hum. reprod.-2010-donnez-1949-58.pdf

ORIGINAL ARTICLE Gynaecology

Complications, pregnancy andrecurrence in a prospective series of500 patients operated on by theshaving technique for deeprectovaginal endometriotic nodulesJacques Donnez* and Jean SquiffletDepartment 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: [email protected]

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 deependometriosis 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. Thisis 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 inseven 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 fourcases (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 con-ceive. Of this number, 221 (57%) became pregnant naturally and 107 by means of IVF. In total, 328 women (84%) conceived. The recurrencerate was 8% among these 500 women, and it was significantly lower (P , 0.05) in women who became pregnant (3.6%) than in thosewho did not (15%). In women who failed to conceive, or were not interested in conceiving, severe pelvic pain recurred in 16–20% ofpatients.

conclusion: In young women, conservative surgery using the shaving technique preserves organs, nerves and the vascular bloodsupply, yielding a high pregnancy rate and low complication and recurrence rates. There is a need, however, for further strong and energeticdebate to weigh up the benefits of shaving (debulking surgery) versus rectal resection (radical surgery).

Key words: deep endometriosis / nodules / shaving technique / bowel resection

IntroductionIn the pelvis, three different forms of endometriosis must be con-sidered: (i) peritoneal endometriosis; (ii) ovarian endometriosis; and(iii) deep rectovaginal endometriosis (Donnez et al., 1996; Nisolleand Donnez, 1997).

The deep rectovaginal form of endometriosis has been defined asdeep endometriosis, rectovaginal endometriosis or adenomyosis ofthe rectovaginal septum. In the literature, it is also calleddeep-infiltrating endometriosis or posterior deep-infiltrating endome-triosis. According to the magnetic resonance imaging (MRI) classifi-cation described by Squifflet et al. (2002), most of these lesionsoriginate from the posterior part of the cervix and may infiltrate theanterior wall of the rectum.

Many different surgical techniques have been proposed and, surpris-ingly, the number of manuscripts advocating bowel resection has dra-matically increased over recent years (Redwine and Wright, 2001;Chapron et al., 2004; Daraı 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 ofthis approach.

Indeed, during meetings on this topic, the debate rages onbetween advocates of the shaving technique and supporters ofbowel resection in case of deep endometriosis with rectal muscularisinvolvement.

The goal of this manuscript is to present data from a prospectiveseries 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.For Permissions, please email: [email protected]

Human Reproduction, Vol.25, No.8 pp. 1949–1958, 2010

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pregnancy and recurrence rates by analyzing the existing literature andour own data. Pregnancy rate is an important outcome because pelvicsurgical procedures followed by complications (e.g. fistula, abscess)will often result in decreased fertility.

Patients and methodsFive hundred patients under 40 years of age operated on for deep endo-metriotic nodules were included in this study from 2004 to 2008. This wasa prospective study, conducted with the approval of the Ethics Committeeof the Catholic University of Louvain. Prospective evaluation is the onlyway to assess the recurrence rate, avoiding the bias of a retrospectiveanalysis (Table I).

Inclusion criteria were: (i) palpation of a nodule plus at least onesymptom of pain (dysmenorrhea, dyspareunia or rectal dyschezia) associ-ated or not with infertility; (ii) type II or III nodules (Squifflet et al., 2002);(iii) no previous surgery for endometriosis; (iv) surgical procedure per-formed by one of the authors; and (v) consent to be followed every 6months 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% ofcases and rectal dyschezia in 48% of cases (Table I).

Three hundred and twenty-four patients (64.8%) were suffering frompelvic pain associated with infertility. In all cases of infertility, evaluationof ovulation, cervical mucus–sperm interaction (postcoital test) andmale factor (defined as ,15 million sperm/ml using a Makler countingchamber) were undertaken. Six patients with ovulatory problems weretreated after surgery by clomiphene citrate or gonadotropins.

