Fertility after laparoscopic colorectal resection for endometriosis: preliminary results

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1 REPRODUCTIVE SURGERY Fertility after laparoscopic colorectal resection for endometriosis: preliminary results Emile Daraï, M.D., Ph.D., a Olivier Marpeau, M.D., a Isabelle Thomassin, M.D., b Gil Dubernard, M.D., a Emmanuel Barranger, M.D., a and Marc Bazot, M.D. b a Services de Gynécologie and b Radiologie, Hôpital Tenon, AP-HP, Paris, France Objective: To examine fertility, reproductive outcomes, and determinants of fertility after laparoscopic segmental colorectal resection for endometriosis. Design: Retrospective longitudinal study. Setting: Tertiary university gynecology unit. Patient(s): The study population consisted of 34 women with colorectal endometriosis, of whom 22 wished to conceive. Demographic, surgical, and histological characteristics of 10 women who conceived were compared with those of 12 women who failed to conceive. Intervention(s): Laparoscopic colorectal resection for endometriosis. Main Outcome Measure(s): Rates of pregnancy and live birth. Result(s): Mean follow-up after segmental colorectal resection was 24 months (range 6 42 months), and the pregnancy rate was 45.5%. The median time to conceive was 8 months (range 3 13 months). Twelve pregnancies occurred in 10 women, comprising nine spontaneous singleton pregnancies (7 vaginal deliveries, 1 cesarean section, and 1 ongoing pregnancy), and three pregnancies obtained by IVF (one miscarriage, one ongoing twin pregnancy, and one triplet pregnancy necessitating cesarean section at 29 weeks for premature rupture of the membranes, with two surviving infants). The live birth rate was 82%. The women who did and did not conceive did not differ in terms of mean follow-up, mean age, body mass index (BMI), parity, smoking, use and duration of oral contraception (OC), duration of infertility, or the length of the resected colorectal segment. Uterine adenomyosis was the main determinant of pregnancy after colorectal resection. Conclusion(s): These preliminary results suggest that extensive laparoscopic segmental colorectal resection for endometriosis can enhance fertility, with high rates of spontaneous pregnancy and live birth. (Fertil Steril 2005; 84: by American Society for Reproductive Medicine.) Key Words: Colorectal endometriosis, laparoscopy, fertility, pregnancy Endometriosis is a well-known gynecological disorder affecting young women and potentially causing chronic pelvic pain and infertility (1). Endometriosis affects approximately 5% 15% of women of reproductive age (2), and up to 40% of infertile women (3). The cause effect relationship between endometriosis and infertility is controversial (3, 4). Infertility could be explained by functional alterations of the peritoneal environment affecting gamete, embryo, or fallopian tube function or by anatomical abnormalities of genital organs (2, 5, 6). Few data are available on fertility after extensive surgery for deep pelvic endometriosis, and particularly after colorectal resection (5, 7 10). Previous studies suggest that complete removal of deep pelvic endometriosis improves quality Received January 13, 2005; revised and accepted April 11, Reprint requests: Emile Daraï, M.D., Ph.D., Service de Gynécologie Obstétrique, Hôpital Tenon, 4 rue de la Chine, Paris, France (FAX: ; emile.darai@tnn.ap-hop-paris.fr). of life and potentially fertility, despite a high risk of postoperative adhesions (10 15). Pregnancy rates (PR) of up to 50% have been reported after laparotomic resection of colorectal endometriosis (11, 16, 17). Laparoscopic colorectal resection for endometriosis was recently shown to be feasible (9, 10, 18 24), and to offer a significant improvement in both symptoms and quality of life. Few data are available on the impact of laparoscopic colorectal resection on fertility in this setting. The aim of this study was to evaluate fertility and pregnancy outcomes in women undergoing laparoscopic colorectal resection for endometriosis. MATERIALS AND METHODS Between March 2001 and March 2004, 56 women with colorectal endometriosis were referred to the gynecology department of Tenon Hospital, Paris. Before surgery, colorectal endometriosis and associated lesions (including endo /05/$30.00 Fertility and Sterility Vol. 84, No. 4, October 2005 doi: /j.fertnstert Copyright 2005 American Society for Reproductive Medicine, Published by Elsevier Inc. 945

