{"paper_id":"22d71465-43f9-4342-b385-1b3d898d16d7","body_text":"Surgical Treatment of Intestinal Endometriosis:\nOutcomes of Three Different Techniques\nTratamento cirúrgico de endometriose intestinal:\nresultados de três técnicas operatórias\nFernando Bray-Beraldo 1 Ana Maria Gomes Pereira 2 Cláudia Gazzo 2 Marcelo Protásio Santos 1\nReginaldo Guedes Coelho Lopes 2\n1 Gastroenterology Surgery Service, Hospital do Servidor Público\nEstadual, São Paulo, SP , Brazil\n2 Ginecology Service, Hospital do Servidor Público Estadual,\nSão Paulo, SP , Brazil\nRev Bras Ginecol Obstet 2018;40:390 –396.\nAddress for correspondence Fernando Bray-Beraldo, MSc, Hospital\ndo Servidor Público Estadual, Rua Pedro de Toledo 1800, 14° andar,\nServiço de Gastrocirurgia - Vila Cl ementino, 04039-000, São Paulo, SP,\nBrasil (e-mail: drfernandobrayberaldo@gmail.com).\nKeywords\n► endometriosis\n► laparoscopy\n► colorectal surgery\nAbstract Objective To outline the demographic and clinical characteristics of patients with\ndeep intestinal endometriosis submitted to surgical treatment at a tertiary referral\ncenter with a multidisciplinary team, and correlate those characteristics with the\nsurgical procedures performed and operative complications.\nMethods A prospective cohort from February 2012 to November 2016 of 32 women\nwith deep intestinal endometriosis operations. The variables analyzed were: age;\nobesity; preoperative symptoms (dysmenorrhea, dyspareunia, acyclic pain, dyschezia,\ninfertility, urinary symptoms, constipation and intestinal bleeding); previous surgery\nfor endometriosis; Enzian classi fication; size of the intestinal lesion; and surgical\ncomplications.\nResults The mean age was 37.75 ( /C6 5.72) years. A total of 7 patients (22%) had a prior\nhistory of endometriosis. The mean of the largest diameter of the intestinal lesions\nidentified intraoperatively was of 28.12 mm ( /C6 14.29 mm). In the Enzian classi fication,\nthere was a predominance of lesions of the rectum and sigmoid, comprising 30 cases\n(94%). There were no statistically signi ficant associations between the predictor\nvariables and the outcome complications, even after the multiple logistic regression\nanalysis. Regarding the size of the lesion, there was also no signi ficant correlation with\nthe outcome complications ( p ¼ 0.18; 95% con fidence interval [95%CI]:0.94 –1.44);\nhowever, there was a positive association between grade 3 of the Enzia classi fication\nand the more extensive surgical techniqu es: segmental intestinal resection and\nrectosigmoidectomy, with a prevalence risk of 4.4 ( p < 0.001; 95%CI:1.60 –12.09).\nConclusion The studied sample consisted of highly symptomatic women. A high\nprevalence of deep in filtrative endometriosis lesions was found located in the rectum\nand sigmoid region, and their size correlated directly with the extent of the surgical\nresection performed.\nreceived\nOctober 17, 2017\naccepted\nApril 16, 2018\npublished online\nJune 27, 2018\nDOI https://doi.org/\n10.1055/s-0038-1660827.\nISSN 0100-7203.\nCopyright © 2018 by Thieme Revinter\nPublicações Ltda, Rio de Janeiro, Brazil\nOriginal Article\nTHIEME\n390\n\n\nIntroduction\nCharacterized by the presence of active endometrial cells\noutside the uterine cavity, endometriosis is the second most\ncommon benign gynecological condition in women of repro-\nductive age, affecting 7 –15% of the female population. 1,2\nGenerally, there is a delay in time between the first symp-\ntoms and the diagnosis of endometriosis, approximately\nseven years, which is caused not only by symptoms of a\nnonspecific nature, but also by the lack of clinical suspicion\nand adequate interaction between different non-gynecolog-\nical specialties.\n2–4\nThe pelvis is the most affected site; however, there may\nbe endometrial lesions in virtually any part of the abdomen,\nand even in other extrapelvic sites. 1,2,5,6 In deep manifes-\ntations of the disease, de fined as in filtration beyond 5 mm\nof the peritoneum, 7 some authors estimate the frequency of\ndeep in filtrative endometriosis (DIE) at 5 –12% of women\nwith endometriosis. 