Careful clinical examination (Koninckx et al., 1996), transrectal ultraso-nography (TRUS) (Ohba et al., 1992), rectal endoscopic sonography(Abrao et al., 2007), transvaginal sonography (TVS), barium enema andMRI (Squifflet et al., 2002; Donnez and Squifflet, 2004) have all been rec-ommended to identify deep rectovaginal endometriotic lesions. Allpatients in this prospective study underwent clinical examination, TVS,TRUS, barium enema and MRI. In our series, examination with a speculum

revealed either a normal vaginal mucosa or a protruded bluish nodule inthe posterior fornix. By palpation, the diameter of the lesion could be eval-uated. Palpation is very often painful and the presence of a noduleaccounts for symptoms like deep dyspareunia and dysmenorrhea.

Preoperative radiography of the colon (barium enema) was systemati-cally carried out in order to assess the involvement of the rectal surfaceand its length. Profile radiography allows the best evaluation of infiltrationof the anterior rectal wall (Fig. 1; Squifflet et al., 2002).

According to Squifflet et al. (2002), there are three types of deep endo-metriotic 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 nodularlesions.

Type I nodules are pure rectovaginal septum lesions, situated far fromthe cervix. They are more commonly considered as vaginal lesions andtheir prevalence was only 10% in a previous study (Squifflet et al., 2002;Donnez and Squifflet, 2004). These lesions were not included in thepresent study, because they are never adherent to the rectum and donot require the shaving technique.

Only patients with type II and III nodules according to the classificationof Squifflet et al. (2002) were included in this series.

Type II nodules are lesions situated in the posterior vaginal fornix andbehind the cervix. Adamyan (1993) also clearly described, in her classifi-cation, endometriotic nodular lesions attached to the cervix and extendingto the rectovaginal septum and anterior part of the rectum.

Type III (hourglass-shaped) lesions (Fig. 3) occur when posterior fornixlesions extend cranially to the anterior rectal wall. Clinical evaluationusually reveals a larger lesion (more than 3 cm) and barium enemaalways shows infiltration and retraction of the rectal muscularis, knownas perivisceritis. This continuum between the rectal muscularis and thecervix is found to obliterate the rectovaginal septum cranially. Type IIIlesions always occur under the peritoneal fold of the recto-uterinepouch of Douglas. Infiltration of the rectal muscularis is consistentlyobserved in this subtype, as demonstrated by barium enema (profileimage; Fig. 1) and TRUS, but infiltration is generally limited to the muscu-laris without mucosal involvement. These lesions may also extend laterallyand involve the ureter (Donnez et al., 2002; Jadoul et al., 2007). In case ofnodules ≥3 cm in size, intravenous pyelography (IVP) is systematicallycarried out. In our series, ureteral involvement (deviation, stricture, sub-stenosis or stenosis) was observed in 66 cases (13.2%).

In the present study, type II and III nodules were observed in, respect-ively, 59.2 and 40.8% of cases (Table I).

Surgery: the shaving techniqueThere is no doubt that we should operate in case of symptomatic deepnodular lesions, but surgical techniques have taken some considerabletime to evolve. However, all of them involve (i) separation of the anteriorrectum from the posterior vagina, (ii) excision or ablation of deep endo-metriosis after complete dissection of the nodule from the posteriorpart of the cervix, systematically removing the posterior vaginal fornix(Fig. 4) and (iii) vaginal closure.

Surgical procedureIn our department, all laparoscopic procedures are performed undergeneral anesthesia. A 12-mm operative laparoscope is inserted througha vertical intraumbilical incision. Three other puncture sites are used: 2–3 cm above the pubis in the midline and in areas adjacent to the deepinferior epigastric vessels, which are visualized directly.

Deep endometriotic nodules involving the cul-de-sac require excision ofthe nodular tissue from the posterior vagina, rectum, posterior cervix anduterosacral ligaments.

Table I Characteristics of patients and incidence ofassociated lesions.