2 metriomas and uterine adenomyosis) were assessed by transvaginal sonography, magnetic resonance imaging (MRI), and rectal endoscopic sonography, based on published criteria (24 26). No Institutional Review Board approval was required for this retrospective study. To avoid a possible bias linked to the type of surgery, only women undergoing laparoscopic segmental colorectal resection were included in the study. Women undergoing superficial or full-thickness rectal resection (n 6), a first laparotomy (n 4), radical surgery including hysterectomy or bilateral salpingo-oophororectomy (n 6), and women older than 43 years (n 2) were excluded from the study. The study population consisted of 38 women. All the women completed symptom questionnaires on gynecological (dysmenorrhea, nonmenstrual pelvic pain, dyspareunia), digestive (pain on defecation) and nonspecific disorders (asthenia). Before and after surgery the women also completed an interview-based symptom questionnaire (10-point analogue rating scale; 0 absent, 10 unbearable) (22, 23). All the patients received GnRh analogues for 3 months before surgery. In brief, the laparoscopic procedure was performed in the modified dorsolithotomy position under endotracheal general anesthesia. Prophylactic anticoagulant therapy (low molecular weight heparin) was given the evening before the operation, and prophylactic antibiotic therapy (cefazolin, 2 g IV) was given at the beginning of the operation. After pneumoperitoneum induction, three suprapubic trocars (12-mm trocar in the right iliac fossa, 15-mm trocar in the median suprapubic area, 5-mm trocar in the left iliac fossa) were introduced for ancillary instrumentation (Karl Stortz, Tuttlingen, Germany). After exploration of the pelvic cavity to evaluate the extent of endometriotic lesions, and after adhesiolysis or ovarian cystectomy if required, the colorectum was released. All endometriotic lesions, including those affecting the uterosacral ligaments, the torus uterinus, the peritoneum of the pouch of Douglas, and the colorectum were mobilized before sectioning the colorectum with an endo GIA 45 (Auto Suture, Tyco S.A., Elancourt, France). After withdrawing the median suprapubic trocar, the incision was enlarged to 3 cm to allow the colorectum to be exteriorized and resected before creating a purse for the anvil using Purstring 45 (Auto Suture, Tyco S.A.). The colon was placed in the pelvic cavity before closing the suprapubic abdominal incision. An end-to-end colorectal anastomosis was constructed using rectally introduced CCEA forceps (Auto Suture, Tyco S.A.). Histological criteria for colorectal endometriosis included the presence of ectopic endometrial glands and stromal tissue penetrating through the bowel wall. The largest diameter of the lesions was measured on the colorectal specimen. All the women had at least 6 months of postsurgical follow-up. Information on the desire to conceive after surgery, together with intercurrent events such as separation, attempts at medically assisted procreation, and outcome of pregnancies were obtained by chart review and were updated by face-to-face or telephone interviews. Infertility was defined by the absence of pregnancy for at least 24 months (World Health Organization criteria). All infertile women had preoperative infertility evaluation including ovulation studies, postcoital testing, sonographic examination, hysterosalpingography, and diagnostic hysteroscopy. Sperm characteristics of the partner were also evaluated. Parametric and nonparametric continuous variables were compared with Student s t test and the Mann-Whitney test, and categorical variables were compared with the 2 test or Fisher s exact test, as appropriate. P values.05 were considered statistically significant. RESULTS Thirty-four of the 38 women (89.5%) of the study underwent a laparoscopic colorectal resection, whereas 4 women required a conversion to laparotomy. All 38 women who underwent colorectal resection had a significant improvement in dysmenorrhea (P.0001), nonmenstrual pelvic pain (P.0001), dyspareunia (P.0001), and pain on defecation (P.001). No improvement in asthenia was observed. Sixteen women (42%) had no desire to conceive and 22 women (58%) wished to conceive. Demographic data and symptom scores before and after surgery are given in Table 1 for the 38 women. The women who wished to conceive were slightly but not significantly younger, whereas the women who did not wish to conceive tended to have lower postoperative dyspareunia scores. No difference in preoperative or postoperative scores for dysmenorrhea, nonmenstrual pelvic pain, pain on defecation, or asthenia were found between women who did and did not wish to conceive. Transvaginal sonography and magnetic resonance imaging (MRI) showed that 4 (18%) of the 22 women who wished to conceive had uterine adenomyosis and that 7 (32%) had endometriomas. In addition to segmental colorectal resection, seven women underwent ovarian cystectomy for endometrioma (unilateral in 3, bilateral in 4) and eight women underwent adnexal adhesiolysis with fallopian tube surgery (unilateral in 4, bilateral in 4). Two (9%) of these 22 women experienced major postoperative complications, comprising a rectovaginal fistula requiring further laparotomic surgery in one case, and a pelvic abscess managed by laparoscopic drainage in the other case. Histological examination of the surgical specimens confirmed colorectal endometriosis in all 22 women. The median length of the resected colorectal segment was 6.7 cm (range 4 18 cm). The median histological length of the lesions was 2.5 cm (range 1 5 cm). Mean follow-up after segmental colorectal resection was 24 months (range 6 42 months). Ten (45.5%) of the Daraï et al. Fertility after colorectal resection for endometriosis Vol. 84, No. 4, October 2005

3 TABLE 1 Demographic characteristics and symptom scores before and after surgery in 34 women who underwent laparoscopic colorectal resection for endometriosis. Characteristics Women wishing to conceive (n 22) Median value (range) Women not wishing to conceive (n 16) Median value (range) P value Age (y) 31 (29 42) 36 (26 43).07 Gravidity 0 (0 3) 0 (0 4) NS Parity 0 (0 2) 0 (0 3) NS Dysmenorrhea Preoperative score 8.5 (6 10) 9 (4 10) NS Postoperative score 0 (0 8) 0 (0 5) NS Nonmenstrual pelvic pain Preoperative score 7.5 (0 10) 9 (8 10) NS Postoperative score 0 (0 8) 1 (0 5) NS Dyspareunia Preoperative score 6.5 (0 10) 7 (2 10) NS Postoperative score 0 (0 10) 0 (0 8).08 Pain on defecation Preoperative score 7.5 (0 10) 8 (0 10) NS Postoperative score 0 (0 7) 0 (0 8) NS Asthenia Preoperative score 2 (0 3) 2 (0 3) NS Postoperative score 1 (0 3) 1 (0 3) NS Daraï. Fertility after colorectal resection for endometriosis. Fertil Steril patients conceived during this period, two women conceiving twice. Five of the 12 infertile women (42%) conceived after colorectal resection. Nine pregnancies (75%) were spontaneous and three were obtained by IVF indicated for fallopian tube disorders. The median time required to conceive after colorectal resection was 8 months (range 3 13 months). The pregnancy outcomes are shown in Table 2. All three women who underwent IVF for fallopian tube disorders conceived after the first IVF cycle. One of these three women miscarried at 8 weeks. Premature rupture of the membranes occurred at 29 weeks in a woman with a triplet pregnancy requiring cesarean section (two infants are alive, and one died at 1 month of life). The third woman had an ongoing twin pregnancy (26 weeks). Among the remaining seven women, who conceived spontaneously, five women had seven term vaginal deliveries, one had an elective cesarean section indicated for previous cesarean section related to unicorn uterus, and one had an ongoing pregnancy (29 weeks) after drainage of a pelvic abscess. The overall live birth rate was 82% (9/11). No ectopic pregnancies occurred. Before laparoscopic colorectal resection, 6 of the 12 infertile women had undergone unsuccessful infertility treatment. Five of these six women underwent IVF (6 attempts in 1 case, 5 attempts in 1 case, 3 attempts in 2 cases, and 1 attempt in 1 case), and the last woman underwent two courses of ovarian stimulation with intrauterine insemination. TABLE 2 Fertility and reproductive outcomes after laparoscopic colorectal resection for endometriosis. Characteristics Data Median interval between surgery 8 (3 13) and first pregnancy (mo) Number of women who conceived 10 Number of pregnancies 12 Spontaneous 9 (75%) After IVF 3 (25%) Ectopic pregnancies 0 Miscarriage 1 (8.5%) Preterm delivery 1 (8.5%) Ongoing pregnancy 2 (17%) Term delivery 8 (66%) Vaginal delivery 7 Cesarean section 1 Daraï. Fertility after colorectal resection for endometriosis. Fertil Steril Fertility and Sterility 947

