaginal septum. Gynecol Obstet Invest
2002;53:204 208.
Chapron C, Chopin N, Borghese B, Malartic C, Decuypere F, Foulot H.
Surgical management of deeply inltrating endometriosis: an update.
Ann NY Acad Sci 2004;1034:326 337.
Chapron C, Chopin N, Borghese B, Foulot H, Dousset B, VacherLavenu MC, Vieira M, Hasan W, Bricou A. Deeply inltrating
endometriosis: pathogenetic implications of the anatomical distribution.
Hum Reprod 2006;21:1839 1845.
Dara E, Marpeau O, Thomassin I, Dubernard G, Barranger E, Bazot M.
Fertility after laparoscopic colorectal resection for endometriosis:
preliminary results. Fertil Steril 2005a;84:945 950.
Dara E, Thomassin I, Barranger E, Detchev R, Cortez A, Houry S, Bazot M
Feasibility and technical outcome of laparoscopic colorectal resection
for endometriosis. Am J Obstet Gynecol 2005b;192:394 400.
De Cicco C, Schonman R, Craessaerts M, Van Cleynenbreugel B, Ussia A,
Koninckx PR. Laparoscopic management of ureteral lesions in
gynecology. Fertil Steril 2009;92:1424 1427.

Downloaded from http://humrep.oxfordjournals.org/ by guest on December 22, 2015

Sepsis (pelvic abscess)

Rectovaginal stula

1958

Muzii L, Bellati F, Bianchi A, Palaia I, Manci N, Zullo M, Angioli R, Panici PB.

Laparoscopic stripping of endometriomas: a randomized trial on
different surgical techniques. Part II. Pathological results. Hum Reprod
2005;20:1987 1992.
Nisolle M, Donnez J. Peritoneal endometriosis, ovarian endometriosis, and
adenomyotic nodules of the rectovaginal septum are three different
entities. Fertil Steril 1997;68:585 596.
Ohba T, Mizutani H, Matsuura K, Ito M, Okamura H. Transrectal
ultrasonographic detection of uterosacral ligaments-preliminary study
for ultrasonographic evaluation of endometriosis. Nippon Sanka Fujinka
Gakkai Zasshi 1992;44:1187 1188.
Pachler J, Wille-Jrgensen P. Quality of life after rectal resection for cancer,
with or without permanent colostomy. Cochrane Database Syst Rev
2005;18:CD004323.
Possover M, Diebolder H, Plaut K, Schneider A. Laparoscopically assisted
vaginal resection of rectovaginal endometriosis. Obstet Gynecol 2000;
96:304 307.
Redwine DB, Wright JT. Laparoscopic treatment of complete obliteration
of the cul-de-sac associated with endometriosis: long-term follow-up of
en bloc resection. Fertil Steril 2001;76:358 365.
Reich H, McGlynn F, Salvat J. Laparoscopic treatment of cul-de-sac
obliteration secondary to retrocervical deep brotic endometriosis.
J Reprod Med 1991;36:516 522.
Roman H, Bourdel N. Against the systematic use of segmental resection in
colorectal endometriosis: do not replace the pain by unpleasant
digestive symptoms! Gynecol Obstet Fertil 2009;37:358 362.
Roman H, Puscasiu L, Kouteich K, Gromez A, Resch B,
Marouteau-Pasquier N, Hochain P, Tuech JJ, Scotte M, Marpeau L.
Laparoscopic management of deep endometriosis with rectal affect.
Chirurgia 2007;102:421 428.
Roman H, Loisel C, Resch B, Tuech JJ, Hochain P, Marpeau L. Delayed
functional outcomes associated with surgical management of rectal
endometriosis: giving our patients an informed choice. Hum Reprod
2010;25:890 899.
Seracchioli R, Poggioli G, Pierangeli F, Manuzzi L, Gualerzi B, Savelli L,
Remorgida V, Mabrouk M, Venturoli S. Surgical outcome and
long-term follow up after laparoscopic rectosigmoid resection in
women with deep inltrating endometriosis. BJOG 2005;
114:889 895.
Slack A, Child T, Lindsey I, Kennedy S, Cunningham C, Mortensen N,
Koninckx P, McVeigh E. Urological and colorectal complications following
surgery for rectovaginal endometriosis. BJOG 2007;14:12781282.
Squifet J, Feger C, Donnez J. Diagnosis and imaging of adenomyotic
disease of the retroperitoneal space. Gynecol Obstet Invest 2002;
54:43 51.
Vercellini P, Fedele L, Pietropaolo G, Frontino G, Somigliana E,
Crosignani PG. Progestogens for endometriosis: forward to the past.
Hum Reprod Update 2003;9:387 396.
Vercellini P, Pietropaolo G, De Giorgi O, Pasin R, Chiodini A,
Crosignani PG. Treatment of symptomatic rectovaginal endometriosis
with an estrogen-progestogen combination versus low-dose
norethindrone acetate. Fertil Steril 2005;84:1375 1387.
Vercellini P, Crosignani PG, Abbiati A, Somigliani E, Viagano P, Fedele L.
The effect of surgery for symptomatic endometriosis: the other side
of the story. Hum Reprod Update 2009;15:177 178.
Wang G. Rich innervation of deep inltrating endometriosis. Hum Reprod
2009;1:1 8.
Weingertner AS, Rodriguez B, Ziane A, Gibon E, Thoma V, Osario F,
Haddad C, Wattiez A. The use of JJ stent in the management of deep
endometriosis lesion, affecting or potentially affecting the ureter: a
review of our practice. BJOG 2008;115:1159 1164.

