Safety and long-term impacts on quality of life of segmental bowel resection for bowel endometriosis: a single-centred 5-year follow-up

Purpose: To evaluate the long-term efficacy of segmental bowel resection for bowel endometriosis and the impact of post-operative complications on clinical outcomes. Methods: 62 symptomatic patients with bowel endometriosis undergoing segmental bowel resection from Jun. 2010 to Jan. 2014 were recruited. A visual analogue scale (VAS) and SF-36 questionnaire were administered before and at least 5 years after surgery. Postoperative complications and pregnancy were also recorded. Median follow-up after operation was 76 months (62-105 months). Results: 62 patients underwent laparoscopic segmental bowel resection, one of which converted to laparotomy. All patients complained of obvious pain symptoms, including dysmenorrhea, dyspareunia, bowel movement pain, chronic pelvic pain and tenesmus. Dysmenorrhea was the most frequent. The relief of all pain symptoms after surgery was statistically significant (P<0.001). The scores for 8 domains of SF-36 questionnaire were significant improved after operation (P<0.001), and the post-operative scores were improved to the level of Chinese female population. Post-operative complication included 18 cases of urinary retention, 4 rectovaginal fistulas, 2 cases of vaginal dehiscence, and 1 case each of thrombogenesis, diffuse peritonitis, peripheral nerve injury, bacteraemia, incomplete intestinal obstruction and mucus bloody stool. All of these patients recovered well. There was no significant difference in post-operative SF-36 questionnaire scores between the patients with and without complications. Conclusion: Segmental bowel resection can significantly relieve pain and improve long-term quality of life for patients with bowel endometriosis. Despite the relatively high complication rate, the complications had little impact on the improvement of quality of life.


Introduction
Endometriosis is a condition in which functional endometrial tissue, including glands and stroma, exist ectopically outside the uterine cavity and myometrium [1]. When ectopic lesion infiltrates into the subserosa or subserosus plexus of bowel and beyond, bowel endometriosis is diagnosed [2]. Approximately 3%-10% of women suffer from endometriosis during childbearing age, 5%-20% of which include bowel endometriosis. 3 The rectum and sigmoid are the most common sites of involvement, accounting for more than 90% of all bowel endometriosis cases [3][4][5]. Bowel endometriosis, usually accompanied by lesions in other sites, can result in severe endometriosis-linked symptoms, such as dysmenorrhea, dyspareunia, chronic pelvic pain and infertility.
Furthermore, because of bowel involvement, patients may complain of various intestinal symptoms, including bowel movement pain, tenesmus, diarrhoea, dyschezia, rectal bleeding, and very rarely, bowel occlusion, all of which can seriously affect quality of life [6,7].
Unfortunately, all medical treatments provide only temporary relief, and symptoms have a high recurrence rate after withdrawal, probably because up to 80% of bowel lesions have a fibrotic component [8,9]. Therefore, surgical resection of endometriosis lesions is the preferred treatment for severe symptomatic or frequent recurrent patients. Usually, there are three options for surgical treatment: shaving, disc resection and segmental bowel resection. A positive correlation has been found between the extent of the lesions to be resected and symptom relief [10].Thus, we aim to remove the entire lesion, and segmental bowel resection may reach the maximal resection. Increasing number of gynaecologists have performed this complicated surgical technique and provided their patients with considerable relief, but the high complication rate and the long-term clinical outcomes Preoperative assessment Each patient completed a symptom questionnaires. Preoperative symptoms of all patients are summarized in Table 2. To evaluate pain, we used visual analogue scale (VAS) to evaluate the severity before surgery. The grades of pain were defined as follows: 0 (no pain), 1-3 (mild), 4-6 (moderated), and 7-10 (severe). A Short-Form 36 health survey questionnaire (SF-36 questionnaire) was administered to each patient before surgery. The SF-36 questionnaire consists of 36 questions that can be classified into 8 domains: physical functioning (RF), role physical (RP), bodily pain (BP), general health (GH), vitality (VT), social functioning (SF), role emotional (RE) and mental health (MH). Each domain can be scored respectively [13].

