Surgical Treatment of Intestinal Endometriosis: Outcomes of Three Different Techniques

► endometriosis ► laparoscopy ► colorectal surgery

Objective To outline the demographic and clinical characteristics of patients with deep intestinal endometriosis submitted to surgical treatment at a tertiary referral center with a multidisciplinary team, and correlate those characteristics with the surgical procedures performed and operative complications.

A prospective cohort from February 2012 to November 2016 of 32 women with deep intestinal endometriosis operations. The variables analyzed were: age; obesity; preoperative symptoms (dysmenorrhea, dyspareunia, acyclic pain, dyschezia, infertility, urinary symptoms, constipation and intestinal bleeding); previous surgery for endometriosis; Enzian classi fication; size of the intestinal lesion; and surgical complications.

The mean age was 37.75 ( /C6 5.72) years. A total of 7 patients (22%) had a prior history of endometriosis. The mean of the largest diameter of the intestinal lesions identified intraoperatively was of 28.12 mm ( /C6 14.29 mm). In the Enzian classi fication, there was a predominance of lesions of the rectum and sigmoid, comprising 30 cases (94%). There were no statistically signi ficant associations between the predictor variables and the outcome complications, even after the multiple logistic regression analysis. Regarding the size of the lesion, there was also no signi ficant correlation with the outcome complications ( p ¼ 0.18; 95% con fidence interval [95%CI]:0.94 –1.44); however, there was a positive association between grade 3 of the Enzia classi fication and the more extensive surgical techniqu es: segmental intestinal resection and rectosigmoidectomy, with a prevalence risk of 4.4 ( p < 0.001; 95%CI:1.60 –12.09).

The studied sample consisted of highly symptomatic women. A high prevalence of deep in filtrative endometriosis lesions was found located in the rectum and sigmoid region, and their size correlated directly with the extent of the surgical resection performed. received October 17, 2017 accepted April 16, 2018 published online June 27, 2018 DOI https://doi.org/ 10.1055/s-0038-1660827. ISSN 0100-7203. Copyright © 2018 by Thieme Revinter Publicações Ltda, Rio de Janeiro, Brazil Original Article THIEME 390

Characterized by the presence of active endometrial cells outside the uterine cavity, endometriosis is the second most common benign gynecological condition in women of repro- ductive age, affecting 7 –15% of the female population. 1,2 Generally, there is a delay in time between the first symp- toms and the diagnosis of endometriosis, approximately seven years, which is caused not only by symptoms of a nonspecific nature, but also by the lack of clinical suspicion and adequate interaction between different non-gynecolog- ical specialties. 2–4 The pelvis is the most affected site; however, there may be endometrial lesions in virtually any part of the abdomen, and even in other extrapelvic sites. 1,2,5,6 In deep manifes- tations of the disease, de fined as in filtration beyond 5 mm of the peritoneum, 7 some authors estimate the frequency of deep in filtrative endometriosis (DIE) at 5 –12% of women with endometriosis. 8–11 Intestinal involvement in DIE is frequent; however, its prevalence is controversial, with a description of 5 to 30% of occurrence in the intestine 9,12,13 depending on the accuracy of the diagnostic methods used and the interaction between the clinical and surgical teams in specialized services. While more than 90% of intestinal localization concern the rectum and distal sigmoid colon.8,14 Colorectal impairment impacts the quality of life of patients, mainly due to complaints of pain, and it causes alterations in bowel function. 11 Surgical treatment is cur- rently considered the first option in symptomatic patients with invasive intestinal compromise, as it leads to lasting relief of symptoms and improvement in quality of life. 1,4,8 A multidisciplinary team with experience in laparoscopic pelvic surgery and a precise preoperative diagnosis are fundamental for surgical planning. Tailored surgery, choos- ing the most appropriate technique for each patient, aims at better results in symptomatology, avoiding extensive, some- times unnecessary, procedures. 