4 TABLE 3 Determinants of fertility after laparoscopic colorectal resection for endometriosis. Determinant Women who conceived (n 10) Women who did not conceive (n 12) P value Age (y) (median; range) 31 (29 35) 31 (30 42) NS Body mass index (kg/m 2 ) (median, range) 21 (18 25) 23 (18 30) NS Follow-up (mo) (median, range) 26 (21 42) 22 (6 39) NS Current smokers 3/10 5/12 NS History of oral contraception (y) (median, range) 7 (2 12) 5 (1 8) NS Prior infertility 5/10 7/12 NS Duration of prior infertility (mo; median, range) 24 (6 72) 42 (24 120) NS Associated factors of infertility (male infertility; 1/10 3/12 NS hormone dysfunction) Previous surgery for endometriosis 7/10 6/12 NS Length of resected colorectal segment (cm) 7 (6 18) 6.5 (4 14) NS (median, range) Histological length of bowel endometriosis (cm) 2.5 (1 5) 3.5 (1.5 7) NS (median, range) Fallopian tube surgery 3/10 5/12 NS Cystectomy for endometrioma 3/10 4/12 NS Uterine adenomyosis 0/10 4/12.03 Daraï. Fertility after colorectal resection for endometriosis. Fertil Steril After laparoscopic colorectal resection, 2 of the 12 infertile women, who had undergone six and three unsuccessful IVF attempts, conceived spontaneously. The woman who had undergone five unsuccessful IVF attempts before surgery became pregnant after the first postoperative IVF (triplet pregnancy). The other three women had no further fertility treatment after surgery and none of them became pregnant. Factors potentially influencing fertility after colorectal resection in the groups of women who conceived and those who did not conceive are shown in Table 3. Although the mean age of the women who conceived and those who did not conceive did not differ significantly, it is noteworthy that all pregnancies occurred in women younger than 35 years. No difference in the body mass index (BMI), mean followup, prior history of infertility, prior surgery for endometriosis, histological findings, or procedures associated with colorectal resection was found between the women who did and did not conceive. The only factor negatively influencing fertility was uterine adenomyosis. DISCUSSION The indications of colorectal resection for endometriosis are controversial, particularly in young women who wish to preserve their child-bearing potential. Previous studies have shown that aggressive surgery for deep pelvic endometriosis offers good symptom relief and a significant improvement in quality of life, but few data are available on subsequent fertility (8, 10, 27, 28). In the present study, 10 (45.5%) of the 22 women who wished to conceive became pregnant. This PR is in keeping with that reported after laparotomic colorectal resection for endometriosis (39.4% 52%) (11, 17). Redwine and Wright (10) reported a fertility rate of 43% after en bloc resection of complete obliteration of the pouch of Douglas related to endometriosis. After laparoscopic segmental colorectal resection, Jerby et al. (20) reported three pregnancies among seven women wishing to conceive. Likewise, Possover et al. (21) reported eight pregnancies among 15 nulliparous women with a history of infertility. However, these investigators did not report the spontaneous/assisted nature or outcome of the pregnancies. In our series, 9 (75%) of the 12 pregnancies were spontaneous and the other three were obtained by IVF. In this study the median time to conceive after laparoscopic colorectal resection was 8 months, and all first pregnancies (two women conceived twice) occurred in the first 13 postoperative months. Coronado et al. (11) reported PRs of 34% at 18 months and 52% at 29 months after laparotomic colorectal resection. The short times to conception in our study could reflect potential advantages of laparoscopy, such as a short recovery time and a lesser risk of postoperative pelvic adhesions, but could also be linked to the epidemiological characteristics of the study population. Further prospective studies are required to settle this issue. However, a previous study (29) showed that the mean time to conceive after myomectomy was shorter after exclusive laparoscopy than after laparoconversion. 948 Daraï et al. Fertility after colorectal resection for endometriosis Vol. 84, No. 4, October 2005

