Fertility after bowel resection for endometriosis

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1 Fertility after bowel resection for endometriosis Simone Ferrero, M.D., a Paola Anserini, M.D., a Luiza Helena Abbamonte, M.D., a Nicola Ragni, M.D., a Giovanni Camerini, M.D., b and Valentino Remorgida, M.D. a a Department of Obstetrics and Gynaecology, San Martino Hospital and University of Genoa, Genoa, Italy; and b Department of Surgery, San Martino Hospital and University of Genoa, Genoa, Italy Objective: To determine the pregnancy rate after bowel resection for rectosigmoid endometriosis. Design: Prospective cohort study. Setting: University hospital. Patient(s): Forty-six symptomatic women with bowel endometriosis requiring colorectal resection. Intervention(s): Bowel resection by either laparoscopy or laparotomy. Main Outcome Measure(s): Pregnancy rate after surgery. Result(s): The pregnancy rate was higher in women who underwent bowel resection by laparoscopy (57.6%) than in those who underwent laparotomy (23.1%). No significant difference was observed in pregnancy rate and mode of conception between women with different fertility status before bowel resection. Women who conceived were significantly younger than those who did not conceive; only 26.7% of women aged R35 years conceived after bowel resection. Uterine adenomyosis was more frequently present in women who did not conceive than in those who conceived. Infertile women who conceived had a shorter length of infertility before surgery than those who did not conceive. Conclusion(s): Laparoscopic colorectal resection is less likely to impact negatively on fertility than the laparotomy approach. Previous laparotomies, age R35 years, uterine adenomyosis, and longer duration of infertility before surgery are associated with decreased pregnancy rate. (Fertil Steril Ò 2009;92:41 6. Ó2009 by American Society for Reproductive Medicine.) Key Words: Bowel endometriosis, bowel resection, endometriosis, infertility, laparoscopy, pregnancy outcome Bowel endometriosis affects between 3.8% and 37% of women with endometriosis (1). It may be associated with a wide range of symptoms, which vary according to the extension of the lesions. Small endometriotic nodules located on the serosal surface rarely cause symptoms (2); large nodules may cause pain and a wide range of gastrointestinal complaints, including diarrhea, constipation, abdominal bloating, and dyschezia (2, 3). Obstructive symptoms may be present in cases of extensive bowel lesions, which cause mural thickening and luminal stenosis. Surgery is required in patients with severe pain symptoms and subocclusion (1); depending on the extension of the lesions, nodulectomy (full thickness or partial thickness) or bowel resection may be performed. Women with bowel endometriosis, besides having gastrointestinal symptoms and pain, may be infertile. Therefore, surgeons must carefully weigh the effect of surgery and its potential complications on fertility against the benefit of the complete removal of bowel endometriotic lesions. Some investigators have suggested that in women for whom achieving or restoring fertility is initially more important than pain relief, a laparoscopic shaving of bowel lesions may be performed, with the understanding that a reoperation may be needed later Received March 15, 2008; revised April 24, 2008; accepted April 28, 2008; published online August 5, S.F. has nothing to disclose. P.A. has nothing to disclose. L.H.A. has nothing to disclose. N.R. has nothing to disclose. G.C. has nothing to disclose. V.R. has nothing to disclose. Reprint requests: Simone Ferrero, M.D., Department of Obstetrics and Gynecology, San Martino Hospital, University of Genoa, Largo R. Benzi 1, Genoa, Italy (FAX: ; dr@simoneferrero. com). for a complete excision of bowel endometriosis (4).However, limited data are currently available on fertility after colorectal bowel resection for endometriosis. In the 1990s pregnancy rates of up to 50% were reported after laparotomic resection of colorectal endometriosis; however, these studies were either retrospective (5) or did not specifically address fertility issues (6). In addition, in the last 15 years, assisted reproductive technologies have largely modified the treatment of infertility. More recently, in a retrospective study, Darai et al. (7) reported a 45.5% pregnancy rate among 22 women wishing to conceive after laparoscopic colorectal resection for bowel endometriosis. Interestingly, 75% of the pregnancies were obtained spontaneously; the median time to conceive after laparoscopic colorectal resection was 8 months, and all first pregnancies occurred in the first 13 postoperative months. This time to conception was lower than that reported in other studies after laparotomic colorectal resection (6), reflecting the potential advantages of laparoscopy (i.e., short recovery time, lesser risk of postoperative pelvic adhesions). The objective of the present prospective cohort study was to investigate the pregnancy rate in women who underwent rectosigmoid resection because of symptomatic bowel endometriosis. MATERIALS AND METHODS Study Population This prospective cohort study included all women who underwent rectosigmoid resection by either laparoscopy or laparotomy at our institution between May 1999 and May 2006 and subsequently tried to conceive. These patients underwent /09/$36.00 Fertility and Sterility â Vol. 92, No. 1, July doi: /j.fertnstert Copyright ª2009 American Society for Reproductive Medicine, Published by Elsevier Inc.

