Short-term outcome of fertility-sparing laparoscopic excision of deeply infiltrating pelvic endometriosis performed in a tertiary referral center

ENDOMETRIOSIS Short-term outcome of fertility-sparing laparoscopic excision of deeply infiltrating pelvic endometriosis performed in a tertiary referral center George K. Pandis, M.R.C.O.G., a Ertan Saridogan, Ph.D., M.R.C.O.G., a Alastair C. J. Windsor, M.D., F.R.C.S., b Cagri Gulumser, M.D., a C. Richard G. Cohen, M.D., F.R.C.S., b and Alfred S. Cutner, M.D., M.R.C.O.G. a a Institute of Women s Health, University College London Hospitals; and b Department of Colorectal Surgery, University College London Hospitals, London, United Kingdom Objective: To examine the short-term surgical outcomes in women undergoing fertility-sparing laparoscopic excision of deeply infiltrating pelvic endometriosis. Design: Retrospective cohort study. Setting: Tertiary referral center for treatment of endometriosis, a university teaching hospital, London, United Kingdom. Patient(s): A total of 177 women who underwent fertility-sparing laparoscopic excision of deeply infiltrating endometriosis between January 1, 2006, and December 31, 2007. Intervention(s): Eligible women were identified from the surgeons database, and their medical notes were reviewed. Data from preoperative assessment, surgery, and postoperative outcomes were analyzed. Main Outcome Measure(s): Complication rate. Result(s): One hundred seventy-seven women underwent fertility-sparing laparoscopic excision of deeply infiltrating endometriosis including excision of uterosacral ligaments (43, 24.3%), excision of rectovaginal septum (56, 31.6%), rectal shave (56, 31.6%), disk excision (7, 4%) or bowel resection (15, 8.5%). The median operative time was 95 minutes with a range of 30 to 270 minutes (interquartile range 75 120 minutes). Overall, complications developed in 18 women (10.2%). In 12 (6.8%) of these only uncomplicated pyrexia developed whereas significant intraoperative and/or postoperative complications developed in the remaining 6 (3.4%). Women spent a median of 2 days recovering in hospital (range 1 7, interquartile range 2 3 days). Conclusion(s): Fertility-sparing laparoscopic excision of deeply infiltrating endometriosis appears to be safe with a low short-term complication rate. (Fertil Steril Ò 2010;93:39 45. Ó2010 by American Society for Reproductive Medicine.) Key Words: Laparoscopy, excision, endometriosis, deeply infiltrating, complications Endometriosis is characterized by the presence of endometrial glands and stroma outside the uterus. The incidence in the female population at their reproductive age is between 10% and 15% (1 4). Deep pelvic endometriosis comprises 20% to 35% of women with endometriosis (5). Its manifestation includes endometrial implants, fibrosis, and muscular hyperplasia. It mainly affects the uterosacral ligaments, the rectovaginal septum, and the rectosigmoid colon with Received August 1, 2008; revised September 10, 2008; accepted September 14, 2008; published online October 29, 2008. G.K.P. has nothing to disclose. E.S. received honoraria from Ethicon Endo-Surgery for speaking and teaching. A.C.J.W. has nothing to disclose. C.G. has nothing to disclose. C.R.C.G. has nothing to disclose. A.S.C. received educational support to Storz and Ethicon Endo- Surgery. Reprint requests: Alfred S. Cutner, M.D., UCL Institute of Women s Health, Elizabeth Garrett Anderson and Obstetric Hospital, Huntley Street, London, WC1E 6DH, United Kingdom (FAX: 00442073908408; E-mail: alfred.cutner@uclh.nhs.uk). complete or partial obliteration of the pouch of Douglas (6). Intestinal endometriosis is one of the most severe forms and accounts for 5% to 12% of women in whom the disease is diagnosed (2 4). It may also affect the lower urinary tract (7). Traditional treatment for deep pelvic endometriosis was total abdominal hysterectomy and bilateral salpingo-oophorectomy, leaving behind in most cases the fibrotic, deeply infiltrating endometriotic tissue in the pelvis (8 11). This was due to the surgical difficulty in achieving complete clearance. However, it is now accepted that effective symptomatic management requires complete excision of the rectovaginal disease (12 15). Furthermore a proportion of these women may wish to preserve their fertility. Advancements in laparoscopic surgery have enabled a fertility-sparing approach for this group of patients (16 19). Thus hysterectomy and removal of both ovaries are not mandatory. This approach is effective in reducing pain and improving quality of life and results in increased fertility rates (15, 20 24). 0015-0282/10/$36.00 Fertility and Sterility â Vol. 93, No. 1, January 2010 39 doi:10.1016/j.fertnstert.2008.09.051 Copyright ª2010 American Society for Reproductive Medicine, Published by Elsevier Inc.