Downloaded from http://humrep.oxfordjournals.org/ by guest on December 22, 2015

Donnez J. Is accreditation for surgery necessary? World Endometriosis Soc

e-J 2008;10:6 7.
Donnez J, Squifet J. Laparoscopic excision of deep endometriosis. Obst
Gynecol Clin N Am 2004;31:567 580.
Donnez J, Nisolle M, Casanas-Roux F, Bassil S, Anaf V. Rectovaginal
septum endometriosis or adenomyosis: laparoscopic management in a
series of 231 patients. Hum Reprod 1995;10:630 635.
Donnez J, Nisolle M, Smoes P, Gillet N, Beguin S, Casanas-Roux F.
Peritoneal endometriosis and endometriotic nodules of the
rectovaginal septum are two different entities. Fertil Steril 1996;
66:362 368.
Donnez J, Nisolle M, Gillerot S, Smets M, Bassil S, Casanas-Roux F.
Rectovaginal septum adenomyotic nodules: a series of 500 cases. Br J
Obstet Gynaecol 1997;104:1014 1018.
Donnez J, Spada F, Squifet J, Nisolle M. Bladder endometriosis must be
considered as bladder adenomyosis. Fertil Steril 2000;74:1175 1181.
Donnez J, Nisolle M, Squifet J. Ureteral endometriosis: a complication of
rectovaginal endometriotic (adenomyotic) nodules. Fertil Steril 2002;
77:32 37.
Donnez J, Jadoul P, Donnez O, Squifet J. Laparoscopic excision of
rectovaginal and retrocervical endometriotric lesions. In: Donnez J
(ed). Atlas of Operative Laparoscopy and Hysteroscopy. UK: Informa
Healthcare, 2007, 63 75.
Donnez J, Lousse JC, Jadoul P, Donnez O, Squifet J. Laparoscopic
management of endometriomas using a combined technique of
excisional (cystectomy) and ablative surgery. Fertil Steril 2010;94:28 32.
Duepree HJ, Senagore AJ, Delaney CP, Marcello P, Brady KM, Falcone T.
Laparoscopic resection of deep pelvic endometriosis with rectosigmoid
involvement. J Am Coll Surg 2002;195:754 758.
Emmanuel KR, Davis C. Outcomes and treatment options in rectovaginal
endometriosis. Curr Opin Obstet Gynecol 2005;17:399 402.
Fleisch MC, Xas D, Bruyne FD, Hucke J, Bender HG, Dall P. Radical
resection of invasive endometriosis with bowel or bladder
involvement: long-term results. Eur J Obstet Gynecol Reprod Biol 2005;
123:224 229.
Ford J, English J, Miles WF, Giannopoulos T. A new technique for
laparoscopic anterior resection for rectal endometriosis. JSLS 2005;
9:73 77.
Jadoul P, Feyaerts A, Squifet J, Donnez J. Combined laparoscopic and
vaginal approach for nephrectomy, ureterectomy, and removal of a
large rectovaginal endometriotic nodule causing loss of renal function.
J Minim Invasive Gynecol 2007;14:256 259.
Keckstein J, Wiesinger H. The laparoscopic treatment of intestinal
endometriosis. In: Sutton C, Jones K, David Adamson G (eds).
Endometriosis. UK: Taylor & Francis, 2006, 177 187.
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.
Landi S, Ceccaroni M, Perutelli A, Allodi C, Barbieri F, Fiaccavento A,
Ruffo G, McVeigh E, Zanolla L, Minelli L. Laparoscopic nerve-sparing
complete excision of deep endometriosis: is it feasible? Hum Reprod
2006;21:774 781.
Maas K, Moriya Y, Kenter G, Trimbos B, van de Velde C. A plea for
preservation of the pelvic automatic nerves. Lancet 1999;354:772 773.
Mereu L, Gagliardi ML, Clarizia R, Mainardi P, Landi S, Minelli L.
Laparoscopic management of ureteral endometriosis in case of
moderate-severe hydroureteronephrosis. Fertil Steril 2010;93:46 51.
Meuleman C, Van Cleynenbreugel B, Beks N, DHooghe T. Outcome
after multidisciplinary CO2 laser laparoscopic excision of deep
inltrating colorectal endometriosis. Reprod Biomed Online 2009;
18:282 289.

Donnez and Squifet