8,11 Different techniques of intestinal resection were used with variable results concern- ing quality of life and relapse of the disease, and the most widespread are rectosigmoidectomy, segmental and discoid resection, as well as shaving. 15–18 The objective of this study was to delineate the character- istics of the patients with DIE submitted to surgical treat- ment in a reference center with a multidisciplinary team, and to correlate the findings with the extent of the disease, the surgical procedures performed, and the complications observed. Resumo Objetivo Delinear as características das pacientes portadoras de endometriose profunda intestinal submetidas a tratamento cirúrgico em centro de referência com equipe multidisciplinar, e correlacionar tais achados com a extensão de doença e com os procedimentos cirúrgicos realizados. Métodos Tratamento cirúrgico no período de fevereiro de 2012 a novembro de 2016 em 32 mulheres portadoras de endometriose profunda intestinal. Variáveis analisadas: idade; obesidade; queixas pré-operatórias: dismenorreia, dispareunia, dor acíclica, disquezia, sangramento uterino anormal, infe rtilidade, sintomas urinários, constipa- ção, e sangramento intestinal; cirurgia prévia para tratamento de endometriose profunda; classi ficação de Enzian; técnica cirúrgica aplicada; tamanho da lesão intestinal; e complicações operatórias. Resultados A média de idade foi de 37,75 ( /C6 5,72) anos. Um total de 7 (22%) pacientes tinha histórico de abordagem prévia da endometriose. A média do maior diâmetro das lesões intestinais foi de 28,12 mm ( /C6 14,29 mm). Na classi ficação de Enzian, houve predomínio das lesões da região de reto ou retossigmoide no comparti- mento posterior, num total de 30 casos (94%). Não foi observada associação estatística significativa entre as variáveis preditivas e o desfecho da complicação, mesmo após análise de regressão logística múltipl a. Quanto ao tamanho da lesão, também não houve correlação signi ficativa com o desfecho complicação ( p ¼ 0,18; intervalo de confiança de 95% [IC95%]: 0,94 –1,44). No entanto, Houve associação positiva entre o grau 3 da classi ficação de Enzian e a técnica cirúrgica mais extensa: ressecção intestinal segmentar e retossigmoidectomia, com risco de prevalência de 4,4 ( p ¼ 0,00003; IC95%: 1,60 –12,09). Conclusão A amostra populacional estudada foi constituída de mulheres muito sintomáticas. Foi encontrada prevalência alta de lesões de endometriose in filtrativa profunda localizadas em região de retossigmoide, e seu tamanho correlacionou-se diretamente com a extensão da ressecção cirúrgica realizada. Palavras-Chave ► endometriose ► laparoscopia ► cirurgia colorretal Rev Bras Ginecol Obstet Vol. 40 No. 7/2018 Surgical Treatment of Int estinal Endometriosis Bray-Beraldo et al. 391

The present study is a partial results report of a bigger research that consists of a long-term follow-up that analyzes clinical and surgical outcomes of patients that underwent surgical treatment for intestinal endometriosis, approved by the Ethics Committee of the Institute of Medical Assistance of the Hospital do Servidor Público Estadual of the city of São Paulo. The method used in this study complied with the criteria of Resolution no. 466/12 on Ethics in Research with Human Beings of the Brazilian National Health Council, under CAAE no. 50405215.1.0000.5463. This prospective cohort consists of 32 women, aged over 18 years, with a diagnosis of deep intestinal endometriosis. All surgical procedures were performed at the Hospital do Servidor Público Estadual of the city of São Paulo by an experienced multidisciplinary team of the Gastroenterology Surgery and Gynecology Services, in the period from Febru- ary 2012 to November 2016. The preoperative complementary propedeutics consisted of rigid rectosigmoidoscopy, nuclear magnetic resonance of the pelvis, and transvaginal pelvic ultrasonography with bowel preparation. 