8–11 Intestinal involvement in DIE is\nfrequent; however, its prevalence is controversial, with a\ndescription of 5 to 30% of occurrence in the intestine 9,12,13\ndepending on the accuracy of the diagnostic methods used\nand the interaction between the clinical and surgical teams\nin specialized services. While more than 90% of intestinal\nlocalization concern the rectum and distal sigmoid\ncolon.8,14\nColorectal impairment impacts the quality of life of\npatients, mainly due to complaints of pain, and it causes\nalterations in bowel function. 11 Surgical treatment is cur-\nrently considered the first option in symptomatic patients\nwith invasive intestinal compromise, as it leads to lasting\nrelief of symptoms and improvement in quality of life. 1,4,8\nA multidisciplinary team with experience in laparoscopic\npelvic surgery and a precise preoperative diagnosis are\nfundamental for surgical planning. Tailored surgery, choos-\ning the most appropriate technique for each patient, aims at\nbetter results in symptomatology, avoiding extensive, some-\ntimes unnecessary, procedures.\n8,11 Different techniques of\nintestinal resection were used with variable results concern-\ning quality of life and relapse of the disease, and the most\nwidespread are rectosigmoidectomy, segmental and discoid\nresection, as well as shaving.\n15–18\nThe objective of this study was to delineate the character-\nistics of the patients with DIE submitted to surgical treat-\nment in a reference center with a multidisciplinary team, and\nto correlate the findings with the extent of the disease, the\nsurgical procedures performed, and the complications\nobserved.\nResumo Objetivo Delinear as características das pacientes portadoras de endometriose\nprofunda intestinal submetidas a tratamento cirúrgico em centro de referência com\nequipe multidisciplinar, e correlacionar tais achados com a extensão de doença e com\nos procedimentos cirúrgicos realizados.\nMétodos Tratamento cirúrgico no período de fevereiro de 2012 a novembro de 2016\nem 32 mulheres portadoras de endometriose profunda intestinal. Variáveis analisadas:\nidade; obesidade; queixas pré-operatórias: dismenorreia, dispareunia, dor acíclica,\ndisquezia, sangramento uterino anormal, infe rtilidade, sintomas urinários, constipa-\nção, e sangramento intestinal; cirurgia prévia para tratamento de endometriose\nprofunda; classi ficação de Enzian; técnica cirúrgica aplicada; tamanho da lesão\nintestinal; e complicações operatórias.\nResultados A média de idade foi de 37,75 ( /C6 5,72) anos. Um total de 7 (22%)\npacientes tinha histórico de abordagem prévia da endometriose. A média do maior\ndiâmetro das lesões intestinais foi de 28,12 mm ( /C6 14,29 mm). Na classi ficação de\nEnzian, houve predomínio das lesões da região de reto ou retossigmoide no comparti-\nmento posterior, num total de 30 casos (94%). Não foi observada associação estatística\nsignificativa entre as variáveis preditivas e o desfecho da complicação, mesmo após\nanálise de regressão logística múltipl a. Quanto ao tamanho da lesão, também não\nhouve correlação signi ficativa com o desfecho complicação ( p ¼ 0,18; intervalo de\nconfiança de 95% [IC95%]: 0,94 –1,44). No entanto, Houve associação positiva entre o\ngrau 3 da classi ficação de Enzian e a técnica cirúrgica mais extensa: ressecção intestinal\nsegmentar e retossigmoidectomia, com risco de prevalência de 4,4 ( p ¼ 0,00003;\nIC95%: 1,60 –12,09).\nConclusão A amostra populacional estudada foi constituída de mulheres muito\nsintomáticas. Foi encontrada prevalência alta de lesões de endometriose in filtrativa\nprofunda localizadas em região de retossigmoide, e seu tamanho correlacionou-se\ndiretamente com a extensão da ressecção cirúrgica realizada.\nPalavras-Chave\n► endometriose\n► laparoscopia\n► cirurgia colorretal\nRev Bras Ginecol Obstet Vol. 40 No. 7/2018\nSurgical Treatment of Int estinal Endometriosis Bray-Beraldo et al. 391\n\n\nMethods\nThe present study is a partial results report of a bigger\nresearch that consists of a long-term follow-up that analyzes\nclinical and surgical outcomes of patients that underwent\nsurgical treatment for intestinal endometriosis, approved by\nthe Ethics Committee of the Institute of Medical Assistance of\nthe Hospital do Servidor Público Estadual of the city of São\nPaulo. The method used in this study complied with the\ncriteria of Resolution no. 466/12 on Ethics in Research with\nHuman Beings of the Brazilian National Health Council,\nunder CAAE no. 50405215.1.0000.5463.