{"paper_id":"82caeb84-f195-4e91-888f-2ed43c2049fe","body_text":"103\nColorectal endometriosis. A proposal of complementary \nclassification and surgical management in stages\nEndometriosis colorrectal. Una propuesta de clasificación complementaria y de manejo \nquirúrgico por etapas\nArmando Cepeda-Silva 1*, Harald Krentel 2, Oliver P. Cruz-Orozco 1, Jorge L. Vela-Cantorán 1,  \nEdgar González-Macedo 1, Alejandro Rendón-Molina 1, and José R. Silvestri-Tomassoni 1\n1Departamento de Ginecología Quirúrgica, Instituto Nacional de Perinatología, Mexico City, Mexico; 2Clinic of Gynecology, Obstetrics, Gynecological \nOncology and Senology, Academic Teaching Hospital, Bethesda Hospital, Duisburg, Germany\nAbstract\nObjective: To organize the experience and international knowledge in the surgical management and staging of colorectal endo-\nmetriosis, with a management proposal in stages. Method: An extensive non-systematic review of the literature was carried to \norganize the disease in stages (limited, intermediate and advanced) according to a scoring system, which considers the charac-\nteristics of the endometrioma, the personal history and surgical findings. We tested the proposed staging in a retrospective group \nof patients. Results: From January 2017 to April 2023, we collected 19 patients with a confirmed diagnosis of colorectal endo-\nmetriosis, treated laparoscopically, by the same group of surgeons, in whom we found a strong correlation between the stage of \nthe disease and the presence of complications that required reinterventions. Conclusions: We suggest a sequence of colorectal \nsurgical management in stages according to the staging of the disease and we hope that this work will be followed by joint efforts \nto test it prospectively in order to compare results between hospital centers and make planned decisions.\nKeywords: Colorectal endometriosis. Intestinal endometriosis. Deep endometriosis.\nResumen\nObjetivo: Organizar la experiencia y el conocimiento internacional en el manejo quirúrgico y la estadificación de la endometriosis \ncolorrectal, con una propuesta de manejo por etapas. Método: Se realizó una revisión amplia no sistemática de la literatura \npara organizar la enfermedad en etapas (limitada, intermedia y avanzada) de acuerdo con un sistema de puntuación que \nconsidera las características del endometrioma, los antecedentes personales y los hallazgos en la cirugía. La estatificación \npropuesta se probó en un grupo retrospectivo de pacientes. Resultados: De enero de 2017 a abril de 2023 recopilamos 19 \npacientes con diagnóstico confirmado de endometriosis colorrectal, tratadas por vía laparoscópica, por el mismo grupo de \ncirujanos, en las que encontramos una fuerte correlación entre el estadio de la enfermedad y la presencia de complicaciones \nque requirieron reintervenciones. Conclusiones: Sugerimos una secuencia de manejo quirúrgico colorrectal en etapas de \nacuerdo con la estadificación de la enfermedad y esperamos que el presente trabajo sea seguido de esfuerzos compartidos \npor probarla de manera prospectiva para poder comparar resultados entre centros hospitalarios y tomar decisiones planificadas.\nPalabras clave : Endometriosis colorrectal. Endometriosis intestinal. Endometriosis profunda.\n ORIGINAL ARTICLE\nCir Cir (Eng). 2024;92(1):103-109  \nContents available at PubMed  \nwww.cirugiaycirujanos.com\n*Correspondence: \nArmando Cepeda-Silva  \nE-mail: corcolos4@gmail.com\n2444-0507/© 2023 Academia Mexicana de Cirugía. Published by Permanyer. This is an open access article under the terms of the CC BY-NC-ND license  \n(http://creativecommons.org/licenses/by-nc-nd/4.0/ ).\nDate of reception: 12-05-2023\nDate of acceptance: 12-08-2023\nDOI: 10.24875/CIRUE.M23000598\nCIRUGIA Y CIRUJANOS (ENG)\n\nCirugía y Cirujanos (Eng). 2024;92(1)\n104\nIntroduction\nEndometriosis is a chronic inflammatory disease \ncaused by endometrial tissue growing outside the \nuterus. It is estimated to affect 2% to 10% of the fe -\nmale population overall, rising up to 50% in women \nwith infertility, affecting, at least, 190 million reproduc -\ntive-age women and some beyond menopause 1.\nA prevalence of 8% to 12% has been estimated for \ncolorectal endometriosis, with almost 90% of all intes -\ntinal lesions being found in the rectum and sigmoid \ncolon2.