Operation procedure
Each patient was clearly informed of the high incidence of potential post-operative complications, and signed a dedicated informed consent form.
All of the patients underwent preoperative bowel preparation with 3000 ml macrogol solution and fasting for at least 12 hours. The operation was performed in laparoscopic procedure. The pelvic retroperitoneum was opened bilaterally. Pelvic adhesion was progressively dissected until both ureters were identified and isolated to the level of uterine artery. After bilateral uterosacral ligament lesions were exposed and resected, the bowel was mobilized from 2 cm below the lesion to the level of inferior mesenteric artery.
We performed segmental bowel resection only when a bowel lesion with maximum diameter more than 3 cm or infiltration depth at least 2 cm in bowel wall was detected.
The bowel was transected along distal margin of lesion using an angled stapling device and the proximal end with lesion was extracted out of pelvic cavity through an incision in the posterior vaginal fornix. The whole involved bowel segment was resected along proximal margin of lesion. The end of bowel was fixed an anvil plate and then returned to pelvic cavity through the vaginal incision, which was sutured later. Finally, bowel anastomosis was performed by using a circular stapler under laparoscopy.

Follow-up
All patients received GnRH-a after operation for 6 months. The VAS, SF-36 questionnaire, and an investigation about fertility were administered to all patients at least 5 year after operation. Median follow-up after operation was 76 months (62-105 months).

Statistical analysis
Statistical analysis was performed with SPSS Version 22.0 (IBM SPSS Statistics, IBM, USA).
Continuous variables were compared with Student's t-test and paired categorical variables were compared with Wilcoxon signed-rank test. P value <0.05 was considered statistically significant.

Surgical findings and intra-operative complications
All of the patients underwent laparoscopic surgery except for one, who required conversion to laparotomy during laparoscopic surgery due to extensive pelvic adhesion and excessive bleeding. All of the patients were found to have severe adhesions in pelvic cavity. The mean operative duration was 312±97min, the length of bowel to be resected was 7.10±2.88cm.
Sixty cases (96.8%) had lesions located in the rectosigmoid region. The remaining 2 cases, one involved the ileocecum, and the other involved the colon descendens. In 6 cases, at

Evolution of symptoms and quality of life
All of the patients complained of endometriosis-linked pain and various intestinal symptoms before surgery, as summarized in Table 2.
All of the patients suffered from pain, including dysmenorrhea, dyspareunia, bowel movement pain, chronic pelvic pain and tenesmus. Dysmenorrhea was the most frequently reported (90.3%). Semi-quantitative data on pre-and post-operative pain symptom intensity was summarized in Table 3 and Figure 1. A significant relief in all pain symptoms was observed. Qualitative data on pre-and post-operative intestinal symptoms was summarized in Table 4. The clinical remission rate (disappeared and relieved) of dyschezia, rectal bleeding and diarrhoea was 78.6%, 80% and 75%, respectively, and no aggravation was observed for any intestinal symptom.
The improvement of post-operative quality of life was statistically significant (P<0.001) for all 8 domains of SF-36 questionnaire. The scores are shown in Figure 2. Compared with the standardized data for the Chinese female population [14], there was no statistically significant difference (P>0.05) in post-operative scores for the 8 domains of SF-36 questionnaire except for VT ( Figure 3). But the post-operative score of VT was higher than standardized data for the Chinese female population.
According to the occurrence of post-operative complications, there was no statistically significant difference (P>0.05) in post-operative scors for all 8 domains of SF-36 questionnaire between patients with and without post-operative complications ( Figure 4).

Pregnancy after surgery
There were 16 patients with infertility history before our treatment, 10 of whom had tried to conceive after surgery. Until our follow-up, 7 had become pregnant, including 2 cases of IVF-ET. Among the 7 pregnant cases, 2 had labour, 3 underwent caesarean sections, one had spontaneous abortion in the second trimester, and one underwent clear palace because missed abortion was found at 14 weeks.