2 surgery because of pain symptoms and severe gastrointestinal complaints up to bowel subocclusion and occlusion; infertility was not a primary indication for surgery in this population. Three different groups of patients were included in the study: previously fertile women, women with previously unknown fertility status, and infertile patients. The groups were defined as follows. Previously fertile women spontaneously conceived and delivered before surgery; women who had termination of pregnancy, miscarriage, or extrauterine pregnancy before surgery were excluded from the study. Women with previously unknown fertility status did not try to conceive before surgery. Infertile patients tried to conceive for more than 1 year before surgery; these couples underwent full preoperative infertility evaluation (including ovulation studies, hysterosalpingography, and sperm analysis). Most of the patients received infertility treatment (IUI and/or IVF) before surgery. Women who had biochemical pregnancy before surgery were included in this group, whereas infertile women who had miscarriage or extrauterine pregnancy before surgery were excluded from the study. No woman who had previously delivered and subsequently unsuccessfully tried to conceive was included in the study. Subjects in the study did not have previous bowel surgery other than appendectomy. Some of the patients previously underwent surgical treatment for endometriosis (by either excision or ablation) in other hospitals; however, pain and gastrointestinal symptoms persisted or recurred after treatment, and they were referred to our hospital. Exclusion criteria for the study were age R40 years at the time of surgery, bilateral salpingo-oophorectomy, and egg donation cycles during follow-up. The investigation was performed in an academic department specializing in the management of endometriosis. The study was approved by the local institutional review board. All patients included in the study signed a written consent form; they gave consent for the use of their clinical data for research purposes and agreed to receive subsequent phone calls to ascertain follow-up. Preoperative Imaging Multislice CT enteroclysis was used for the preoperative diagnosis of bowel endometriosis; the effectiveness of this technique in determining the presence and depth of bowel endometriotic lesions has previously been reported (8, 9). The presence of uterine adenomyosis was determined at MRI and transvaginal ultrasonography (10). Surgical Technique No medical preoperative therapy was used. During laparoscopy all visible endometriotic lesions (apart from those located on the diaphragm) were excised. Bowel resections were not randomly performed by either laparoscopy or laparotomy; the choice of the surgical approach was based on the availability of a general surgeon who could perform the procedure by laparoscopy, and it was not based on the severity of endometriosis. Bowel resection was performed according to previously published criteria: single lesion R3 cm in diameter, single lesion infiltrating R50% of the bowel wall, and three or more lesions infiltrating the muscular layer (2, 11). Pararectal spaces were opened to obtain mobilization of the bowel. We removed the disease en bloc; no attempt was made to dissect the endometriotic nodule from the rectosigmoid. In cases of deep lateral preparation a nervesparing technique was used to avoid postoperative urinary complications (12). Separation of the fibrofatty tissue attached to the bowel was performed immediately adjacent to the bowel wall, where the vessels are smaller and easy to coagulate before transection. The mesentery was dissected no more than 2 cm past the nodular mass deforming the bowel wall, to maintain adequate blood supply to the edges of the anastomosis. In laparoscopic procedures the exposed bowel was transacted caudal to the endometriotic lesions using ENDO GIA (AutoSuture; Tyco Healthcare, Norwalk, CT). Complete laparoscopic mobilization of the rectum allowed extraction of its cephalic portion through a small suprapubic incision (3 5 cm), which was obtained by enlarging the midline trocar incision