\nThe main symptoms of endometriosis include chron -\nic pelvic pain related to the menstrual cycle and infer -\ntility. When the condition affects the intestines, \nadditional symptoms such as abdominal bloating, \nchanges to bowel habits (constipation or diarrhea), \npassage of mucus with bowel movements, rectal \nbleeding, urgency to defecate, and feeling of incom -\nplete evacuation may occur, often worsening with the \nmenstrual cycle. Additionally, endometriotic nodules \ncan cause narrowing of the intestinal lumen leading \nto obstructive symptoms, and eventually to reduced \nquality of life affecting not only women with endome -\ntriosis but also their partners and families 3,4.\nMedical treatment of deep endometriosis involving \nthe colorectum is an option for many women, with \nsymptomatic relief probabilities ranging from 70% to \n80%5 and increased overall pregnancy rates from 42% \nup to 80% 3. However, there is a group of patients who \nwill require surgical management, including those who \nhave not responded favorably to medical manage -\nment, those with contraindications or intolerance to \nhormonal therapy, those with intestinal obstructive \nsymptoms, and couples seeking natural conception or \npreferring surgery 6.\nTwo distinct approaches have been described in the \nmanagement of colorectal endometriosis, with differ -\nent rates of complications, long-term side effects, and \nrecurrences:\n– A radical approach with segmental colorectal re -\nsection and anastomosis.\n– A more conservative approach involving local \ntransmural and non-transmural resections, with \nreconstructions using manual or mechanical \nsutures5,6.\nThe balance between the conservative or the radical \napproach regarding complications and recurrence \nrates has led to a debate among different surgical \nschools, with no current consensus on the standard \nsurgical technique 5.\nWe believe that the problem arises when discussing \ncolorectal endometriosis as a uniform condition with -\nout recognizing the significant differences in treating \nlimited vs advanced disease. Currently, there is no \nstandardized classification to design staged therapies \nthat can be compared among different working groups \nregarding cure outcomes, morbidity/mortality, and \nrecurrence.\nTherefore, we decided to develop a staging classifi -\ncation for colorectal endometriosis, considering the cu -\nmulative global experience in its management, including \nthe treating surgeon’s criteria for choosing the extent \nand type of surgery, associated complications, disease \nrecurrence rates, and need for reinterventions. We ret -\nrospectively tested this classification on a group of \npatients treated at Instituto Nacional de Perinatología, \nMexico City, Mexico from 2017 through 2023.\nMethod\nThe group of authors, including 6 national and 1 \ninternational member of various backgrounds (gyne -\ncologists, urogynecologists, reproductive biologists, \ncolorectal surgeons, and general surgeons), all expe -\nrienced in advanced pelvic surgery, both laparoscopic \nand open, worked collaboratively, both in-person and \nonline, to conduct a non-systematic review of the lit -\nerature. This review included the clinical practice \nguidelines from the European Society of Human Re -\nproduction and Embryology (ESHRE) 7, the German \nguidelines from 2014 8, and meta-analyses, random -\nized and non-randomized controlled clinical trials, pro -\nspective and retrospective studies since 2006 through \n2022. Overall, these sources included a total of \n16 846 patients, aiming to review the factors involved \nin the surgeons’ decisions when treating patients with \ncolorectal endometriosis, the factors associated with \nintra- and postoperative complications, and the factors \nassociated with disease recurrence.\nOnce these factors were identified, they were \ngrouped into categories, being the most relevant \nthose associated with tumor characteristics (T), with \nthe patients’ medical history (H) and with surgical fac -\ntors (S), creating the acronym THS.\nAfter defining the categories, they were categorized \ninto 3 groups, being the first one the best clinical-\nsurgical scenario and the third one being the worst \nscenario and defining an intermediate group in terms \nof technical difficulty, complications, and recurrences.\n\nA. Cepeda-Silva et al. Colorectal endometriosis. Treatment\n105\nEach group was assigned a numerical parameter \nrepresenting it, allowing for proper differentiation of \neach group. This resulted in defining an unclassifiable \nstage due to lack of data, an initial stage or THS 1, \nan intermediate stage of evolution or THS 2, and an \nadvanced stage of the disease or THS 3.