\nThis prospective cohort consists of 32 women, aged over\n18 years, with a diagnosis of deep intestinal endometriosis.\nAll surgical procedures were performed at the Hospital do\nServidor Público Estadual of the city of São Paulo by an\nexperienced multidisciplinary team of the Gastroenterology\nSurgery and Gynecology Services, in the period from Febru-\nary 2012 to November 2016.\nThe preoperative complementary propedeutics consisted\nof rigid rectosigmoidoscopy, nuclear magnetic resonance of\nthe pelvis, and transvaginal pelvic ultrasonography with\nbowel preparation.\n19\nThe Enzian classification20,21 was adopted to describe the\nextent of the endometriosis identi fied during the intra-\noperative period; since it was used exclusively to describe\nthe surgical findings, it did not interfere with the surgical\njudgment. This classi fication enables a good morphological\ndescription of deep invasive endometriosis through the de-\nnomination of the affected compartments and the size of the\nlesion.\n20,21\nColonic retrograde preparation was used on the eve of the\nprocedure with glycerin and prophylactic intraoperative\nantibiotic with second generation cephalosporin (Cefoxitin,\nPfizer Inc., New York, NY, US). The laparoscopic access was\nperformed through a 10-mm umbilical trocar and 30 degree\nlaparoscope. The access trocars had 12 mm and 5 mm on the\nright flank, and 5 mm on the left flank. In some cases, a 5-mm\nsuprapubic auxiliary puncture was performed.\nThe surgical management of each technique was based on\nendometriosis foci patterns such as length, single or multiple\nlesions, and degree of bowel in filtration, and a complete\nresection of all macroscopic diseases was performed. When\nsegmental resection or rectosigmoidectomy were performed,\ncolorectal anastomosis was performed using a double stapling\ntechnique and extraction of the surgical specimen through a\nPfannenstiel incision (\n►Fig. 1 ). In the full-thickness discoid\nresections, the surgical specimen was removed through circu-\nlar stapling, which had a diameter of 33 mm. In all “shaving”\nresections, the intestinal muscular layer was sutured with\nCaprofyl 3.0 (Ethicon Inc., Bridgewater, NJ, US).\nThe variables analyzed were: age; obesity; preoperative\nsymptoms (dysmenorrhea, dyspareunia, acyclic pain, dysche-\nzia, infertility, urinary symptoms, constipation and intestinal\nbleeding); previous surgery for endometriosis; Enzian classifi-\ncation; size of the intestinal lesion; and surgical complications.\nNote that the size of the endometriotic lesion was measured at\nthe operation room just after the specimen was resected.\nIn the data analysis, the arithmetic mean and standard\ndeviation were used when there was a normal distribution of\nthe sampl,e and median and quartiles were used when the\ndata were not parametric. The frequency distributions of the\ncategorical variables were also observed and reported as\nabsolute numbers followed by percentages: n (%). The statis-\ntical program used was the R (R Foundation for Statistical\nComputing, Vienna, Austria) software, version 3.3.1, for the\nmultiple regression analysis, to try to detect a correlation\nbetween predictor variables and outcomes. In the modeling\nof the regressions, the variables were initially selected by a\nsignificance cut-off point of /C20 0.20 to provide a more\ncomprehensive range of possible predictor variables. The\nfinal statistical signi ficance level was set at p < 0.05, corre-\nsponding to a 95% con fidence interval (95%CI).\nResults\nIn total, 32 women with DIE were analyzed, with a mean age\nof 37.75 ( /C6 5.72) years, ranging from 27 to 50 years. The\ndistribution of the frequency of the symptoms reported prior\nto the surgical treatment is shown in ►Table 1 .\nNo patient complained of intestinal bleeding. All were on\nsteroid hormone medication for induction of amenorrhea,\nand 14 (45.16%) had used a gonadotropin-releasing hormone\n(GnRH) analogue during the preoperative clinical treatment.\nFig. 1 Surgical specimen after rectal segmental resection.\nTable 1 Distribution of the frequency of preoperative symptoms\nSymptoms n (%)\nDysmenorrhea 27 (84.38)\nDyspareunia 22 (68.76)\nAcyclic pelvic pain 20 (62.50)\nDyschezia 16 (50.00)\nIntestinal constipation 16 (50.00)\nInfertility 11 (34.38)\nAbnormal uterine bleeding 5 (15.63)\nAbbreviations: n, absolute number; %, percentage.