site. The affected bowel segment was resected after extra-abdominal inspection and palpation. A purse was created for the anvil before placing the colon in the pelvic cavity and closing the suprapubic abdominal incision. An end-to-end anastomosis was performed using rectally introduced CCEA forceps (AutoSuture, Tyco Healthcare) according to the Knight-Griffen technique (13). Histologic examination of bowel specimens removed at surgery was performed as previously described (2); the histologic criteria for diagnosing colorectal endometriosis included the presence of ectopic glands and stroma penetrating through the bowel wall. Fertility Follow-Up After Surgery Fertility status was investigated at follow-up consultations at our hospital (every 6 months). Women who were referred to our hospital from other regions were interviewed on the telephone at 6-months intervals by the same investigator who invited the patients to participate to the study. After surgery, women were invited to immediately inform the endometriosis center in case of positive pregnancy test results. A standardized questionnaire was used to record clinical information (including starting date of attempt to conceive, infertility treatments, and pregnancy outcome); a copy of this questionnaire was administered to the patients when they were discharged from the hospital. Statistical Analysis Continuous variables were compared by analysis of variance; categoric variables were compared with the c 2 test or Fisher s exact test as appropriate. Analyses were performed using the Statistical Package for the Social Sciences, version 13.0 (SPSS, Chicago, IL) and the Sigma-Stat 3.5 software package (SPSS). A P value of <.05 was considered statistically significant. 42 Ferrero et al. Fertility after bowel resection Vol. 92, No. 1, July 2009

3 RESULTS Characteristics of the Study Population Forty-six women were included in the study; 33 bowel resections were performed by laparoscopy and 13 by laparotomy. Patients included in the study had the following indications for surgery: dysmenorrhea (n ¼ 42, 91.3%), dyspareunia (n ¼ 35, 76.1%), chronic pelvic pain (n ¼ 39, 84.8%), diarrhea during the menstrual period (n ¼ 15, 32.6%), persistent diarrhea (n ¼ 2, 4.3%), constipation during the menstrual period (n ¼ 8, 17.4%), persistent constipation (n ¼ 7, 15.2%), diarrhea alternating with constipation (n ¼ 11, 23.9%), bowel movement pain or cramping (n ¼ 26, 56.5%), dyschezia (n ¼ 15, 32.6%), painful tenesmus (n ¼ 9, 19.6%), rectal bleeding (n ¼ 6, 13.0%), and nausea and vomiting (n ¼ 3; 6.5%). There were nine major complications and eight minor complications (Table 1); there was no significant difference in the prevalence of major complications between patients who underwent laparoscopy or laparotomy (P¼.229). Follow-up was available for all patients; the mean (SD) length of follow-up was months. Table 2 shows the characteristics of the study population according to preoperative fertility status. Live Birth Rate According to Preoperative Fertility Status Five previously fertile women were included in the study; the mean time between delivery and surgery at our hospital was months. Three of these women (60%) conceived and delivered during follow-up. Twenty women with unknown fertility status before surgery were included in the study; 50.0% of them (n ¼ 10) conceived at least once during the follow-up. One of these patients conceived and delivered twice; another woman had a miscarriage 7 months after the first delivery. Among these patients, 1 had a miscarriage. Another woman had an extrauterine pregnancy after intracytoplasmic sperm injection; she underwent laparoscopic salpingectomy and, to date, has not conceived again. Twenty-one infertile patients underwent bowel resection; the median duration of infertility before surgery was 25 months (range, months). Three women had a male partner with severe dyspermia (< sperm/ml, <30% progressive motility, and <30% typical forms). Of the infertile women, 85.7% underwent some infertility treatment (IUI or IVF) before surgery; 15 women underwent IUI (median number of previous IUI cycles, 3; range, 1 4), and 7 