19 The Enzian classification20,21 was adopted to describe the extent of the endometriosis identi fied during the intra- operative period; since it was used exclusively to describe the surgical findings, it did not interfere with the surgical judgment. This classi fication enables a good morphological description of deep invasive endometriosis through the de- nomination of the affected compartments and the size of the lesion. 20,21 Colonic retrograde preparation was used on the eve of the procedure with glycerin and prophylactic intraoperative antibiotic with second generation cephalosporin (Cefoxitin, Pfizer Inc., New York, NY, US). The laparoscopic access was performed through a 10-mm umbilical trocar and 30 degree laparoscope. The access trocars had 12 mm and 5 mm on the right flank, and 5 mm on the left flank. In some cases, a 5-mm suprapubic auxiliary puncture was performed. The surgical management of each technique was based on endometriosis foci patterns such as length, single or multiple lesions, and degree of bowel in filtration, and a complete resection of all macroscopic diseases was performed. When segmental resection or rectosigmoidectomy were performed, colorectal anastomosis was performed using a double stapling technique and extraction of the surgical specimen through a Pfannenstiel incision ( ►Fig. 1 ). In the full-thickness discoid resections, the surgical specimen was removed through circu- lar stapling, which had a diameter of 33 mm. In all “shaving” resections, the intestinal muscular layer was sutured with Caprofyl 3.0 (Ethicon Inc., Bridgewater, NJ, US). The variables analyzed were: age; obesity; preoperative symptoms (dysmenorrhea, dyspareunia, acyclic pain, dysche- zia, infertility, urinary symptoms, constipation and intestinal bleeding); previous surgery for endometriosis; Enzian classifi- cation; size of the intestinal lesion; and surgical complications. Note that the size of the endometriotic lesion was measured at the operation room just after the specimen was resected. In the data analysis, the arithmetic mean and standard deviation were used when there was a normal distribution of the sampl,e and median and quartiles were used when the data were not parametric. The frequency distributions of the categorical variables were also observed and reported as absolute numbers followed by percentages: n (%). The statis- tical program used was the R (R Foundation for Statistical Computing, Vienna, Austria) software, version 3.3.1, for the multiple regression analysis, to try to detect a correlation between predictor variables and outcomes. In the modeling of the regressions, the variables were initially selected by a significance cut-off point of /C20 0.20 to provide a more comprehensive range of possible predictor variables. The final statistical signi ficance level was set at p < 0.05, corre- sponding to a 95% con fidence interval (95%CI).

In total, 32 women with DIE were analyzed, with a mean age of 37.75 ( /C6 5.72) years, ranging from 27 to 50 years. The distribution of the frequency of the symptoms reported prior to the surgical treatment is shown in ►Table 1 . No patient complained of intestinal bleeding. All were on steroid hormone medication for induction of amenorrhea, and 14 (45.16%) had used a gonadotropin-releasing hormone (GnRH) analogue during the preoperative clinical treatment. Fig. 1 Surgical specimen after rectal segmental resection. Table 1 Distribution of the frequency of preoperative symptoms Symptoms n (%) Dysmenorrhea 27 (84.38) Dyspareunia 22 (68.76) Acyclic pelvic pain 20 (62.50) Dyschezia 16 (50.00) Intestinal constipation 16 (50.00) Infertility 11 (34.38) Abnormal uterine bleeding 5 (15.63) Abbreviations: n, absolute number; %, percentage. Rev Bras Ginecol Obstet Vol. 40 No. 7/2018 Surgical Treatment of Intestinal Endometriosis Bray-Beraldo et al.392 All patients underwent surgery after the failure of the clinical treatment to control the pelvic pain. In the preoperative evaluation, 11 (34.38%) patients pre- sented associated diseases, of different natures, without clinical