Surgical management of severe disease often requires a multidisciplinary team approach, because surgery may be complex, requiring input from colorectal and urologic colleagues. In our center we have been practicing complete surgical excision of all affected tissue for almost a decade. Our current multidisciplinary approach to surgery was established fully by the beginning of 2006. Laparoscopic skills of the gynecologists, colorectal surgeons, and urologists involved in the endometriosis center were developed fully by this time. The aim of this study was to examine the shortterm surgical outcome in this group of patients. In particular, we wished to assess the rate of surgical complications. MATERIALS AND METHODS All women undergoing laparoscopic excision of deeply infiltrating pelvic endometriosis between January 1, 2006, and December 31, 2007, were included in this retrospective review. Eligible cases were identified from operative databases. Relevant preoperative, intraoperative, and postoperative data were retrieved from the medical notes. In those women undergoing a two-stage operation, only data from the second procedure were analyzed, because the first procedure was invariably a diagnostic one. The surgical treatment and follow-up were part of standard management of women attending the Endometriosis Centre at University College Hospital. The retrospective review of anonymized data was performed following the ethical principles found in the Declaration of Helsinki as developed by the World Medical Association. This audit had the approval of the hospital Audit Department (institutional board approval), and data were presented in the scheduled obstetrics and gynecology audit meeting. Women were referred to the endometriosis center for treatment either by their general practitioner or by other gynecologists. The latter group commonly had had a primary laparoscopic assessment and, sometimes, partial treatment before referral. Previous medical or surgical treatment for endometriosis was recorded. All women who had been sexually active underwent a vaginal examination to assess for rectovaginal endometriotic nodules. Preoperative assessment included a pelvic scan and renal scan in all cases. In cases of ureteric involvement with hydronephrosis, further evaluation by one of the two collaborating urologists was sought, which could include further contrast imaging and preoperative ureteric stenting. Some women in whom the predominant symptoms were dyschezia or menstrual rectal bleeding underwent a magnetic resonance imaging or an outpatient endoscopic examination of the bowel. After extensive counseling regarding the associated risks of surgery all women provided a written consent. Where extensive disease was already diagnosed, GnRH analogues (GnRH-as) were given before surgery. Those women not given analogues were specifically warned of the possibility of a two-stage procedure, the first stage being drainage of endometriotic cysts. This was followed by GnRH-as and then excisional surgery of the rectovaginal disease. All women had bowel preparation taken at home (10 mg sodium picosulfate with magnesium citrate per sachet; Picolax, Ferring Pharmaceuticals, Slough, Berkshire, United Kingdom) 1 day before surgery and were admitted to the hospital on the day of surgery. The patients received general anesthesia and were placed in Lloyd-Davies position. A Foley catheter was placed into the bladder, and a uterine manipulator placed in the uterus. Prophylactic antibiotics were administered intravenously. A carbon dioxide pneumoperitoneum at a pressure of 20 mm Hg was created via a Veress needle inserted into the peritoneal cavity through an umbilical incision. Where the patient had a previous laparotomy, an initial subcostal insertion was used after the introduction of a nasogastric tube (25). The umbilical port was then inserted after clearance of relevant adhesions. For very thin patients a Hasson entry was used (26). Three additional ports were used to carry out the surgery. Two secondary 5-mm ports were inserted at the level of the umbilicus lateral to the rectus sheath, and a further 5-mm or 12-mm port was inserted in the midline in the suprapubic region. The diameter of the latter port depended on the intention to perform laparoscopic suturing or laparoscopic bowel resection. We routinely performed initial bilateral ovarian suspension to facilitate access to the pelvis (27). If endometriomas were present, drainage and either stripping or ablation with bipolar