underwent IVF (median number of previous IVF cycles, 2; range, 1 3). After bowel resection, the pregnancy rate in this study group was 42.9%; the majority of patients conceived by IUI or IVF (Table 2). Two women had miscarriages; 1 of them subsequently conceived by IUI and delivered. No significant difference was observed in pregnancy rate and mode of conception (spontaneous, IUI, IVF) between women with different fertility status before bowel resection (Table 2). Live Birth Rate According to Patient Characteristics The majority of patients underwent bowel resection by laparoscopy (71.7%). The pregnancy rate was significantly higher in women who underwent bowel resection by laparoscopy (57.6%; 95% confidence interval [CI] 39.2% 74.5%) than in those who underwent laparotomy (23.1%; 95% CI 5.0% 53.8%; P¼.035). The pregnancy rate was significantly higher in women who had no previous surgery for endometriosis (10 of 17; 58.8%; 95% CI 32.9% 81.6%) than in those who had a previous laparotomy for treatment of pelvic endometriosis (2 of 13; 15.4%; 95% CI 1.9% 45.4%; P¼.016); no significant difference was observed in pregnancy rate between women who had no previous surgery for endometriosis and those who had a previous laparoscopic treatment of pelvic endometriosis (10 of 16; 62.5%; 95% CI 35.4% 84.8%; P¼.829). TABLE 1 Minor and major complications in 46 women who underwent bowel resection by either laparoscopy or laparotomy. Complication Laparoscopy (n [ 33) Laparotomy (n [ 13) Major complications Pelvic abscess 0 1 (7.7) Rectovaginal fistula 0 1 (7.7) Temporary ileostomy at the time of surgery 1 (3.0) 0 Anastomotic leakage requiring temporary ileostomy 1 (3.0) 0 Heterologous blood transfusion 3 (9.1) 2 (7.7) Minor complications Mild rectal stricture requiring dilatation 2 (6.1) 1 (7.7) Urinary retention after 30 d from surgery 2 (6.1) 0 Peripheral sensory disturbances after 30 d from surgery 2 (6.1) 0 Wound infection 0 1 (7.7) Note: Values are number (percentage). Fertility and Sterility â 43

4 TABLE 2 Characteristics of the study population. Characteristic Previously fertile women Women with previously unknown fertility status Infertile women P value Total n Age (y) Previous surgery for 3 (60.0) 13 (65.0) 13 (57.1) (63.0) endometriosis (n, %) Previous surgical procedures 1 (1 3) 1 (1 4) 1 (1 3) (1 4) Previous surgery by laparotomy 1 (20.0) 6 (30.0) 6 (28.6) (28.3) Type of surgical procedure.905 Laparoscopy 4 (80.0) 14 (70.0) 15 (71.4) 33 (71.7) Laparotomy 1 (20.0) 6 (30.0) 6 (28.6) 13 (28.3) Pregnancy rate 3 (60.0) 10 (50.0) 9 (42.9) (47.8) Pregnancy rate according to the type of surgical procedure Laparoscopy 3 (75.0) 8 (57.1) 8 (53.3) (57.6) Laparotomy 0 2 (33.3) 1 (16.7) (23.1) Live birth rate 3 (60.0) 8 (40) 8 (38.1).662 Live birth rate according to the type of surgical procedure Laparoscopy 3 (75.0) 7 (50.0) 7 (46.7) (51.5) Laparotomy 0 1 (16.7) 1 (16.7) (15.4) Mode of conception a.511 Spontaneous 1 (20.0) 6 (30.0) 2 (9.5) 9 (19.6) IUI 1 (20.0) 1 (5.0) 3 (14.3) 5 (10.7) IVF/intracytoplasmic 1 (20.0) 3 (40.0) 4 (19.0) 8 (17.4) sperm injection Time between attempt to conceive after surgery and conception (mo) a Note: Values are number (percentage), mean SD, or median (range). a Only the first conception was considered. Time Between Bowel Resection and Conception The median time between the attempt to conceive and conception was 12.5 months (range, 6 46 months). There was no significant difference in the time between attempt to conceive after surgery and conception among the three study groups (P¼.380). There was a trend for time between attempt to conceive after surgery and conception to be less in women who underwent laparoscopic bowel resection (n ¼ 19; months) when compared with those who underwent laparotomic bowel resection (n ¼ 3; months), but the difference was not statistically significant (P¼.067) (Figure 1). Comparison of Women Who Conceived and Did Not Conceive After Bowel Resection Table 3 shows a comparison of the characteristics of women who conceived and did not conceive after bowel resection. Uterine adenomyosis was significantly less frequent among women who conceived than in those