Age (mean, range) 26.1 (18–39 years)

Nodules (n patients; %)

Type II 296 (59.2%)

Type III 204 (40.8%)

Symptoms (n patients; %)

Dysmenorrhea 476 (95.2%)

Deep dyspareunia 432 (86.4%)

Rectal dyschezia 241 (48.2%)

Associated infertility (n patients; %) 324 (64.8%)

Associated endometriotic lesions (n patients; %)

None or minimal (one or two spots) 152 (30.4%)

Peritoneal (mild/moderate) 146 (29.2%)

Ovarian endometriosis (cyst . 2 cm) 352 (70.4%)

Bladder nodules 38 (7.6%)

Ureteral lesions (substenosis/stenosis) 66 (13.2%)

Patients underwent surgery for deep rectovaginal endometriotic nodules using theshaving technique.

1950 Donnez and Squifflet

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To determine the diagnosis of cul-de-sac obliteration during laparo-scopy, a sponge on a ring forceps is inserted into the posterior vaginalfornix. A dilator (Hegar 25) or rectal probe is systematically insertedinto the rectum (Donnez et al., 2007). In addition, a cannula is insertedinto the uterine cavity to markedly antevert the uterus. Complete oblitera-tion is diagnosed when the outline of the posterior fornix cannot be seenthrough the laparoscope.

Cul-de-sac obliteration is considered partial when rectal tenting isvisible, but a protrusion of the sponge into the posterior vaginal fornix isidentified between the rectum and the inverted U of the uterosacral liga-ments. Sometimes, however, deep lesions of the rectovaginal septum areonly barely visible by laparoscopy.

As previously mentioned, surgical techniques all involve separation ofthe anterior rectum from the posterior vagina and excision of thenodule in that area. Aquadissection and CO2 laser are used.

In case of nodules with possible ureteral involvement [suspected by MRIor IVP in 66 cases (13.2%) in our study], a JJ stent is inserted before start-ing the laparoscopic procedure and ureterolysis is then performed(Donnez et al., 2002). The usefulness of JJ stents in preventing subsequentcomplications was recently confirmed by Weingertner et al. (2008). Thegroup of Koninckx also published a large series of ureteral injuries (DeCicco et al., 2009). They demonstrated that ureteral repair was often

possible by laparoscopy with excellent outcomes. Moreover, in case oflateral extension, the uterine artery is often included in the fibroticprocess and needs to be clipped to prevent severe blood loss, whereasassociated bladder nodules require partial cystectomy (n ¼ 38; 7.6% inour series) according to a previously described technique (Donnezet al., 2000).

The follow-up duration in our series was 3.1 years (median, range 2–6years).

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

ResultsAll 500 patients were treated by laparoscopy. No conversion tolaparotomy 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 areremoved from the bladder, ureter and bowel, sometimes including

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

Barium enema: profile radiography allows the best evaluation of infiltration of the anterior rectal wall. Typical ‘endometriotic’ infiltration of the anterior rectal wall withoutstenosis is clearly visible. No infiltration of the mucosa is detected.

Deep endometriotic nodules 1951

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laparoscopic nephrectomy (n ¼ 4 cases in this study) during thesame procedure, as described by Jadoul et al. (2007). In somecases, type II nodules (,2 cm) could be removed in ,10 min,particularly when they were not adherent to the rectum, thevagina being sutured in 3 min. This explains why, in some cases,the duration of surgery was so short.

Peri- and post-operative complicationsIn our series of 500 cases, laparoscopic rectal perforation occurred inseven cases (1.4%) (Fig. 5A). In all these cases, barium enema had

detected muscularis involvement of more than 3 cm in length(profile radiography; Table II). The rectum was always repaired bylaparoscopy (Fig. 5B and C).

Laparoscopic suture was carried out through a full-thickness layerusing Vicryl 2.0 (Ethicon, Johnson and Johnson, USA) with separatestitches. The area was finally covered with fibrin glue (Tissucol,Johnson and Johnson, USA; Fig. 5D). Among the seven cases,neither fistulas nor any other complications were observed. Rectalmuscle defects frequently arise during the shaving procedure andare repaired by suturing. If the rectal lumen is not entered, it isnot considered a complication, just part of the procedure.