repercussion. Regarding the previous surgery, 7 (21.88%) women had a prior history of endometriosis, all without intestinal intervention. The distribution pattern of intestinal lesions was 30 (93.75%) in the middle and high rectum, 4 (12.50%) in the sigmoid colon, 3 (9.37%) in the appendix, and 1 (3.12%) in the terminal ileum. The mean of the largest diameter of the intestinal lesions was of 28.12 mm ( /C6 14.29 mm), with a median of 27.5 mm (15 – 40 mm). It is important to mention that the accuracy of the preoperative radiologic exams was satisfactory, with the ex- ception of the lesions in the appendix and ileum, which were diagnosed only during the surgical intervention. After the multiple linear regression analysis, there was no statistically signi ficant correlation between the epidemio- logical data or the symptoms and the size of the DIE lesion ( ►Table 2 ). The staging of the in filtrative endometriotic disease through the Enzian classi fication is shown in ►Table 3 , with a predominance of lesions in the rectum or rectosig- moid region in the posterior compartment, comprising 30 (93.75%) cases. In 13 (40.62%) women, there was an associa- tion of ovarian cystic endometriosis, and 4 (12.5%) cases presented association with bladder lesions. A total of 4 (12.5%) other cases presented involvement of other intestinal segments: 1 (3.12%) in the ileum, and 3 (9.37%) in the appendix. The Enzian classi fication refers to lesions as “A” when they affect the region of the rectovaginal septum or vagina; “B” when they reach the retrocervical region and/or uterosacral ligaments; and “C” when the involvement is intestinal in filtration of the rectum or rectosigmoid. In addition, it separates lesion size into 3 cm, creating a visual staging of the pelvic involve- ment of deep endometriosis. ►Table 4 presents the distribution of the surgical techni- ques used for the resection of the intestinal lesions. All procedures were performed exclusively through laparosco- py. There was no requirement for ureteral resections, with 4 (12.50%) resections of nodules in the vesicouterine recess. In 1 (3.12%) patient, vaginal dome resection and rectum wall “shaving” were performed. Hospital discharge occurred after the return of intestinal peristalsis and good acceptance of a solid oral diet, with an approximate hospitalization time of 5 to 7 days, except for 1 (3.12%) patient. This case evolved with colorectal anastomo- sis fistula after segmental resection of the rectum, which was treated with antibiotic therapy. A total of 1 (3.12%) other patient required reoperation due to the manifestation of a rectovaginal fistula on the 8th postoperative day. A laparo- scopic derivative ileostomy loop approach was performed, followed after six weeks by resection of the fistulated anas- tomosis of the vagina, vaginal raf fia, and colorectal reanas- tomosis. After one month, the intestinal transit was restored. The cases of the anastomotic fistula and rectovaginal fistula were defined as “complications.” No statistically signi ficant associations were observed between possible predictor variables and the “complication” outcome, even after the multiple logistic regression analysis. There was also no signi ficant correlation with increased risk for “complication” in lesions greater than 30 mm (Enzian grade 3), ( p ¼ 0.18; 95%CI: 0.94 –1.44). There was a positive association between grade 3 of the Enzian classi fication and the most extensive surgical techniques: segmental intestinal resection and rectosigmoidectomy, with a prevalence risk of 4.4 (p ¼ 0.00003; 95%CI: 1.60 –12.09). Multiple logistic regression analysis was applied to the following variables: number of pregnancies, number of births, complaints of constipation, dyschezia and infertility, and size of the lesion in millimeters. A statistically significant association was found between lesion size and the outcome of bowel resection adjusted for the presence of dyschezia and previous surgery, as seen in ►Table 5 . Table 2 Multiple linear regression analysis for correlation of epidemiological characteristics and symptoms with DIE lesion size