diathermy (where there was not an easily identifiable capsule) was performed before ovarian suspension. The rectosigmoid colon was mobilized from the congenital adhesions on the left pelvic side wall to allow for optimal exposure. Bilateral ureterolysis was then carried out to move the ureters lateral to the rectovaginal nodule. Ureteric catheters were used selectively where ureteric identification was difficult. The pararectal spaces were identified and opened, and the rectum separated from the vagina. The extent of excision depended on the degree of disease. In milder cases the uterosacral ligaments were excised. In more severe cases the rectovaginal septum was also excised. This included partial- or full-thickness excision of involved vagina in some cases. Vaginal defects were closed laparoscopically or vaginally depending on the extension of the defect. Bowel excision required either shaving the endometriosis off the surface or discoid excision of bowel or a segmental resection. Occasionally, where indicated, a covering ileostomy was performed at the end of the procedure; this was considered to be a required primary surgical step taken by the attending colorectal surgeon and thus was not included in the short-term complications. The majority of the above surgical procedures were carried out entirely by the gynecologic team. Colorectal assistance was required for some bowel dissections, disk resections, segmental resections, and ileostomies. The instruments used included endoscopic graspers, laparoscopic scissors, bipolar 40 Pandis et al. Laparoscopic excision of endometriosis Vol. 93, No. 1, January 2010

forceps, an aspiration-irrigation system, and a harmonic scalpel (ACE Ultracision; Ethicon Endo-Surgery, Cincinnati, OH). Bowel defects were closed laparoscopically in layers with 3 0 0 PDS II (polydioxanone) suture (Ethicon) in two layers. Segmental resection involved initial mobilization and the application of a laparoscopic stapler below the level affected. The suprapubic incision was then extended to allow exteriorization of the proximal end and removal of the affected area. After insertion of the head of a circular stapler in the healthy proximal bowel lumen, a circular running suture was inserted at the edge of the proximal bowel and tied safely to secure the position of the inserted head. The bowel was then reinserted into the abdomen, and the abdominal incision was closed. A circular stapler was introduced rectally, and an end-to-end anastomosis was carried out under laparoscopic guidance. Bowel integrity was always checked by an underwater air leak test with use of either a 50-mL syringe or a rigid sigmoidoscope in those cases of significant bowel dissection. The urinary catheter inserted at the time of surgery was removed at 6 AM the following morning. A trial of voiding was then instituted with postvoid residuals checked by bladder sonography. Those with residuals >150 ml had the catheter reinserted with antibiotic cover, and a further trial of voiding was commenced the day after. The remaining individuals in whom the trial was unsuccessful were given a third trial day, and if this failed they were discharged home with an indwelling catheter and an appropriate follow-up appointment. In this study analysis of short-term surgical outcomes is presented. All patients were clinically reviewed in the outpatient endometriosis clinic 3 months after surgery or earlier in cases requiring urgent medical attention. Postoperative evaluation consisted of general assessment of well-being, pelvic examination, and transvaginal pelvic ultrasonography where clinically indicated. Operative and postoperative data recorded from the notes review included type of surgery, operative time (calculated from first incision to skin closure), immediate postoperative complications, return to theater, readmission, duration of bladder catheterization, and length of hospitalization. Histologic confirmation of endometriosis also was noted. Statistical Analysis Descriptive data were examined for normality of distribution with use of the Shapiro-Wilks test. They are described as mean and SD for normally distributed data and median and interquartile range (IQR) when not normally distributed. RESULTS Over the study period a total of 354 women underwent laparoscopic treatment of endometriosis in our center. We analyzed data from all 177 women who underwent fertility-sparing laparoscopic excision of deeply infiltrating pelvic endometriosis. This included excision of uterosacral TABLE 