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.

Figure 2 Classification of deep endometriotic nodules.

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


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Four cases (0.8%) of ureteral injury were noted in our patients.One case was diagnosed on the first post-operative day by thepresence of abundant fluid in the peritoneal cavity. High levels ofurea and creatinine in the ‘peritoneal’ fluid and IVP confirmed thediagnosis of a lateral ureteral lesion. A JJ catheter was immediatelyinserted and remained in place for 3 months. Hydronephrosiswas detected 1 month after removal of the JJ stent, and thiswoman needed vesico-ureteral reimplantation for hydronephrosisowing to fibrotic stenosis of the lower ureteral segment andnephrostomy.

The remaining three cases of ureteral injury were the result ofthermal damage (bipolar coagulation). The patients presented 6–8days after their initial surgery with diffuse abdominal pain and liquidin the lower abdomen. Pyelography revealed lateral ureteral lesions.They were treated by insertion of a JJ stent, which was removed3 months later and the patients made a full recovery.

Temporary urinary retention was observed in four cases (0.8%), butnormal micturition resumed within 2 weeks of surgery.

Pregnancy rates and recurrenceThe duration of follow-up was 2–6 years (median 3.1 years) (Fig. 6).Among the 500 women, 388 (78%) wished to conceive (Fig. 6). Of thisnumber, 221 (57%) became pregnant naturally during follow-up.

After delivery, progestogens were administered, consistent with thefindings of Vercellini et al. (2003, 2005), who proved that continuousoral contraceptives and progestogens were effective at preventingrecurrence of symptoms. Progestogens [Primolut-Nor 5 mg (norethis-terone), Bayer, Berlin, Germany] were continued until patients wishedto become pregnant again. In this subgroup of 221 women, recurrencewas noted in only four cases (2%).

Among the 388 women who wished to conceive, 167 (43%) under-went IVF procedures (from 1 to 6 attempts) because they failed to fallpregnant naturally (after 1 year of regular sexual intercourse), orbecause of severe male factor infertility (n ¼ 42; 25%), requiringimmediate 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). Sixwomen experienced recurrence of pelvic pain during IVF and twoafter delivery. Among these 107 women, the recurrence rate ofpelvic pain was therefore 7.4% (n ¼ 8). Among the 60 women whofailed to conceive, recurrence of severe pelvic pain was reported in12 (20%), the majority of whom were then successfully treated withprogestogens [Primolut-Nor 5 mg (norethisterone), Bayer, Berlin,Germany].

Of the 500 women in our series, 112 (22%) did not wish to con-ceive. Continuous progestogens or oral contraceptives (containing20 mg of ethinylestradiol) were administered to all of these patients.Recurrence of severe pelvic pain (severe dysmenorrhea and severedeep dyspareunia according to Biberoglu and Berhman, 1981) wasnoted in 15 cases (13%).

Repeat surgery was carried out for recurrence of severe pelvic painresistant to medical therapy in 12 women. Seven of them underwentnodule resection, three underwent anterior segmental bowel resec-tion, and two underwent large discoid resection (Fig. 7) becauserecurrence was associated with bowel involvement, including themucosa, as confirmed by colonoscopy and biopsy. Surgery was per-formed by laparoscopy in all cases. Discoid bowel resection remainsa possibility (Fig. 7A–D), even after the shaving technique.

Recurrence of pelvic pain was thus found to be significantly 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 recur-rence rate among all 500 women, it gives a figure of 7.8% (39/500).

DiscussionSurgery for deep rectovaginal endometriosis was first described byReich et al. (1991), and the first two large series including 231 and500 women, respectively, were published in 1995 and 1997(Donnez et al., 1995, 1997).