Variables Initial OR (95%CI) Adjusted OR (95%CI) Adjusted p-value (Wald test) Infertility 13.00 (3.30–22.69) 9.46 (–1.38–20.30) 0.08 Dyschezia 9.67 (–0.23–19.52) 6.06 (–3.92–16.04) 0.22 Abnormal uterine bleeding –10.81 (–24.69–3.06) –5.66 (–19.35–8.02) 0.40 Abbreviations: 95%CI, 95% con fidence interval; DIE, deep in filtrative endometriosis; OR, odds ratio. Table 3 Distribution of lesion lo cation through the Enzian classification Lesion size (cm) Degree Affected area ABC 33 1 0 1 3 Table 4 Distribution of surgical techniques Surgical technique n (%) “Shaving” of the rectum 14 (43.75) Segmental resection of the rectum 9 (28.13) Discoid resection of the rectum 6 (18.75) Rectosigmoidectomy 3 (9.38) Appendectomy 3 (9.37) “Shaving” of the ileum 1 (3.12) Abbreviations: n, absolute number; %, percentage. Rev Bras Ginecol Obstet Vol. 40 No. 7/2018 Surgical Treatment of Int estinal Endometriosis Bray-Beraldo et al. 393

Intestinal in filtrative endometriosis can be managed with clinical follow-up as long as the patient remains asymptom- atic and the intestinal lesion is not stenotic or bleeding. Although some women remain oligosymptomatic or without complaints, many persist with complaints of intense pain, which has an important impact on their personal and professional lives. 11 The most frequently encountered symp- toms are dysmenorrhea and dyspareunia, which corroborate with the findings of the present series of cases, in which the percentages were 84% and 69% respectively. Very similar data were found in a series of cases previously observed in our service22 and in a large study with more than 3,000 operated women, which found 95% of dysmenorrhea and 87% of dyspareunia.16 There is a wide range of drug options for symptom control; however, the decision to perform surgical treatment with resection of the endometriotic lesions proved to be the therapeutic option with better results in the control of symptoms and for quality of life. 23,24 In addition, a signi fi- cant number of intestinal lesions have a fibrotic component that does not respond to hormonal suppression. 25 In order to stage the endometriosis, the most commonly used classi fication system is from the American Society for Reproductive Medicine.26 However, there are limitations with respect to this classification, especially when involving retro- peritoneal structures and non-gynecological pelvic organs. Therefore, the Enzian classification was chosen, which enables the description of in filtrative lesions in the retrocervical region, rectovaginal septum, intestinal structures, bladder, and ureter. 20,21 In all cases in the present study there was intestinal involvement, with a predominance of in filtrative disease in compartment C of the classification (rectal interface with retrocervical and sigmoid region), corresponding to 93.75% of the lesions with/C24 28 mm of extension. These results differ from those in the literature regarding the main site of infiltrative disease; in the literature, there is a higher frequency of lesions located in compartment B (region of the uterosacral and cardinal ligaments). 21 This divergence may be the result of a selection bias in our series of cases due to referral for treatment in conjunction with a coloproctologist, suggesting intestinal involvement, or it may be due to the natural dif fi- culty to precisely de fine the location of the lesion, since the compartments (A, B, and C) of this classi fication are anatomi- cally contiguous. Although there is some disagreement in the application of the Enzian classification, this model seems to be the most adequate and functional, providing a postoperative description of DIE lesions. The techniques used to treat the intestinal lesions con- formed to the criteria to try to avoid large intestinal resec - tions, within the possibilities of the size of the lesion, while maintaining the radicality necessary to treat the symptom- atic disease. 