\nDue to the nature of the disease and the difficulties \nin diagnosis, an initial preoperative classification (for \nsurgical planning purposes) will be performed, which \nwill be complemented with intraoperative findings and \ndefined postoperatively with histopathological results \n(both with prognostic purposes).\nThe version thus obtained is retrospectively eval -\nuated using data from electronic health records \nfrom a group of consecutive patients treated at In -\nstituto Nacional de Perinatología from January 2017 \nthrough April 2023 (including the years of the CO -\nVID-19 pandemic, which limited non-emergency \nsurgeries due to hospital restructuring), with a con -\nfirmed histopathological diagnosis of colorectal \nendometriosis.\nBased on the findings made, the group provides \nrecommendations for the staged surgical treatment of \npatients with colorectal endometriosis.\nResults\nCharacteristics to be assessed by the \nsurgeon for surgical decision-making in \npatients with colorectal endometriosis\nAfter reviewing the literature on factors impacting \nthe surgeon’s decision-making on the surgical treat -\nment of patients with colorectal endometriosis, factors \nassociated with intra-  and postoperative complica -\ntions, and factors associated with disease recurrence, \nwe stay with the following elements as the character -\nistics that should be evaluated: those that are endo -\nmetrioma-dependent, those dependent on the patients’ \npast medical history, and those dependent on surgery \n(Table 1):\n– Tumor or endometrioma: size, number, location, \ndepth of invasion of colorectal wall, and presence \nor absence of intestinal lumen obstruction.\n– Patient history: age, body mass index, thrombo -\nembolic risk, and health status.\n– Surgery: previous surgeries for endometriosis, \ntype of current surgery, intraoperative bleeding, \nand histopathological examination of resected \nmaterial.\nTable 1. Characteristics to be evaluated by the surgeon for surgical \ndecision-making in a patient with colorectal endometriosis\nTumor (characteristics of \ncolorectal endometrioma)\nSize\nNumber\nLocation\nDepth of invasion\nIntestinal lumen obstruction\nBackground Age\nBMI\nCaprini (thromboembolic risk \nclassification)\nASA (American Society of \nAnesthesiologists) health status \nclassification\nSurgery History of previous surgeries for \nendometriosis\nType of surgery performed in the \ncurrent procedure\nIntraoperative bleeding\nHistopathological resection\nASA: American Society of Anesthesiologists; BMI: body mass index.\nOnce the characteristics to be considered by the \nsurgeon in decision-making were defined and grouped, \na table was created to score their importance in 3 \ncategories, from 0 to 3, based on the importance of \neach characteristic and its specific weight in decision-\nmaking process ( Table 2).\nRegarding the characteristics of the endometrioma \nor tumor, we considered as the most favorable \nscenarios the presence of only 1 lesion, size \n< 3 cm, location above the rectum, depth of invasion \nnot exceeding the serosa, and no evidence of \ncolorectal lumen obstruction. Conversely, the least \nfavorable characteristics include endometrioma or \ntumor size > 3 cm, presence of 3 or more lesions, \nlower rectum location, involving the full thickness \nof the wall, and causing some form of colorectal \nlumen obstruction.\nRegarding the patient’s past medical history, the \nmost favorable scenarios are said to be age younger \nthan 40 years, a body mass index (BMI) under 34, \nlow-to-moderate thromboembolic risk, and a healthy-\nto-stable and controlled comorbidity status (American \nSociety of Anesthesiologists [ASA] I-II). Conversely, \nthe least favorable scenarios include age older than \n\nCirugía y Cirujanos (Eng). 2024;92(1)\n106\nTable 2. Auxiliary table for scoring characteristics based on their importance for decision-making in the treatment of a patient with \ncolorectal endometriosis\nItem 0 points 1 point 3 points\nTumor Size: < 3 cm No scoring Size: > 3 cm\nNumber: 1 Number: 2 Number: > 3\nLocation: above rectum Location: rectosigmoid junction Location: lower rectum\nDepth: serosal Depth: muscular Depth: full thickness\nObstruction: no No scoring Intestinal lumen obstruction: yes\nHistory Age: < 40 years Age: > 40 No scoring\nBMI: < 34 BMI: > 35 \nCaprini: low, medium Caprini: high or very high\nASA: I-II ASA: > III\nSurgery Previous surgeries for endometriosis: no Previous surgeries for endometriosis: yes No scoring\nCurrent surgery: nodules resection Current surgery: includes hysterectomy Current surgery: includes urinary tract \nopening or extrapelvic involvement\nHemorrhage: < 500 mL No scoring Hemorrhage: > 500 mL\nPathology: complete resection Pathology: residual endometriosis No scoring\nASA: American Society of Anesthesiologists; BMI: body mass index.