who did not conceive after surgery. Only 4 women (23.5%) aged R35 years conceived after bowel resection; 3 of them conceived through IVF and 1 through IUI. The pregnancy rate was significantly higher in women aged <35 years at the time of surgery (18 of 29) than in those aged R35 years (4 of 17; P¼.012). Among infertile women included in the study, those who conceived after surgery (n ¼ 9) had a shorter duration of infertility than those who did not conceive (n ¼ 12; P¼.035). DISCUSSION To the best of our knowledge this is the first prospective study designed to evaluate the pregnancy rate after bowel resection for rectosigmoid endometriosis. We observed a significantly higher pregnancy rate after laparoscopic colorectal resection (57.6%) than after laparotomic procedures (23.1%). Previous 44 Ferrero et al. Fertility after bowel resection Vol. 92, No. 1, July 2009

5 TABLE 3 Comparison of women who conceived and did not conceive after bowel resection. Characteristic Women who conceived (n [ 22) Women who did not conceive (n [ 24) P value Age (y) Fertility status before surgery.762 Fertile 3 (13.6) 2 (8.3) Unknown 10 (45.5) 10 (41.7) Infertile 9 (40.9) 12 (50.0) Duration of infertility before surgery (mo) a Bilateral tubal occlusion 1 (4.5) 2 (8.3).533 Ovarian endometrioma 11 (50.0) 14 (58.3).571 Uterine adenomyosis 1 (4.5) 7 (29.2).032 Length of the resected bowel segment (cm) Male factor infertility 2 (9.1) 1 (4.2).467 Note: Values are mean SD or number (percentage). a For infertile women. investigators reported pregnancy rates ranging between 34% and 53.3% after laparoscopic colorectal resection (4, 7, 14, 15) and pregnancy rates ranging between 23.5% and 39.4% after laparotomic colorectal resection (6, 16). It remains unclear why the pregnancy rate was significantly decreased after laparotomic procedures. Studies performed in patients with uterine myomas did not demonstrate a detrimental effect of laparotomy on pregnancy rate (17). It is possible that laparotomic rectosigmoid resection is associated with more postoperative adhesions in the pelvic cavity than other procedures. Unfortunately, presence and severity of adhesions after laparoscopy or laparotomy were not evaluated; therefore, this study cannot determine whether differences in fertility outcomes may be explained by adhesion formation. In addition, laparotomy may theoretically determine greater traumatism to the peritoneum when compared with laparoscopic surgery. FIGURE 1 Cumulative pregnancy rate in women who underwent laparoscopic and laparotomic bowel resection. Finally, the magnification of the view at laparoscopy may allow better hemostasis and cleaning of the pelvic cavity at the end of the procedure, thus reducing the risk of adhesions. In a previous study including patients who underwent laparoscopic colorectal resection, Darai et al. (7) reported that 75% of the pregnancies were conceived spontaneously and that the median time to conceive was 8 months (range, 3 13 months). In our study only 41% of the pregnancies were spontaneous, and the median time for spontaneous conception was 13 months (range, 6 46 months). Obviously various factors may affect spontaneous fertility (including age of the woman, presence of male factor infertility, and attitude of the couple toward spontaneous conception and infertility treatments). In addition, we cannot exclude that our patients were referred to infertility treatments earlier than in other centers, thus reducing the theoretical possibility of spontaneous conception. However, the median time for spontaneous conception in our series was higher than that reported by Darai et al. (7), suggesting that spontaneous pregnancy is not an easy event in women who underwent extensive surgery for pelvic and bowel endometriosis. Importantly, no spontaneous conception occurred in women aged R35 years at the time of surgery; only 23.5% of the patients aged R35 years conceived either by IUI (in 1 case) or IVF (in 3 cases). On the basis of these observations, we believe that women near 35 years of age at the time of colorectal resection may be advised to immediately undergo IVF when wishing to conceive. Among patients with uterine adenomyosis, only 1 woman (12.5%) conceived and delivered after surgery. Although adenomyosis has traditionally been associated with multiparity (18) and not with infertility, in recent years some studies suggested a detrimental effect of uterine adenomyosis on conception in both humans (7) and animal models (19). In case Fertility and Sterility â 45