1 Presenting symptoms of women in the study. Symptoms No. (N [ 177) % Dysmenorrhea 166 93.8 Pelvic pain 145 81.9 Dyspareunia 85 48.0 Dyschezia 40 22.6 Menorrhagia 22 12.4 Infertility 17 9.6 Constipation 15 8.5 Bladder pain 14 7.9 Rectal bleeding 13 7.3 Other 4 2.3 Bladder bleeding 3 1.7 ligaments, excision of rectovaginal septum, rectal shave, disk excision of bowel, and bowel resection. The women s age in the study was 33.2 5.9 years. In this study group 153 (86.4%) women were nulliparous. Presenting symptoms are shown in Table 1, and the majority of women (93.2%) had more than one presenting symptom. In this cohort 56 (31.6%) women had received prior medical treatment for endometriosis. More specifically, 38 (21.5%) women had been taking the oral contraceptive pill, a further 11 (6.2%) had received GnRH-as, and the remaining 7 (3.9%) had been taking progestogenic agents including the Mirena intrauterine system (Bayer HealthCare Pharmaceuticals, Newbury, Berkshire, United Kingdom). A previous laparoscopic treatment was reported by 48 (27.1%) women, and of these 12 (25%) had more than one previous laparoscopic treatment. A previous laparotomy was reported by 10 (5.6%) women. Sixty-three (35.6%) women began taking GnRH-as before surgery. A two-stage procedure was performed in 34 (19.2%) women. In 44 (24.9%) cases other disciplines were required for surgery; in 34 the assistance of the colorectal team was required, in two cases urologic input was sought, and in 8 cases both disciplines were involved in the surgery. The majority of urologic involvement was related to insertion of JJ ureteric stents. Only one case was converted to laparotomy (lower abdominal transverse incision) for completion of the bowel surgery because of difficulty in mobilization. The conversion rate was therefore 0.6%. The median operative time was 95 minutes with a range of 30 to 270 minutes (IQR 75 120 minutes). Details of the primary excisional surgery carried out, mean revised American Fertility Society scores in each group, length of operation, and complication rates are shown in Table 2. Additional surgical procedures included excision of pelvic side wall endometriosis in 112 (63.3%) cases, treatment of endometriomas in 96 (54.2%) cases, partial- and full-thickness bladder wall excision in 26 (14.7%) and 4 (2.3%) cases, respectively, and oophorectomy in 3 (1.7%) cases. Fertility and Sterility â 41

TABLE 2 Type of primary excisional surgery, revised American Fertility Society scores, length of operation, and complication rates in each group. Procedure No. (%) (N [ 177) Median (range) revised American Fertility Society score Median (range) operation time (min) No. (%) of complications a (N [ 177) Uterosacral ligaments 43 (24.3) 10 (4 44) 63 (35 110) 0 Rectovaginal septum 56 (31.6) 16 (4 102) 84 (30 270) 3 (1.7) Total bowel surgery b 78 (44.1) 75 (3 150) 122 (45 240) 15 (8.5) Rectal shave 56 (31.6) 58 (3 150) 112 (45 240) 9 (5.1) Disk resection 7 (4.0) 81 (8 124) 112 (90 150) 1 (0.6) Segmental resection 15 (8.5) 100 (22 150) 164 (110 240) 5 (2.8) a Complication refers to the number of women with any complication. b Total bowel surgery contains rectal shave, disk resection, and segmental resection. The vagina was opened requiring laparoscopic or vaginal closure in 20 (11.3%) cases. A drain was placed in 36 (20.3%) cases, and a Mirena intrauterine system was inserted in 55 (31.1%) women. A covering ileostomy was required in two (1.1%) women who had a bowel resection. In the first case this was deemed necessary because of the proximity of the anastomosis to the anal margin. In the second case there was evidence of an anastomotic defect after an underwater air leak test. Histologic confirmation of endometriosis in the specimen removed was reported in 175 cases (98.9%). The median length of stay was 2 days (range 1 7, IQR 2 3 days). The more major the procedure, the longer the hospital stay (Table 3). The overall complication rate was 10.2% with a total of 24 complications developing in 18 women. More specifically, there were 13 cases of pyrexia, 2 cases of paralytic ileus, and 2 cases of pelvic collection. A wound infection developed in one woman, and one other had a postoperative hemorrhage that required blood transfusion. There were 2 (1.1%) cases of unintentional bladder injury, the first during insertion of the 5-mm suprapubic port and the second during excision of an endometriotic deposit from the right ureter near its insertion into the bladder. The injuries were recognized during