Discussion
In this study, we demonstrated the efficacy of segmental bowel resection for treating bowel endometriosis. This procedure provided obvious relief of pain and intestinal symptoms and significant improvement in quality of life.
Bowel endometriosis can be located in any part, mainly in rectosigmoid region, followed by ileocecum, appendix and caecum [2][3][4][5]. When the rectosigmoid region is involved, the most common intestinal symptoms are bowel movement pain and periodic tenesmus. This study found 60 cases of rectosigmoid region involvement. Of the remaining 2 cases of non-rectosigmoid involvement, one involved the ileocecum, a 4 cm×3 cm lesion had made the involved bowel segment rigid and constrictive; the other involved the colon descendens and presented 3 lesions at least 3 cm in size. Amazingly, despite such poor intestinal environments, the 2 non-rectosigmoid region involved patients had few intestinal symptoms. Intestinal symptoms may be related to the site of involvement. In our study, we did not find any lesions in the upper gastrointestinal tract. For patients with bowel endometriosis, less than 10% of cases are outside of the pelvic cavity [15]. In fact, not all patients with bowel endometriosis complain of intestinal symptoms; in this study, 12 patients had none. But all 62 patients complained of severe pain and sought treatment for pain. Therefore, the greatest discomfort resulting from bowel endometriosis is pain.
Previous studies about pain showed VAS scores of 8-9, 5-6, 1-8 and 2-6 for dysmenorrhea, dyspareunia, bowel movement pain and chronic pelvic pain [16][17][18], respectively, consistent with our study. Additionally, the mean scores for the 8 domains of the SF-36 questionnaire were quite low in this study, and BP had the lowest mean score (15.9). Our data implied that patients' quality of life were affected seriously, especially in terms of pain. Therefore, our treatment mainly aimed to relieve pain and improve quality of life.
As mentioned, medical treatments may be the first-line for DIE patients. Although several medical treatments can be efficacy, high rate of symptoms recur after withdrawal should be noted. Thus, these medicines may be used for prolonged periods of time, even years [19][20][21][22][23]. When bowel endometriosis seriously impacts quality of life, surgical resection is the preferred treatment [19]. Regarding the previous treatment of the patients in our study, 17 patients had received previous medical treatment for endometriosis with recurrence after withdrawal. On the other hand, 20 patients had undergone previous surgical treatment for endometriosis; however, only one involved the bowel, and it was just a simple biopsy for intestinal lesion. If entire lesions were not radically resected, patients may be at high risk of requiring re-operation. There are three options for surgical treatment: shaving, disc resection and segmental bowel resection [11]. Redwine and Sharpe firstly reported a case of laparoscopic segmental resection of the sigmoid colon as a treatment for bowel endometriosis [24]. Fedele have shown that the risk of clinical recurrence requiring further treatment was significantly higher in women who did not undergo colorectal resection when this region was involved widely [25]. Our indications of the surgical routes are as follows: 1. Shaving: lesions in the superficial seromuscular layer and less than 1 cm in size. 2. Disc resection: lesions invading the deep layer and no more than 2 cm in size that involve no more than 1/3 of the circumference of the whole bowel wall. 3. Segmental bowel resection: huge masses more than 3 cm in size or involving more They also showed significant improvement in all 8 domains of SF-36 questionnaire. But this study did not evaluate the impact of complications. [17] In addition, we cited the standardized data for the Chinese female population from Rui et al. [ 14], who examined 3124 SF-36 questionnaires from healthy population in Beijing, Shanghai, Guangzhou, Xian and Wuhan, the biggest cities in the north, east, south, west and centre of China, respectively. We found no significant difference between the post-operative scores of patients and the standardized data for Chinese female population except for VT, but the post-operative score of VT was the higher. This comparison indicated that bowel resection surgery can improve patients' quality of life to the level of the healthy population. A similar result has been found for the quality of life between the healthy population and patients who underwent segmental bowel resection of a much larger operative area to treat malignant tumour [30].
Although segmental bowel resection can achieve a satisfactory curative effect, this surgical route remains quite controversial because of the risk of complications [31][32][33].
There is still no consensus regarding the choice between radical (segmental resection) or conservative (shaving and disc resection) surgical management for bowel endometriosis, and different standards are applied in different centres. Some studies summarized their surgical procedure by indicating that there may be no difference in risk between disc resection and segmental bowel resection. Radical technique usually has a positive impact on clinical improvement of gynaecological and intestinal symptoms in patients with bowel involvement, but it requires high-tech comprehensive skill and surgical skill has a greater impact on risk than the surgical approach does [34][35][36]. The complication rate of segmental bowel resection for bowel endometriosis is estimated to be 10-22% [37,38].
Because of benign change, we resected the lesions just along the margins. No report indicates a better curative effect as a result of extending the bowel to be resected.
Mabrouk et al. indicated that the presence of satellite lesions or even positive resection margins did not seem to influence the clinical outcomes of segmental colorectal resection [18]. In addition, Abrão et al. 29  It is well known that endometriosis is associated with infertility. The infertility rate associated with endometriosis is 23-66%, of which 90% were primary [27,28,41,42]. But no study has indicated a higher pregnancy rate among patients who have undergone operation [43]. A systematic review conducted to assess the impact of colorectal surgery on the fertility of patients with DIE, has found a spontaneous pregnancy rate of 40-60% [41]. For asymptomatic bowel endometriosis patients with infertility, ART may be preferred, and bowel surgery may be necessary if IVF fails twice or more [44]. If surgery is needed, laparoscopy would achieve a better curative effect and pregnancy rate than    Table 3 Pre