\nRev Bras Ginecol Obstet Vol. 40 No. 7/2018\nSurgical Treatment of Intestinal Endometriosis Bray-Beraldo et al.392\n\n\nAll patients underwent surgery after the failure of the clinical\ntreatment to control the pelvic pain.\nIn the preoperative evaluation, 11 (34.38%) patients pre-\nsented associated diseases, of different natures, without\nclinical repercussion. Regarding the previous surgery, 7\n(21.88%) women had a prior history of endometriosis, all\nwithout intestinal intervention.\nThe distribution pattern of intestinal lesions was 30 (93.75%)\nin the middle and high rectum, 4 (12.50%) in the sigmoid colon,\n3 (9.37%) in the appendix, and 1 (3.12%) in the terminal ileum.\nThe mean of the largest diameter of the intestinal lesions was of\n28.12 mm ( /C6 14.29 mm), with a median of 27.5 mm (15 –\n40 mm). It is important to mention that the accuracy of the\npreoperative radiologic exams was satisfactory, with the ex-\nception of the lesions in the appendix and ileum, which were\ndiagnosed only during the surgical intervention.\nAfter the multiple linear regression analysis, there was no\nstatistically signi ficant correlation between the epidemio-\nlogical data or the symptoms and the size of the DIE lesion\n(\n►Table 2 ).\nThe staging of the in filtrative endometriotic disease\nthrough the Enzian classi fication is shown in ►Table 3 ,\nwith a predominance of lesions in the rectum or rectosig-\nmoid region in the posterior compartment, comprising 30\n(93.75%) cases. In 13 (40.62%) women, there was an associa-\ntion of ovarian cystic endometriosis, and 4 (12.5%) cases\npresented association with bladder lesions. A total of 4\n(12.5%) other cases presented involvement of other intestinal\nsegments: 1 (3.12%) in the ileum, and 3 (9.37%) in the\nappendix. The Enzian classi fication refers to lesions as “A”\nwhen they affect the region of the rectovaginal septum or\nvagina; “B” when they reach the retrocervical region and/or\nuterosacral ligaments; and “C” when the involvement is\nintestinal in filtration of the rectum or rectosigmoid. In\naddition, it separates lesion size into < 1c m ,1t o3c m ,\nand > 3 cm, creating a visual staging of the pelvic involve-\nment of deep endometriosis.\n►Table 4 presents the distribution of the surgical techni-\nques used for the resection of the intestinal lesions. All\nprocedures were performed exclusively through laparosco-\npy. There was no requirement for ureteral resections, with 4\n(12.50%) resections of nodules in the vesicouterine recess. In\n1 (3.12%) patient, vaginal dome resection and rectum wall\n“shaving” were performed.\nHospital discharge occurred after the return of intestinal\nperistalsis and good acceptance of a solid oral diet, with an\napproximate hospitalization time of 5 to 7 days, except for 1\n(3.12%) patient. This case evolved with colorectal anastomo-\nsis fistula after segmental resection of the rectum, which was\ntreated with antibiotic therapy. A total of 1 (3.12%) other\npatient required reoperation due to the manifestation of a\nrectovaginal fistula on the 8th postoperative day. A laparo-\nscopic derivative ileostomy loop approach was performed,\nfollowed after six weeks by resection of the fistulated anas-\ntomosis of the vagina, vaginal raf fia, and colorectal reanas-\ntomosis. After one month, the intestinal transit was restored.\nThe cases of the anastomotic fistula and rectovaginal fistula\nwere defined as “complications.”\nNo statistically signi ficant associations were observed\nbetween possible predictor variables and the “complication”\noutcome, even after the multiple logistic regression analysis.\nThere was also no signi ficant correlation with increased risk\nfor “complication” in lesions greater than 30 mm (Enzian\ngrade 3), ( p ¼ 0.18; 95%CI: 0.94 –1.44). There was a positive\nassociation between grade 3 of the Enzian classi fication and\nthe most extensive surgical techniques: segmental intestinal\nresection and rectosigmoidectomy, with a prevalence risk of\n4.4 (p ¼ 0.00003; 95%CI: 1.60 –12.09).