the procedure and were repaired laparoscopically. No ureteric, unintentional bowel, or vessel injuries occurred. After surgery there were no cases of admission to intensive therapy unit, venous thromboembolism, anastomotic leak, or fistula formation. Two women returned to theater: In the first a staple line hemorrhage developed that was successfully controlled with a clip applied via a sigmoidoscope. The problem arose on the first postoperative day, and the woman required a blood transfusion. The second was readmitted on the sixth postoperative day with brown vaginal discharge and underwent surgical drainage of a pelvic collection. Two other women were readmitted after discharge. The first complained of significant pelvic pain that was found to be due to constipation. The second had a pelvic hematoma that was successfully managed conservatively. After surgery, one woman was treated for pyrexia with a wound infection, and paralytic ileus developed that resolved after conservative management. A further 12 (6.8%) women had pyrexia alone. Results of relevant septic screening were negative in all cases, and the symptom settled within TABLE 3 Hospital stay of women according to type of excisional surgery. Procedure 1 Day (n [ 27) 2 Days (n [ 98) 3 Days (n [ 38) 4 Days (n [ 4) 5 Days (n [ 7) 7 Days (n [ 3) Uterosacral ligament 16 22 5 0 0 0 Rectovaginal septum 10 39 7 0 0 0 Total bowel surgery a 1 37 26 4 7 3 Rectal shave 1 35 16 1 2 1 Disk resection 0 1 5 1 0 0 Segmental resection 0 1 5 2 5 2 a Total bowel surgery contains rectal shave, disk resection, and segmental resection. 42 Pandis et al. Laparoscopic excision of endometriosis Vol. 93, No. 1, January 2010

TABLE 4 Duration of catheterization of women according to type of excisional surgery. Excisional procedure Day 1 (n [ 90) Day 2 (n [ 71) Day 3 (n [ 9) Home with catheter (n [ 7) Uterosacral ligaments 35 6 2 0 Rectovaginal septum 37 17 0 2 Total bowel surgery a 18 48 7 5 Rectal shave 16 35 1 4 Disk resection 2 3 2 0 Segmental resection 0 10 4 1 a Total bowel surgery contains rectal shave, disk resection, and segmental resection. 48 hours with simple measures including hydration, antipyretics, and antibiotics where appropriate. Excluding these 12 cases of pyrexia gave a complication rate of 3.4%. All women had bladder scan residuals on removal of the catheter and, if the residual was >150 ml, had it reinserted. The length of time for bladder catheterization is shown in Table 4. Seven women were discharged home with an indwelling catheter. DISCUSSION This study has demonstrated that laparoscopic excision of deeply infiltrating pelvic endometriosis within a multidisciplinary setup in a tertiary referral center appears to be safe with a low rate of significant short-term complications. To our knowledge this is one of the largest sets of data presented to date on this subject, where procedures are designed and carried out jointly by members of a multidisciplinary team including gynecologic surgeons, colorectal surgeons, and urologists all trained in minimal access surgery and with a good understanding of endometriosis. It is of note that half of the total number of women treated surgically for endometriosis in our institution had deeply infiltrating pelvic endometriosis, which is a reflection of the high number of tertiary referrals from general practitioners and other gynecologists. In such clinical scenarios one would be keen to evaluate the impact of cases with high degree of surgical complexity in the complication rate. Not uncommonly in similar circumstances, these two parameters tend to demonstrate a direct correlation. Therefore, this large series provides an important insight into the role of a multidisciplinary approach in the laparoscopic excisional treatment of deep infiltrating endometriosis, and the outcomes described are relevant for clinicians working in this field, as well as general gynecologists. Our overall complication rate is higher compared with the one reported by Donnez et al. (16) and Donnez and Squifflet (28). In two series of 500 and 1,942 women undergoing laparoscopic excision of deep endometriosis, the authors reported complication rates of 2% and 1.4%, respectively. However, there were no cases of bowel surgery included in these data, which would suggest less extensive surgery. Results of four other studies with inclusion of laparoscopic bowel surgery as part of the overall treatment of endometriosis are in agreement with our reported complication rate (19, 29 31). Excision of