16,27–29 In 44% of the cases, it was possible to carry out the excision of lesions by means of “shaving,” precisely because those lesions restrict themselves to the more super ficial muscular layer of the intestine. In 19% of the lesions with involvement beyond the muscular layer and up to 30 mm, a discoid resec - tion of the rectum was performed. In in filtrative lesions more than 30 mm in size, there was a need for segmental resection of the rectum or rectosigmoidectomy (in 37% of the cases), which was demonstrated by the positive correlation observed in the analysis between the degree of injury in the Enzian classification and the type of intestinal resection performed. Multiple regression showed that the larger the lesion size, the greater the association with the use of wider intestinal resec - tion, so that perhaps earlier diagnoses of minor lesions would enable the use of less extensive techniques, avoiding aggres- sive dissections and short- and long-term complications. Despite evidence on the improvement of symptoms after surgical treatment for intestinal endometriosis, there is no consensus about the superiority of one resection technique over another. 16,30–33 In addition, it is worth remembering that the proposed surgical treatment is always accompanied by risks of serious complications such as colorectal anastomosisfistula, ureteral lesion, rectovaginalfistula, and vascular lesions. 6,31,34 In the present study, there was only 1 (3.12%) case of a major complication that required reoperation. A rectovaginal fistula occurred due to the probable involvement of the posterior wall of the vagina in the stapling of the colorectal anastomosis during the segmental rectal resection. The occurrence of complications was low, with only two cases being reported, and there was no case of surgical conversion to the laparotomic technique; however, the number of cases in this series is too small for us to make adequate compar- isons with other reports in the literature. In addition, it was not possible to observe a statistical correlation between the variables and complications studied. Our multidisciplinary team does not routinely perform ileostomy after colorectal anastomosis. There was a need for ileostomy in a protective loop after segmental rectal resection in only one patient, due to the positive test for anastomotic leakage, both with air and methylene blue. Although most colorectal anastomoses are low, it is not necessary to indicate a systematic derivative stoma similar to that performed in low anterior rectosigmoidectomy in the treatment of colorectal cancer, as the pro file of the sample is completely different, composed of young women without severe comorbidities and well-nourished; however, this practice challenges those of other authors. 6 Table 5 Multiple logistic regression analysis for the correlation with the segmental resection surgical technique Variables Initial OR (95%CI) Adjusted OR (95%CI) Adjusted p-value (Wald Test) Size of the lesion 1.17 (1.05–1.3) 1.16 (1.04–1.30) 0.007 Dyschezia 5.57 (1.13–27.52) 3.09 (0.36–26.43) 0.303 Previous surgery 0.37 (0.06–2.19) 0.79 (0.0–8.84) 0.846 Abbreviations: 95%CI, 95% con fidence interval; OR, odds ratio. Rev Bras Ginecol Obstet Vol. 40 No. 7/2018 Surgical Treatment of Intestinal Endometriosis Bray-Beraldo et al.394 The distribution pattern of in filtrative endometriotic disease greatly distorts the pelvic anatomy, which makes it essential to have an in-depth knowledge of the anatomical planes and dissemination patterns of the disease, as well as a multidisciplinary team with experience in laparoscopic pel- vic surgery to perform the treatment with the maximum functional preservation of the pelvic organs. The authors arere aware that this study has a major limitation, since the amount of patients enrolled was low, and this directly affects the comparison of the surgical techniques performed. Nevertheless, the cohort is being enlarged, as surgical procedures continue to be performed by our study group, and an ultimate result may be published, as the endpoint established of one hundred patients is achieved.