\nMultiple logistic regression analysis was applied to the\nfollowing variables: number of pregnancies, number of\nbirths, complaints of constipation, dyschezia and infertility,\nand size of the lesion in millimeters. A statistically significant\nassociation was found between lesion size and the outcome\nof bowel resection adjusted for the presence of dyschezia and\nprevious surgery, as seen in\n►Table 5 .\nTable 2 Multiple linear regression analysis for correlation of\nepidemiological characteristics and symptoms with DIE lesion size\nVariables Initial OR\n(95%CI)\nAdjusted OR\n(95%CI)\nAdjusted\np-value\n(Wald test)\nInfertility 13.00\n(3.30–22.69)\n9.46\n(–1.38–20.30)\n0.08\nDyschezia 9.67\n(–0.23–19.52)\n6.06\n(–3.92–16.04)\n0.22\nAbnormal\nuterine\nbleeding\n–10.81\n(–24.69–3.06)\n–5.66\n(–19.35–8.02)\n0.40\nAbbreviations: 95%CI, 95% con fidence interval; DIE, deep in filtrative\nendometriosis; OR, odds ratio.\nTable 3 Distribution of lesion lo cation through the Enzian\nclassification\nLesion size (cm) Degree Affected area\nABC\n< 11 0 0 0\n1t o3 2 1 0 1 7\n> 33 1 0 1 3\nTable 4 Distribution of surgical techniques\nSurgical technique n (%)\n“Shaving” of the rectum 14 (43.75)\nSegmental resection of the rectum 9 (28.13)\nDiscoid resection of the rectum 6 (18.75)\nRectosigmoidectomy 3 (9.38)\nAppendectomy 3 (9.37)\n“Shaving” of the ileum 1 (3.12)\nAbbreviations: n, absolute number; %, percentage.\nRev Bras Ginecol Obstet Vol. 40 No. 7/2018\nSurgical Treatment of Int estinal Endometriosis Bray-Beraldo et al. 393\n\n\nDiscussion\nIntestinal in filtrative endometriosis can be managed with\nclinical follow-up as long as the patient remains asymptom-\natic and the intestinal lesion is not stenotic or bleeding.\nAlthough some women remain oligosymptomatic or without\ncomplaints, many persist with complaints of intense pain,\nwhich has an important impact on their personal and\nprofessional lives.\n11 The most frequently encountered symp-\ntoms are dysmenorrhea and dyspareunia, which corroborate\nwith the findings of the present series of cases, in which the\npercentages were 84% and 69% respectively. Very similar data\nwere found in a series of cases previously observed in our\nservice22 and in a large study with more than 3,000 operated\nwomen, which found 95% of dysmenorrhea and 87% of\ndyspareunia.16\nThere is a wide range of drug options for symptom control;\nhowever, the decision to perform surgical treatment with\nresection of the endometriotic lesions proved to be the\ntherapeutic option with better results in the control of\nsymptoms and for quality of life. 23,24 In addition, a signi fi-\ncant number of intestinal lesions have a fibrotic component\nthat does not respond to hormonal suppression. 25\nIn order to stage the endometriosis, the most commonly\nused classi fication system is from the American Society for\nReproductive Medicine.26 However, there are limitations with\nrespect to this classification, especially when involving retro-\nperitoneal structures and non-gynecological pelvic organs.\nTherefore, the Enzian classification was chosen, which enables\nthe description of in filtrative lesions in the retrocervical\nregion, rectovaginal septum, intestinal structures, bladder,\nand ureter.\n20,21 In all cases in the present study there was\nintestinal involvement, with a predominance of in filtrative\ndisease in compartment C of the classification (rectal interface\nwith retrocervical and sigmoid region), corresponding to\n93.75% of the lesions with/C24 28 mm of extension. These results\ndiffer from those in the literature regarding the main site of\ninfiltrative disease; in the literature, there is a higher frequency\nof lesions located in compartment B (region of the uterosacral\nand cardinal ligaments).\n21 This divergence may be the result of\na selection bias in our series of cases due to referral for\ntreatment in conjunction with a coloproctologist, suggesting\nintestinal involvement, or it may be due to the natural dif fi-\nculty to precisely de fine the location of the lesion, since the\ncompartments (A, B, and C) of this classi fication are anatomi-\ncally contiguous. Although there is some disagreement in the\napplication of the Enzian classification, this model seems to be\nthe most adequate and functional, providing a postoperative\ndescription of DIE lesions.\nThe techniques used to treat the intestinal lesions con-\nformed to the criteria to try to avoid large intestinal resec -\ntions, within the possibilities of the size of the lesion, while\nmaintaining the radicality necessary to treat the symptom-\natic disease.