Although these papers concluded that it is prudent to curtail ratherthan encourage the widespread use of an aggressive and potentiallymorbid procedure, increasingly aggressive surgery, including bowel

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


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resection, is still systematically proposed in case of deep endometrio-sis with muscularis involvement, even in the absence of mucosal invol-vement (Redwine and Wright, 2001; Chapron et al., 2002; 2004;2006; Daraı 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 comparedwith shaving surgery. The lack of evidence of better improvement incase of bowel resection was recently underlined by Vercellini et al.(2009).

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

2004; Daraı et al., 2005a, b; Emmanuel and Davis, 2005; Fleischet al., 2005; Ford et al., 2005; Seracchioli et al., 2005; Keckstein andWiesinger, 2006; Mereu et al., 2008; Meuleman et al., 2009). Unfortu-nately, much of the recent literature appears to encourage very inva-sive techniques, including bowel resection in case of rectal muscularisinvolvement. Our review of recent publications (see above) reportingthe results and complications of laparoscopy-assisted bowel resectionfor deep endometriotic nodules reveals a relatively high complicationrate compared with the shaving technique. Indeed, rates of urinaryretention (3–5%), ureteral lesions (2–4%), fecal peritonitis (3–5%),severe anastomotic stenosis (3%), rectovaginal fistulas (6–9%) andpelvic abscesses (2–4%) were found to be higher than with theshaving technique. A possible bias could have been the relativelysmall number of patients involved in some series (Seracchioli et al.,2005), but it should be pointed out that, even in very experiencedhands (Daraı et al., 2005b; Keckstein and Wiesinger, 2006), the rateof severe complications (rectovaginal fistulas, abscesses, stenosis,fecal peritonitis) can be more than 10%.

Very recently, Meuleman et al. (2009) reported an 11% rate ofsevere complications, some of which resulted from the duration ofsurgery (mean over 7 h). Indeed, lower leg compartment syndromewas observed in three cases (3/56), requiring fasciotomy. It is impor-tant to note that there was no mucosal infiltration of the rectum in thisseries. This relatively high rate of severe complications was encoun-tered despite a multidisciplinary approach including a urologist anddigestive surgeon. In this series, the median operating time was 7 h16 min (range 180–780 min). The duration is also related to costsfor the hospital (operating room, nurses, anesthetist, etc.).

It should also be pointed out that colorectal segmental resection is acomplex procedure, sometimes resulting in pelvic nerve damage andunpleasant urinary and digestive symptoms (Slack et al., 2007;Roman and Bourdel, 2009; Vercellini et al., 2009; Roman et al., 2010).

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

Table II A series of 500 cases of deep endometriosistreated by the laparoscopic shaving technique withoutsegmental resection.

Laparoscopic shaving surgery (n ¼ 500)

Lesion size (cm) 3.4 (2–6)

Duration of surgery (min) 78 (50–218)

Post-operative hospitalization (days) 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%)


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Care must always be taken to preserve the pelvic autonomicnerves, as they are the pathway for the neurogenic control of rectal,bladder and sexual arousal function (Maas et al., 1999; Possoveret al., 2000; Landi et al., 2006). The shaving technique allows preser-vation of the nerves by avoiding deep lateral rectal dissection (necess-ary for rectosigmoid resection). Indeed, lateral dissection is mandatoryonly in case of lateral extension of the disease with ureteral involve-ment (Donnez et al., 2002) and, even in this case, it rarely involves dis-section 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 beenable to prove that it is any more effective than the shaving technique.Very recently, Landi et al. (2006) reported that full-thickness disc exci-sion using a circular stapler could prevent the potential morbidityassociated with low anastomosis. As only a few months earlier thesame group (Mereu et al., 2008) reported a major complication ratethat required repeat operations in 20 among 192 cases (10.4%),they are now probably evaluating a less aggressive surgical techniquethan bowel resection (Landi et al., 2006). The same trend awayfrom bowel resection toward a less aggressive approach has recentlybeen described by Slack et al. (2007) and Roman et al. (2010).