The sample was composed of very symptomatic women; however, no symptoms or epidemiological characteristics correlated with the size of the DIE lesions or operative complications. On the other hand, the size of the lesions correlated directly with the extent of surgical resection performed, but not with the operative complications. Contributions Bray-Beraldo F, Pereira AMG, Gazzo C, Santos MP and Lopes RGC contributed with the conception and design, data collection and analysis, interpretation of data, writ- ing of the article, critical review of the intellectual con- tent, and final approval of the version to be published. Conflicts of Interest The authors have no con flicts of interest to disclose.

1 Klugsberger B, Shamiyeh A, Oppelt P, Jabkowski C, Schimetta W, Haas D. Clinical outcome after colonic resection in women with endometriosis. BioMed Res Int 2015;2015(15):514383 2 Alkatout I, Egberts JH, Mettler L, et al. Interdisciplinary diagnosis and treatment of deep in filtrating endometriosis. Zentralbl Chir 2016;141(06):630–638. Doi: 10.1055/s-0034-1383272 3 Arruda MS, Petta CA, Abrão MS, Benetti-Pinto CL. Time elapsed from onset of symptoms to diagnosis of endometriosis in a cohort study of Brazilian women. Hum Reprod 2003;18(04):756 –759 4 Santos TMV, Pereira AMG, Lopes RGC, Depes DdeB. Lag time between onset of symptoms and diagnosis of endometriosis. Einstein (Sao Paulo) 2012;10(01):39 –43. Doi: 10.1590/S1679- 45082012000100009 5 Prystowsky JB, Stryker SJ, Ujiki GT, Poticha SM. Gastrointestinal endometriosis. Incidence and indications for resection. Arch Surg 1988;123(07):855–858 6 Bachmann R, Bachmann C, Lange J, et al. Surgical outcome of deep infiltrating colorectal endometriosis in a multidisciplinary set- ting. Arch Gynecol Obstet 2014;290(05):919 –924. Doi: 10.1007/ s00404-014-3257-x 7 Cornillie FJ, Oosterlynck D, Lauweryns JM, Koninckx PR. Deeply infiltrating pelvic endometriosis: histology and clinical signi fi- cance. Fertil Steril 1990;53(06):978 –983. Doi: 10.1016/S0015- 0282(16)53570-5 8 Abrão MS, Petraglia F, Falcone T, Keckstein J, Osuga Y, Chapron C. Deep endometriosis infiltrating the recto-sigmoid: critical factors to consider before management. Hum Reprod Update 2015;21 (03):329–339. Doi: 10.1093/humupd/dmv003 9 Chapron C, Fauconnier A, Vieira M, et al. Anatomical distribution of deeply in filtrating endometriosis: surgical implications and pro- position for a classification. Hum Reprod 2003;18(01):157–161 10 Neme RM, Schraibman V, Okazaki S, et al. Deep infiltrating colorectal endometriosis treated with robotic -assisted rectosigmoidectomy. JSLS 2013;17(02):227–234. Doi: 10.4293/108680813/C2 13693422521836 11 Wolthuis AM, Meuleman C, Tomassetti C, D’Hooghe T, de Buck van Overstraeten A, D ’Hoore A. Bowel endometriosis: colorectal sur- geon’s perspective in a multidisciplinary surgical team. World J Gastroenterol 2014;20(42):15616–15623. Doi: 10.3748/wjg.v20. i42.15616 12 Seracchioli R, Poggioli G, Pierangeli F, et al. Surgical outcome and long-term follow up after laparoscopic rectosigmoid resection in women with deep infiltrating endometriosis. BJOG 2007;114(07): 889–895. Doi: 10.1111/j.1471-0528.2007.01363.x 13 Jerby BL, Kessler H, Falcone T, Milsom JW. Laparoscopic manage- ment of colorectal endometriosis. Surg Endosc 1999;13(11): 1125–1128 14 Bailey HR, Ott MT, Hartendorp P. Aggressive surgical management for advanced colorectal endometriosis. Dis Colon Rectum 1994;37 (08):747–753. Doi: 10.1007/BF02050136 15 Ruffo G, Scopelliti F, Manzoni A, et al. Long-term outcome after laparoscopic bowel resections for deep in filtrating endometrio- sis: a single-center experience after 900 cases. BioMed Res Int 2014;2014(14):463058 16 Donnez J, Jadoul P , Colette S, Luyckx M, Squifflet J, Donnez O. Deep rectovaginal endometriotic nodules: perioperative complications from a series of 3,298 patients operated on by the shaving technique. Gynecol Surg 2013;10(01):31–40. Doi: 10.1007/s10397-012-0759-z 17 Ceccaroni M, Clarizia R, Bruni F, et al. Nerve-sparing laparoscopic eradication of deep endometriosis with segmental rectal and parametrial resection: the Negrar method. A single-center, pro- spective, clinical trial. Surg Endosc 2012;26(07):2029 –2045. Doi: 10.1007/s00464-012-2153-3 18 Ribeiro