deeply infiltrating pelvic endometriosis involving the intestine and the urinary tract is one of the most challenging and complex gynecologic procedures. Initially this surgery was performed via laparotomy (16, 32), but developments in technology and surgical skills have enabled a laparoscopic approach (15, 19, 29, 30). The requirement to remove all endometriotic tissue has been questioned, but there is now evidence to suggest that complete treatment results in improvement of pelvic pain, dysmenorrhea, digestive symptoms, quality of life, and fertility rates (14, 15, 20 24). That is why we exclusively perform excisional surgery. We use the harmonic scalpel, and our complication rate compares favorably with previously reported data on other surgical modalities (19, 29, 30). It is important to highlight the fact that, after excluding women with solely uncomplicated pyrexia, the complication rate was 3.4%. Deep pelvic dissection may predispose to postoperative bladder dysfunction, which can be an infrequent albeit serious complication (16, 19, 28). Retention with overdistention can result in long-term voiding problems (33). None of our patients had such voiding problems in the short term, probably because of careful postoperative assessment of bladder function preventing retention. Long-term data will be required to confirm that no deterioration has occurred. Although we are aware of the lack of robust evidence to support the use of preoperative GnRH-as in conjunction with surgical treatment to endometriosis (34), we favor the administration of such agents before performing surgery for known rectovaginal endometriosis. Available data suggest that preoperative use of GnRH-as may decrease the extent of endometriosis and result in a statistically significant reduction in implant American Fertility Society scores (35 37). It has been our impression that preoperative hormonal inhibition of ovulation reduces the bulk and vascularity of the affected tissues and that this may facilitate complete excision. Fertility and Sterility â 43

The European Society of Human Reproduction and Embryology has recommended the creation of tertiary referral centers for the treatment of endometriosis where appropriate clinical skills are available at the correct time in the most cost-effective way (38). The diagnostic unit at University College London Hospitals provides a high standard of pelvic ultrasound assessment. Combined with clinical assessment this enables careful planning for the operative surgical skills required, such as colorectal or urologic support. The diagnostic accuracy of transvaginal sonography for rectovaginal endometriosis has been shown previously (39). In our institution the deployment of such a system has allowed us to organize three different types of gynecologic surgical lists for the treatment of endometriosis: independent, routine lists where nongynecologic assistance is sought only in an emergency; high-risk lists where gynecologists and colorectal or urology surgeons operate on the same floor and are readily available should their assistance be necessary; and joint lists where the appropriate specialists operate together. The last group are reserved for women known to require significant bowel or urologic surgery. Almost one quarter of our cases were performed jointly, and >40% of women required some form of bowel surgery. Previous studies have shown that the number of significant short-term surgical complications increases as the number of cases with bowel surgery for endometriosis increases (19, 29 31). In a reported series of 192 women treated with laparoscopic excision of deep endometriosis and segmental colorectal resection, the overall complication rate was 36.4% with a median hospitalization of 9.4 days (31). In our series, in the group undergoing bowel surgery (including rectal shave, disk resection, and bowel resection) the overall complication rate was 19.2% with a median hospitalization of 3 days. It is possible that multidisciplinary approach has contributed to these low short-term complication rates. Additionally, in our experience, integrated operative teams do not appear to cause delays in the completion of complex surgical procedures. After an initial period of integration where surgeons of different specialties are tuned together by learning from each other and developing their laparoscopic skills further, our operative times are comparable with those presented by other teams (19, 31). 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