In our hands, the shaving approach has proved to be adequate. Inmost cases, muscularis infiltration observed in all cases of type IIIlesions may be left in place, at least partially, since the shaving tech-nique already removes what is necessary. Residual lesions in the mus-cularis of the rectum do not evolve and remain constant for a longtime (Donnez and Squifflet, 2004). The argument used by some gyne-cologists and surgeons to defend bowel resection is that this pro-cedure is more ‘radical’. This is simply not true. Indeed, even withbowel resection, the margins are not free of disease in more than10% of cases (Anaf et al., 2009; Roman et al., 2010), so their argumentis not borne out.

Recurrence and pregnancy ratesIn our series, the recurrence rate of symptoms (severe dysmenorrhea,severe dyspareunia and severe pelvic pain) evaluated prospectivelywas 7% after shaving surgery. The rate of recurrent pain observedin this large series is therefore no higher than the rate encounteredafter more aggressive surgery, including bowel resection. In themajority of series reporting data on bowel resection, the recurrencerate of severe pelvic pain is evaluated to be between 6 and 20%

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

Analysis at 3 years of follow-up.


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(Redwine and Wright, 2001; Duepree et al., 2002; Chapron et al.,2004; Daraı et al., 2005a, b; Emmanuel and Davis, 2005; Fleischet al., 2005; Ford et al., 2005; Seracchioli et al., 2005; Keckstein andWiesinger, 2006; Mereu et al., 2008; Meuleman et al., 2009).However, in these studies, it is difficult to gauge the proportion ofwomen suffering from pelvic pain linked to a genuine recurrence ofendometriosis, and those with post-operative adhesions related tosevere complications, such as pelvic abscesses or peritonitis.

The favorable results observed in our study in terms of pelvic painrecurrence may be explained by the almost complete resection ofdeep nodular endometriosis, which is innervated abundantly bysensory C cholinergic and adrenergic nerve fibers, as recently demon-strated by Wang (2009). Even if some residual endometriotic fociremain in the bowel muscularis, they are not related to pelvic pain per-sistence. On the other hand, as stated above, even when bowel resec-tion 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 inour study could be explained by three possible factors:

(i) Lesions are resected without extension or lateral dissection, fre-quently associated with subsequent adhesions in case of bowelresection (Pachler and Wille-Jørgensen, 2005).

(ii) In almost 30% of cases, as described both previously (Nisolle andDonnez, 1997) and in the present study, nodules are not associ-ated with severe peritoneal endometriosis or ovarianendometriomas.

(iii) When ovarian endometriotic lesions are present, use of the com-bined technique (Donnez et al., 2010) avoids removal of primor-dial follicles together with the endometrioma capsule, asdemonstrated by Muzii et al. (2005).

As vigorously discussed at the last World Endometriosis Society Con-gress in Melbourne (Donnez, 2008), it is time to discourage veryaggressive surgery under the false pretenses that a more radical

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

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


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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 sexlife. They do not necessarily want to be completely free of endome-triosis. Indeed, as stated by Vercellini et al. (2003, 2005), the overallextent of disease correlates neither with the frequency or severityof symptoms, nor with the long-term prognosis in terms of conceptionor pain recurrence.

In 2009, we can no longer accept Redwine and Wright’s claim(2001) that the success of surgical treatment is determined by howmuch disease remains after operative intervention. Indeed, weshould bear in mind that radical bowel surgery is associated with long-term morbidity and, as previously reported in a Cochrane Review(Pachler and Wille-Jørgensen, 2005), quality of life is significantlyimpaired following rectal resection.

ConclusionEndometriosis is not cancer and does not require the same treatmentapproach. Conservative surgery of deep endometriosis in youngwomen means preservation of organs, nerves and the vascularblood supply. There is therefore a need for further strong and ener-getic debate to weigh up the benefits of shaving (debulking surgery)versus rectal resection (radical surgery). Feasibility is not always synon-ymous with efficacy.

Authors’ rolesJ.D. first described the shaving technique in 1995, performed surgeryin a large number of cases and wrote the manuscript. J.S. performedsurgery, established the MRI classification and participated in discus-sions about the manuscript.