\n16,27–29\nIn 44% of the cases, it was possible to carry out the excision\nof lesions by means of “shaving,” precisely because those\nlesions restrict themselves to the more super ficial muscular\nlayer of the intestine. In 19% of the lesions with involvement\nbeyond the muscular layer and up to 30 mm, a discoid resec -\ntion of the rectum was performed. In in filtrative lesions more\nthan 30 mm in size, there was a need for segmental resection\nof the rectum or rectosigmoidectomy (in 37% of the cases),\nwhich was demonstrated by the positive correlation observed\nin the analysis between the degree of injury in the Enzian\nclassification and the type of intestinal resection performed.\nMultiple regression showed that the larger the lesion size, the\ngreater the association with the use of wider intestinal resec -\ntion, so that perhaps earlier diagnoses of minor lesions would\nenable the use of less extensive techniques, avoiding aggres-\nsive dissections and short- and long-term complications.\nDespite evidence on the improvement of symptoms after\nsurgical treatment for intestinal endometriosis, there is no\nconsensus about the superiority of one resection technique\nover another.\n16,30–33 In addition, it is worth remembering that\nthe proposed surgical treatment is always accompanied by risks\nof serious complications such as colorectal anastomosisfistula,\nureteral lesion, rectovaginalfistula, and vascular lesions.\n6,31,34\nIn the present study, there was only 1 (3.12%) case of a\nmajor complication that required reoperation. A rectovaginal\nfistula occurred due to the probable involvement of the\nposterior wall of the vagina in the stapling of the colorectal\nanastomosis during the segmental rectal resection. The\noccurrence of complications was low, with only two cases\nbeing reported, and there was no case of surgical conversion\nto the laparotomic technique; however, the number of cases\nin this series is too small for us to make adequate compar-\nisons with other reports in the literature. In addition, it was\nnot possible to observe a statistical correlation between the\nvariables and complications studied.\nOur multidisciplinary team does not routinely perform\nileostomy after colorectal anastomosis. There was a need for\nileostomy in a protective loop after segmental rectal resection\nin only one patient, due to the positive test for anastomotic\nleakage, both with air and methylene blue. Although most\ncolorectal anastomoses are low, it is not necessary to indicate a\nsystematic derivative stoma similar to that performed in low\nanterior rectosigmoidectomy in the treatment of colorectal\ncancer, as the pro file of the sample is completely different,\ncomposed of young women without severe comorbidities and\nwell-nourished; however, this practice challenges those of\nother authors.\n6\nTable 5 Multiple logistic regression analysis for the correlation\nwith the segmental resection surgical technique\nVariables Initial OR\n(95%CI)\nAdjusted OR\n(95%CI)\nAdjusted\np-value\n(Wald Test)\nSize of\nthe lesion\n1.17\n(1.05–1.3)\n1.16\n(1.04–1.30)\n0.007\nDyschezia 5.57\n(1.13–27.52)\n3.09\n(0.36–26.43)\n0.303\nPrevious\nsurgery\n0.37\n(0.06–2.19)\n0.79\n(0.0–8.84)\n0.846\nAbbreviations: 95%CI, 95% con fidence interval; OR, odds ratio.\nRev Bras Ginecol Obstet Vol. 40 No. 7/2018\nSurgical Treatment of Intestinal Endometriosis Bray-Beraldo et al.394\n\n\nThe distribution pattern of in filtrative endometriotic\ndisease greatly distorts the pelvic anatomy, which makes it\nessential to have an in-depth knowledge of the anatomical\nplanes and dissemination patterns of the disease, as well as a\nmultidisciplinary team with experience in laparoscopic pel-\nvic surgery to perform the treatment with the maximum\nfunctional preservation of the pelvic organs.\nThe authors arere aware that this study has a major\nlimitation, since the amount of patients enrolled was low,\nand this directly affects the comparison of the surgical\ntechniques performed. Nevertheless, the cohort is being\nenlarged, as surgical procedures continue to be performed\nby our study group, and an ultimate result may be published,\nas the endpoint established of one hundred patients is\nachieved.