\n40 years, BMI > 35, high-to-very high thromboembolic \nrisk, and ASA > III health status. The patient’s pats \nmedical history was scored from 0 to 1 point as it was \nconsidered by the surgeons to be of lesser importance \nin intraoperative decision-making vs tumor \ncharacteristics or surgical factors.\nRegarding surgical factors, the most favorable \nscenario is when the patient has no history of \nprevious surgeries for endometriosis, only undergoing \nresection of endometriotic nodules in the current \nsurgery, with intraoperative bleeding of < 500 mL, \nand pathology reporting complete resection of the \nendometrioma margins. In contrast, the least \nfavorable scenario includes a history of previous \nsurgeries for endometriosis, current surgery involving \nopening the genital or urinary tracts or with extrapelvic \ninvolvement, intraoperative bleeding > 500 mL, and \nresidual endometriosis on the histopathological \nexamination.\nHaving defined the importance of these \ncharacteristics and grouped them for scoring, patients \nwere categorized into 4 stages. The first stage \nincluding those for whom sufficient information was \nnot available for classification, while the remaining \nstages include those with limited, intermediate, and \nadvanced disease ( Table 3).\nRetrospective assessment of patients \ntreated with a confirmed diagnosis of \ncolorectal endometriosis\nFrom January 2017 through April 2023, we collected \ndata from 19 patients diagnosed with colorectal \nendometriosis, treated laparoscopically by the same \ngroup of lead surgeons ( Table 4).\nAccording to the Enzian classification, 17 of our \npatients were considered to have C1 colorectal \ninvolvement, 1  patient had C2 involvement, and \nanother one, C3 involvement. When categorized \nbased on the THS system, patients fell into THS \n1 (8 patients), THS 2 (6 patients), and THS 3 (5 patients) \n(Table 5).\nTable 3. Stage categorization of patients with colorectal \nendometriosis \nStage Meaning Score\nU Unclassifiable Missing data for classification purposes\nTHS 1 Limited 0-2\nTHS 2 Intermediate 3-4\nTHS 3 Advanced > 5\n\nA. Cepeda-Silva et al. Colorectal endometriosis. Treatment\n107\nTable 4. Retrospective evaluation of patients treated at Instituto Nacional de Perinatología with a confirmed diagnosis of colorectal \nendometriosis\nPatient THS score THS stage Enzian classification* Surgical management Complications and observations\n1 4 2 C1 LNTR No\n2 4 2 C1 LNTR No\n3 4 2 C1 LNTR No\n4 1 1 C1 LNTR No\n5 6 3 C1 SRA No\n6 4 2 C1 LNTR No\n7 0 1 C1 LNTR No\n8 8 3 C1 LNTR Yes†\n9 4 2 C1 LNTR No\n10 4 2 C1 LNTR No\n11 2 1 C1 LNTR No\n12 5 3 C1 LNTR Yes‡\n13 4 2 C1 LNTR No\n14 4 2 C1 LNTR No\n15 1 1 C2 LNTR Yes§\n16 12 3 C3 SRA Yes¶\n17 2 1 C1 LNTR No\n18 6 3 C1 LNTR Yes**\n19 2 1 C1 LNTR No\nLNTR: local non-transmural resection; SRA: segmental resection with anastomosis.\n*Only Enzian stage is considered for colorectal involvement. \n†Intestinal perforation as a complication not detected intraoperatively, requiring intestinal resection and emergency stoma in a 2nd surgical act. \n‡Surgical wound infection. Six colorectal nodules, each 1 cm in size, were resected during a 6-hour surgery. \n§Surgical drainage of pelvic hematoma via laparoscopy. \n¶3rd degree burn due to equipment use, requiring escharotomy and double interpositional flap. \n**Intraoperative hemorrhage (1800 mL) and 6-hour surgical time.\nRegarding the type of surgical management used, \n17 patients underwent local non-transmural resection \n(LNTR), and 2  patients underwent segmental resec -\ntion with colo-colo segmental resection with anasto -\nmosis (SRA) without protective stoma.\nWe encountered complications in 5 patients, ac -\ncounting for 26% of the sample, with 74% of the pa -\ntients progressing uneventfully.\nAmong patients treated with SRA, 1 progressed un -\neventfully, while another one suffered a third-degree \nburn due to equipment use, which required escharoto -\nmy and a double interpositional flap in a 2nd surgical act.