5 The live birth rate in our study was 82%. Very few data are available on pregnancy outcome after laparoscopic colorectal resection. In the series published by Redwine and Wright (10), which involved women undergoing en bloc laparoscopic resection of the pouch of Douglas for endometriosis, the live birth rate was only 41.6%, with four miscarriages and one ectopic pregnancy. Determinants of fertility after laparoscopic colorectal resection for endometriosis are mainly related to the patients characteristics. In keeping with previous studies of fertility after fibroid surgery (30, 31), age was the main prognostic factors. All of the pregnancies observed in our study occurred in women who were younger than 35 years. This implies that immediate IVF might be indicated for women older than 35 years after colorectal resection of endometriosis. The presence of uterine adenomyosis seemed to have a negative impact on the PR. In contrast to peritoneal endometriosis (2 6), little is known of the relation between fertility and adenomyosis. Our data are in keeping with those of an experimental study (32) showing reduced infertility in baboons with adenomyosis. One dilemma facing women with deep pelvic endometriosis, and particularly those with bowel involvement, is whether to opt for IVF or extensive surgery first. Although ovarian stimulation for IVF may have a negative impact on endometriotic lesions, it is well known that pregnancy has a positive effect on endometriotic symptoms (33). The first randomized trial comparing surgical removal of deep pelvic endometriosis to wait-and-see management (34) recently showed an advantage of the surgical strategy. Fedele et al. (33) have reported that risk factors for clinical recurrence and second operations after surgery for endometriosis are young age and incomplete removal of deep pelvic endometriosis, particularly forms involving the bowel. Our reproductive outcomes after laparoscopic colorectal resection for endometriosis support the view that complete surgical removal can enhance fertility. Three women with a history of unsuccessful IVF became pregnant spontaneously after surgery, underlining the key role of the peritoneal environment in fertility. Both gynecological and digestive symptoms improved after laparoscopic colorectal resection of endometriosis, in keeping with previous reports of laparotomic (11, 17) or laparoscopic removal of colorectal endometriosis (19 24). However, this surgical strategy can be associated with severe postoperative complications that may affect negatively subsequent fertility. In our series, two women wishing to become pregnant developed complications, consisting of a rectovaginal fistula requiring further laparotomy, and a pelvic abscess managed by laparoscopic drainage. Duepree et al. (22) showed that the risk of postoperative complications depended on type of bowel surgery, with rates of 3.8% and 11.1%, respectively, after superficial and segmental resection. It is noteworthy that our study only involved women undergoing segmental resection. Our complication rate is in keeping with that reported by Jerby et al. (20), who observed rectovaginal fistulae in one of seven women undergoing segmental colorectal resection. Possover et al. (21) observed two anastomotic dehiscences in a series of 30 women undergoing colorectal resection by the combined laparoscopic and vaginal routes. In conclusion, these preliminary results on conception and live birth rates after laparoscopic segmental colorectal resection for endometriosis tend to confirm that extensive surgery can enhance fertility. Further prospective trials are required to identify determinants of infertility and the patient population most likely to benefit from this major surgery. REFERENCES 1. 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