\nConclusion\nThe sample was composed of very symptomatic women;\nhowever, no symptoms or epidemiological characteristics\ncorrelated with the size of the DIE lesions or operative\ncomplications. On the other hand, the size of the lesions\ncorrelated directly with the extent of surgical resection\nperformed, but not with the operative complications.\nContributions\nBray-Beraldo F, Pereira AMG, Gazzo C, Santos MP and\nLopes RGC contributed with the conception and design,\ndata collection and analysis, interpretation of data, writ-\ning of the article, critical review of the intellectual con-\ntent, and final approval of the version to be published.\nConflicts of Interest\nThe authors have no con flicts of interest to disclose.\nReferences\n1 Klugsberger B, Shamiyeh A, Oppelt P, Jabkowski C, Schimetta W,\nHaas D. Clinical outcome after colonic resection in women with\nendometriosis. BioMed Res Int 2015;2015(15):514383\n2 Alkatout I, Egberts JH, Mettler L, et al. Interdisciplinary diagnosis\nand treatment of deep in filtrating endometriosis. Zentralbl Chir\n2016;141(06):630–638. Doi: 10.1055/s-0034-1383272\n3 Arruda MS, Petta CA, Abrão MS, Benetti-Pinto CL. Time elapsed\nfrom onset of symptoms to diagnosis of endometriosis in a cohort\nstudy of Brazilian women. Hum Reprod 2003;18(04):756 –759\n4 Santos TMV, Pereira AMG, Lopes RGC, Depes DdeB. Lag time\nbetween onset of symptoms and diagnosis of endometriosis.\nEinstein (Sao Paulo) 2012;10(01):39 –43. Doi: 10.1590/S1679-\n45082012000100009\n5 Prystowsky JB, Stryker SJ, Ujiki GT, Poticha SM. Gastrointestinal\nendometriosis. Incidence and indications for resection. Arch Surg\n1988;123(07):855–858\n6 Bachmann R, Bachmann C, Lange J, et al. Surgical outcome of deep\ninfiltrating colorectal endometriosis in a multidisciplinary set-\nting. Arch Gynecol Obstet 2014;290(05):919 –924. Doi: 10.1007/\ns00404-014-3257-x\n7 Cornillie FJ, Oosterlynck D, Lauweryns JM, Koninckx PR. Deeply\ninfiltrating pelvic endometriosis: histology and clinical signi fi-\ncance. Fertil Steril 1990;53(06):978 –983. Doi: 10.1016/S0015-\n0282(16)53570-5\n8 Abrão MS, Petraglia F, Falcone T, Keckstein J, Osuga Y, Chapron C.\nDeep endometriosis infiltrating the recto-sigmoid: critical factors\nto consider before management. Hum Reprod Update 2015;21\n(03):329–339. Doi: 10.1093/humupd/dmv003\n9 Chapron C, Fauconnier A, Vieira M, et al. Anatomical distribution of\ndeeply in filtrating endometriosis: surgical implications and pro-\nposition for a classification. Hum Reprod 2003;18(01):157–161\n10 Neme RM, Schraibman V, Okazaki S, et al. Deep infiltrating colorectal\nendometriosis treated with robotic -assisted rectosigmoidectomy. JSLS\n2013;17(02):227–234. Doi: 10.4293/108680813/C2 13693422521836\n11 Wolthuis AM, Meuleman C, Tomassetti C, D’Hooghe T, de Buck van\nOverstraeten A, D ’Hoore A. Bowel endometriosis: colorectal sur-\ngeon’s perspective in a multidisciplinary surgical team. World J\nGastroenterol 2014;20(42):15616–15623. Doi: 10.3748/wjg.v20.\ni42.15616\n12 Seracchioli R, Poggioli G, Pierangeli F, et al. Surgical outcome and\nlong-term follow up after laparoscopic rectosigmoid resection in\nwomen with deep infiltrating endometriosis. BJOG 2007;114(07):\n889–895. Doi: 10.1111/j.1471-0528.2007.01363.x\n13 Jerby BL, Kessler H, Falcone T, Milsom JW. Laparoscopic manage-\nment of colorectal endometriosis. Surg Endosc 1999;13(11):\n1125–1128\n14 Bailey HR, Ott MT, Hartendorp P. Aggressive surgical management\nfor advanced colorectal endometriosis. Dis Colon Rectum 1994;37\n(08):747–753. Doi: 10.1007/BF02050136\n15 Ruffo G, Scopelliti F, Manzoni A, et al. Long-term outcome after\nlaparoscopic bowel resections for deep in filtrating endometrio-\nsis: a single-center experience after 900 cases. BioMed Res Int\n2014;2014(14):463058\n16 Donnez J, Jadoul P , Colette S, Luyckx M, Squifflet J, Donnez O. Deep\nrectovaginal endometriotic nodules: perioperative complications\nfrom a series of 3,298 patients operated on by the shaving technique.