6 of focal adenomyosis, conservative surgical excision of the nodules may be performed (20). However, the laparoscopic removal of focal adenomyosis and the reconstruction of the myometrium may be challenging even for expert laparoscopic surgeons. In our clinical practice we do not usually remove uterine adenomyosis at the time of bowel resection; this choice is justified by the fact that preoperatively it is difficult to determine how severely adenomyosis contributes to pain symptoms reported by patients with bowel and pelvic endometriosis. Future studies should determine whether the excision of focal adenomyosis may increase pregnancy rates in infertile women. The finding of the present study cannot be generalized to all women with bowel endometriosis. Subjects of the study were highly symptomatic, surgery was judged to be required on the basis of pain and gastrointestinal symptoms, and bowel resection was performed because of the extension of bowel endometriotic lesions. Obviously other patients with bowel endometriosis may complain of less-severe symptoms, and it remains unclear whether surgery should be postponed until these patients have tried to conceive either spontaneously or by IVF. However, 21 infertile women were included in the study. Although most of them had undergone unsuccessful IUI (71.4%) or IVF (38.1%) before surgery, the postoperative pregnancy rate in this group was 42.9%. We are aware that these data does to not provide enough evidence to propose the excision of pelvic and bowel endometriosis to infertile women. However, our results seem to confirm that, in symptomatic patients, complete laparoscopic excision of pelvic and bowel endometriosis can be accomplished with no detrimental effect on fertility. One of the limitations of this study is that patients were not randomized to undergo laparoscopic or laparotomic bowel resection. However, the choice between laparoscopy and laparotomy was based on the availability of a general surgeon who could perform the procedure by laparoscopy and not on the clinical characteristics of the patients or on the severity of endometriosis. Another potential limitation of this study is the small number of patients included. Although this investigation was performed in a referral center for the surgical treatment of endometriosis, symptomatic bowel endometriosis requiring colorectal resection is a rare condition, and it is difficult to perform prospective, randomized trials. A further limitation of this investigation is that the study subjects were heterogeneous in the preoperative fertility status; therefore our study design does not allow drawing definitive conclusions on the management of fertility in women who undergo colorectal resection. In conclusion, results of the present study suggest that in women with bowel endometriosis, laparoscopic colorectal resection is less likely to impact negatively on fertility than the laparotomic approach. Although spontaneous conception may occur, these patients may require infertility treatment, particularly when aged R35 years at the time of surgery. Definitive conclusions on fertility after surgery for bowel endometriosis cannot be draw from this study owing to its limitations (i.e., small sample size, heterogeneous population, nonrandomized design). Larger, multicenter, prospective trials are required to confirm our observations. In addition, future studies should investigate whether complete excision of endometriosis, including bowel nodules, should be performed in infertile women without severe pain and extensive gastrointestinal symptoms. REFERENCES 1. Remorgida V, Ferrero S, Fulcheri E, Ragni N, Martin DC. Bowel endometriosis: presentation, diagnosis, and treatment. 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