PAA, Rodrigues FC, Kehdi IPA, et al. Laparoscopic resection of intestinal endometriosis: a 5-year experience. J Minim Invasive Gynecol 2006;13(05):442 –446. Doi: 10.1016/j.jmig.2006.05.010 19 Abrao MS, Gonçalves MO, Dias JA Jr, Podgaec S, Chamie LP, Blasbalg R. Comparison between clinical examination, transva- ginal sonography and magnetic resonance imaging for the diag- nosis of deep endometriosis. Hum Reprod 2007;22(12): 3092–3097. Doi: 10.1093/humrep/dem187 20 Haas D, Chvatal R, Habelsberger A, Wurm P, Schimetta W, Oppelt P. Comparison of revised American Fertility Society and ENZIAN staging: a critical evaluation of classifications of endometriosis on the basis of our patient population. Fertil Steril 2011;95(05): 1574–1578. Doi: 10.1016/j.fertnstert.2011.01.135 21 Haas D, Wurm P, Shamiyeh A, Shebl O, Chvatal R, Oppelt P. Efficacy of the revised Enzian classi fication: a retrospective analysis. Does the revised Enzian classi fication solve the problem of duplicate classification in rASRM and Enzian? Arch Gynecol Obstet 2013; 287(05):941–945. Doi: 10.1007/s00404-012-2647-1 22 Fahmy WM, Lopes RCG, Ramos JFD, et al. Evaluation of the results of surgical treatment of patients with endometriosis of the rectovaginal septum. Rev Bras Ginecol Obstet 2005;27(10): 613–618. Doi: 10.1590/S0100-72032005001000008 23 Dubernard G, Piketty M, Rouzier R, Houry S, Bazot M, Darai E. Quality of life after laparoscopic colorectal resection for endometriosis. Hum Reprod 2006;21(05):1243–1247. Doi: 10.1093/humrep/dei491 24 Bassi MA, Podgaec S, Dias JA Jr, D’Amico Filho N, Petta CA, Abrao MS. Quality of life after segmental resection of the rectosigmoid by laparoscopy in patients with deep in filtrating endometriosis with bowel involvement. J Minim Invasive Gynecol 2011;18(06):730–733. Doi: 10.1016/j.jmig.2011.07.014 Rev Bras Ginecol Obstet Vol. 40 No. 7/2018 Surgical Treatment of Int estinal Endometriosis Bray-Beraldo et al. 395 25 Remorgida V, Ferrero S, Fulcheri E, Ragni N, Martin DC. Bowel endometriosis: presentation, diagnosis, and treatment. Obstet Gyne- col Surv 2007;62(07):461 –470. Doi: 10.1097/01.ogx.0000268688. 55653.5c 26 Revised American Society for Reproductive Medicine classi fica- tion of endometriosis: 1996. Fertil Steril 1997;67(05):817 –821. Doi: 10.1016/S0015-0282(97)81391-X 27 de Almeida A, Fernandes LF, Averbach M, Abrão MS. Disc resection is the first option in the management of rectal endometriosis for unifocal lesions with less than 3 centimeters of longitudinal diameter. Surg Technol Int 2014;24:243 –248 28 Meuleman C, Tomassetti C, D ’Hoore A, et al. Surgical treatment of deeply infiltrating endometriosis with colorectal involvement. Hum Reprod Update 2011;17(03):311 –326. Doi: 10.1093/humupd/ dmq057 29 Roman H, Tuech JJ, Arambage K. Deep rectal shaving followed by transanal disc excision in large deep endometriosis of the lower rectum. J Minim Invasive Gynecol 2014;21(05):730 –731. Doi: 10.1016/j.jmig.2014.03.003 30 Fedele L, Bianchi S, Zanconato G, Bettoni G, Gotsch F. Long-term follow-up after conservative surgery for rectovaginal endome- triosis. Am J Obstet Gynecol 2004;190(04):1020 –1024. Doi: 10.1016/j.ajog.2003.10.698 31 De Cicco C, Corona R, Schonman R, Mailova K, Ussia A, Koninckx P. Bowel resection for deep endometriosis: a sys- tematic review. BJOG 2011;118(03):285 –291. Doi: 10.1111/ j.1471-0528.2010.02744.x 32 Acién P, Núñez C, Quereda F, Velasco I, Valiente M, Vidal V. Is a bowel resection necessary for deep endometriosis with rectova- ginal or colorectal involvement? Int J Womens Health 2013; 5:449–455. Doi: 10.2147/IJWH.S46519 33 Koh CE, Juszczyk K, Cooper MJW, Solomon MJ. Management of deeply infiltrating endometriosis involving the rectum. Dis Colon Rectum 2012;55(09):925–931. Doi: 10.1097/DCR.0b013e31825f3092 34 Darai E, Ackerman G, Bazot M, Rouzier R, Dubernard G. Laparo- scopic segmental colorectal resection for endometriosis: limits and complications. Surg Endosc 2007;21(09):1572 –1577. Doi: 10.1007/s00464-006-9160-1 Rev Bras Ginecol Obstet Vol. 40 No. 7/2018 Surgical Treatment of Intestinal Endometriosis Bray-Beraldo et al.396