\nGynecol Surg 2013;10(01):31–40. Doi: 10.1007/s10397-012-0759-z\n17 Ceccaroni M, Clarizia R, Bruni F, et al. Nerve-sparing laparoscopic\neradication of deep endometriosis with segmental rectal and\nparametrial resection: the Negrar method. A single-center, pro-\nspective, clinical trial. Surg Endosc 2012;26(07):2029 –2045. Doi:\n10.1007/s00464-012-2153-3\n18 Ribeiro PAA, Rodrigues FC, Kehdi IPA, et al. Laparoscopic resection\nof intestinal endometriosis: a 5-year experience. J Minim Invasive\nGynecol 2006;13(05):442 –446. Doi: 10.1016/j.jmig.2006.05.010\n19 Abrao MS, Gonçalves MO, Dias JA Jr, Podgaec S, Chamie LP,\nBlasbalg R. Comparison between clinical examination, transva-\nginal sonography and magnetic resonance imaging for the diag-\nnosis of deep endometriosis. Hum Reprod 2007;22(12):\n3092–3097. Doi: 10.1093/humrep/dem187\n20 Haas D, Chvatal R, Habelsberger A, Wurm P, Schimetta W, Oppelt P.\nComparison of revised American Fertility Society and ENZIAN\nstaging: a critical evaluation of classifications of endometriosis on\nthe basis of our patient population. Fertil Steril 2011;95(05):\n1574–1578. Doi: 10.1016/j.fertnstert.2011.01.135\n21 Haas D, Wurm P, Shamiyeh A, Shebl O, Chvatal R, Oppelt P. Efficacy\nof the revised Enzian classi fication: a retrospective analysis. Does\nthe revised Enzian classi fication solve the problem of duplicate\nclassification in rASRM and Enzian? Arch Gynecol Obstet 2013;\n287(05):941–945. Doi: 10.1007/s00404-012-2647-1\n22 Fahmy WM, Lopes RCG, Ramos JFD, et al. Evaluation of the results\nof surgical treatment of patients with endometriosis of the\nrectovaginal septum. Rev Bras Ginecol Obstet 2005;27(10):\n613–618. Doi: 10.1590/S0100-72032005001000008\n23 Dubernard G, Piketty M, Rouzier R, Houry S, Bazot M, Darai E. Quality\nof life after laparoscopic colorectal resection for endometriosis. Hum\nReprod 2006;21(05):1243–1247. Doi: 10.1093/humrep/dei491\n24 Bassi MA, Podgaec S, Dias JA Jr, D’Amico Filho N, Petta CA, Abrao MS.\nQuality of life after segmental resection of the rectosigmoid by\nlaparoscopy in patients with deep in filtrating endometriosis with\nbowel involvement. J Minim Invasive Gynecol 2011;18(06):730–733.\nDoi: 10.1016/j.jmig.2011.07.014\nRev Bras Ginecol Obstet Vol. 40 No. 7/2018\nSurgical Treatment of Int estinal Endometriosis Bray-Beraldo et al. 395\n\n\n25 Remorgida V, Ferrero S, Fulcheri E, Ragni N, Martin DC. Bowel\nendometriosis: presentation, diagnosis, and treatment. Obstet Gyne-\ncol Surv 2007;62(07):461 –470. Doi: 10.1097/01.ogx.0000268688.\n55653.5c\n26 Revised American Society for Reproductive Medicine classi fica-\ntion of endometriosis: 1996. Fertil Steril 1997;67(05):817 –821.\nDoi: 10.1016/S0015-0282(97)81391-X\n27 de Almeida A, Fernandes LF, Averbach M, Abrão MS. Disc resection\nis the first option in the management of rectal endometriosis for\nunifocal lesions with less than 3 centimeters of longitudinal\ndiameter. Surg Technol Int 2014;24:243 –248\n28 Meuleman C, Tomassetti C, D ’Hoore A, et al. Surgical treatment of\ndeeply infiltrating endometriosis with colorectal involvement. Hum\nReprod Update 2011;17(03):311 –326. Doi: 10.1093/humupd/\ndmq057\n29 Roman H, Tuech JJ, Arambage K. Deep rectal shaving followed by\ntransanal disc excision in large deep endometriosis of the lower\nrectum. J Minim Invasive Gynecol 2014;21(05):730 –731. Doi:\n10.1016/j.jmig.2014.03.003\n30 Fedele L, Bianchi S, Zanconato G, Bettoni G, Gotsch F. Long-term\nfollow-up after conservative surgery for rectovaginal endome-\ntriosis. Am J Obstet Gynecol 2004;190(04):1020 –1024. Doi:\n10.1016/j.ajog.2003.10.698\n31 De Cicco C, Corona R, Schonman R, Mailova K, Ussia A,\nKoninckx P. Bowel resection for deep endometriosis: a sys-\ntematic review. BJOG 2011;118(03):285 –291. Doi: 10.1111/\nj.1471-0528.2010.02744.x\n32 Acién P, Núñez C, Quereda F, Velasco I, Valiente M, Vidal V. Is a\nbowel resection necessary for deep endometriosis with rectova-\nginal or colorectal involvement? Int J Womens Health 2013;\n5:449–455. Doi: 10.2147/IJWH.S46519\n33 Koh CE, Juszczyk K, Cooper MJW, Solomon MJ. Management of deeply\ninfiltrating endometriosis involving the rectum. Dis Colon Rectum\n2012;55(09):925–931. Doi: 10.1097/DCR.0b013e31825f3092\n34 Darai E, Ackerman G, Bazot M, Rouzier R, Dubernard G. Laparo-\nscopic segmental colorectal resection for endometriosis: limits\nand complications. Surg Endosc 2007;21(09):1572 –1577. Doi:\n10.1007/s00464-006-9160-1\nRev Bras Ginecol Obstet Vol. 40 No. 7/2018\nSurgical Treatment of Intestinal Endometriosis Bray-Beraldo et al.396","source_license":"CC0","license_restricted":false}