ReferencesAbrao MS, Goncalves MO, Dias JA Jr, Podgaec S, Chamie LP, Blasbalg R.

Comparison between clinical examination, transvaginal sonography andmagnetic 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 significance of a positive barium enema in deep infiltratingendometriosis of the large bowel. World J Surg 2009;33:822–827.

Biberoglu KO, Berhrman SJ. Dosage aspects of danazol therapy inendometriosis: short-term and long-term effectiveness. Am J ObstetGynecol 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. Magneticresonance imaging and endometriosis: deeply infiltrating endometriosisdoes not originate from the rectovaginal septum. Gynecol Obstet Invest2002;53:204–208.

Chapron C, Chopin N, Borghese B, Malartic C, Decuypere F, Foulot H.Surgical management of deeply infiltrating endometriosis: an update.Ann NY Acad Sci 2004;1034:326–337.

Chapron C, Chopin N, Borghese B, Foulot H, Dousset B, Vacher-Lavenu MC, Vieira M, Hasan W, Bricou A. Deeply infiltratingendometriosis: pathogenetic implications of the anatomical distribution.Hum Reprod 2006;21:1839–1845.

Daraı 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.

Daraı E, Thomassin I, Barranger E, Detchev R, Cortez A, Houry S, Bazot MFeasibility and technical outcome of laparoscopic colorectal resectionfor 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 ingynecology. Fertil Steril 2009;92:1424–1427.

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Table III Complication rate after surgery for deep rectovaginal endometriotic nodules using the shaving techniquecompared with bowel resection (selected systematic review).

Shaving technique(data from present study)(n 5 500)

Rectal resection (selected systematic review; Redwine andWright, 2001; Duepree et al., 2002; Chapron et al., 2004;Daraı et al., 2005a, b; Emmanuel and Davis, 2005; Fleischet 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 ¼ 4) 3–5%

Ureteral lesions (uroperitoneum) 0.8% (n ¼ 4) 2–4%

Fecal peritonitis, anastomotic leakage 0% 3–5%

Severe anastomotic stenosis – 3%

Occlusion 0% 1%

Sepsis (pelvic abscess) 0% 2–4%

Rectovaginal fistula 0% 6–9%

Rectal perforation upon shaving (diagnosed andrepaired during surgery, no furthercomplications)

1.4% (n ¼ 7) –


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Donnez J. Is accreditation for surgery necessary? World Endometriosis Soce-J 2008;10:6–7.

Donnez J, Squifflet J. Laparoscopic excision of deep endometriosis. ObstGynecol Clin N Am 2004;31:567–580.

Donnez J, Nisolle M, Casanas-Roux F, Bassil S, Anaf V. Rectovaginalseptum endometriosis or adenomyosis: laparoscopic management in aseries 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 therectovaginal 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 JObstet Gynaecol 1997;104:1014–1018.

Donnez J, Spada F, Squifflet J, Nisolle M. Bladder endometriosis must beconsidered as bladder adenomyosis. Fertil Steril 2000;74:1175–1181.

Donnez J, Nisolle M, Squifflet J. Ureteral endometriosis: a complication ofrectovaginal endometriotic (adenomyotic) nodules. Fertil Steril 2002;77:32–37.

Donnez J, Jadoul P, Donnez O, Squifflet J. Laparoscopic excision ofrectovaginal and retrocervical endometriotric lesions. In: Donnez J(ed). Atlas of Operative Laparoscopy and Hysteroscopy. UK: InformaHealthcare, 2007, 63–75.

Donnez J, Lousse JC, Jadoul P, Donnez O, Squifflet J. Laparoscopicmanagement of endometriomas using a combined technique ofexcisional (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 rectosigmoidinvolvement. J Am Coll Surg 2002;195:754–758.

Emmanuel KR, Davis C. Outcomes and treatment options in rectovaginalendometriosis. Curr Opin Obstet Gynecol 2005;17:399–402.

Fleisch MC, Xafis D, Bruyne FD, Hucke J, Bender HG, Dall P. Radicalresection of invasive endometriosis with bowel or bladderinvolvement: long-term results. Eur J Obstet Gynecol Reprod Biol 2005;123:224–229.

Ford J, English J, Miles WF, Giannopoulos T. A new technique forlaparoscopic anterior resection for rectal endometriosis. JSLS 2005;9:73–77.

Jadoul P, Feyaerts A, Squifflet J, Donnez J. Combined laparoscopic andvaginal approach for nephrectomy, ureterectomy, and removal of alarge rectovaginal endometriotic nodule causing loss of renal function.J Minim Invasive Gynecol 2007;14:256–259.

Keckstein J, Wiesinger H. The laparoscopic treatment of intestinalendometriosis. 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 deependometriosis by clinical examination during menstruation and plasmaCA-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-sparingcomplete excision of deep endometriosis: is it feasible? Hum Reprod2006;21:774–781.

Maas K, Moriya Y, Kenter G, Trimbos B, van de Velde C. A plea forpreservation 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 ofmoderate-severe hydroureteronephrosis. Fertil Steril 2010;93:46–51.

Meuleman C, Van Cleynenbreugel B, Beks N, D’Hooghe T. Outcomeafter multidisciplinary CO2 laser laparoscopic excision of deepinfiltrating colorectal endometriosis. Reprod Biomed Online 2009;18:282–289.

Muzii L, Bellati F, Bianchi A, Palaia I, Manci N, Zullo M, Angioli R, Panici PB.Laparoscopic stripping of endometriomas: a randomized trial ondifferent surgical techniques. Part II. Pathological results. Hum Reprod2005;20:1987–1992.

Nisolle M, Donnez J. Peritoneal endometriosis, ovarian endometriosis, andadenomyotic nodules of the rectovaginal septum are three differententities. Fertil Steril 1997;68:585–596.

Ohba T, Mizutani H, Matsuura K, Ito M, Okamura H. Transrectalultrasonographic detection of uterosacral ligaments-preliminary studyfor ultrasonographic evaluation of endometriosis. Nippon Sanka FujinkaGakkai Zasshi 1992;44:1187–1188.

Pachler J, Wille-Jørgensen P. Quality of life after rectal resection for cancer,with or without permanent colostomy. Cochrane Database Syst Rev2005;18:CD004323.

Possover M, Diebolder H, Plaut K, Schneider A. Laparoscopically assistedvaginal resection of rectovaginal endometriosis. Obstet Gynecol 2000;96:304–307.

Redwine DB, Wright JT. Laparoscopic treatment of complete obliterationof the cul-de-sac associated with endometriosis: long-term follow-up ofen bloc resection. Fertil Steril 2001;76:358–365.

Reich H, McGlynn F, Salvat J. Laparoscopic treatment of cul-de-sacobliteration secondary to retrocervical deep fibrotic endometriosis.J Reprod Med 1991;36:516–522.

Roman H, Bourdel N. Against the systematic use of segmental resection incolorectal endometriosis: do not replace the pain by unpleasantdigestive 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. Delayedfunctional outcomes associated with surgical management of rectalendometriosis: giving our patients an informed choice. Hum Reprod2010;25:890–899.

Seracchioli R, Poggioli G, Pierangeli F, Manuzzi L, Gualerzi B, Savelli L,Remorgida V, Mabrouk M, Venturoli S. Surgical outcome andlong-term follow up after laparoscopic rectosigmoid resection inwomen with deep infiltrating 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 followingsurgery for rectovaginal endometriosis. BJOG 2007;14:1278–1282.

Squifflet J, Feger C, Donnez J. Diagnosis and imaging of adenomyoticdisease 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 endometriosiswith an estrogen-progestogen combination versus low-dosenorethindrone 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 sideof the story. Hum Reprod Update 2009;15:177–178.

Wang G. Rich innervation of deep infiltrating endometriosis. Hum Reprod2009;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 deependometriosis lesion, affecting or potentially affecting the ureter: areview of our practice. BJOG 2008;115:1159–1164.


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