\nAmong the patients operated on with LNTR, we had \n4 cases with complications: 1 had an intraoperative \nundetected intestinal perforation, which required intes -\ntinal resection and emergency stoma in a 2 nd surgical \nact, 1 had a surgical wound infection, 1 required surgi -\ncal laparoscopial drainage of a pelvic hematoma, and \nfinally, 1 experienced intraoperative bleeding (1800 mL) \nand a 6-hour surgical procedural time.\nFour out of the 5 patients with complications had \nadvanced colorectal disease with THS 3, which ac -\ncounted for 80% of the sample. Additionally, we ob -\nserved that a THS 3 level positively correlated with \nthe presence or absence of surgical complications, \n80% and 93% sensitivity and specificity rates, respec -\ntively ( Table 6).\nDiscussion\nEndometriosis is a condition estimated to affect \n190 million reproductive-aged women worldwide, with \n\nCirugía y Cirujanos (Eng). 2024;92(1)\n108\na prevalence of colorectal involvement of 8% up to \n12%, accounting for approximately 19 million women \nin this age group 2. Colorectal complications in patients \nwith endometriosis are challenging for the medical \nteam, requiring the availability of special resources \nincluding human expertise (experienced pelvic \nsurgeon, urologist, and general or colorectal surgeon) \nand material resources (advanced laparoscopic \nequipment and instrumentation with intestinal \nendographe).\nTherefore, preoperative management planning is \ncrucial, based on the patient’s clinical presentation, \nincluding bimanual, rectal, and speculum examination, \nsupported by diagnostic aids such as transvaginal \nultrasound and occasionally magnetic resonance \nimaging with rectal and vaginal contrast 9.\nCurrently, the most widely used classification for \nendometriosis is the Enzian classification, which \nspecifically considers only the size of the lesion \n(C1 = 1 cm, C2 = 1-2 cm, and C3 > 3 cm) 10. However, \nupon analyzing the international literature for this study \non 16 846 patients, we found that the surgical \nmanagement decision-making process for the surgeon \ninvolves other factors besides the size of the nodule, \nsuch as the number and depth of lesions, the presence \nor absence of intestinal lumen obstruction, the opening \nof genital, urinary, and digestive tracts in the same \nsurgical act, intraoperative blood loss, history of \nprevious surgeries for endometriosis, the patient’s \noverall health status, specific surgical risk, and the \npossibility of clinically relevant disease recurrence. \nTherefore, we decided to include these factors in a \nclassification system we coined THS (tumor or \nendometrioma characteristics, the patients’ medical \nhistory and observations during surgery)\nWe categorized our patients into 3 stages of disease \n(limited, intermediate, and advanced) and tested the \nstaging classification in a group of patients \nretrospectively treated at Instituto Nacional \nPerinatología from January 2017 through April 2023. \nWe found a strong correlation within our group between \nhigh THS scale values (advanced colorectal \nendometriotic disease) and the presence of \ncomplications requiring subsequent surgical \nmanagement. Based on this correlation, we suggest a \nstaged surgical management scheme:\n– For all stages:\n•\t Management in centers experienced in the \nmanagement of endometriosis.\n•\t Preoperative definition of Enzian and THS \nstage as accurately as possible based on \nexperience and available institutional resources \n(physical and bimanual vaginal examination \nwith speculoscopy and transvaginal ultrasound, \nsupplemented, if necessary, with magnetic \nresonance imaging with rectal and vaginal \ncontrast).\n•\t Appropriate informed consent. Do not operate \nif the patient does not agree and is not aware \nof the benefits and risks of the procedure, or if \nthe risks due to comorbidities outweigh the \nexpected benefits.\n•\t Availability of complete human team \n(gynecological, general, urological, and \ncolorectal surgeons) and technical equipment \nto address unforeseen events (staplers, blood \nproducts, etc.)\n•\t Preoperative intestinal preparation.\n– THS 1 stage (limited): local non-transmural \nextirpations or resections.\n– THS 2 stage (intermediate): transmural discoid \nresection. No more than 2 in segments < 10 cm.\n– THS 3 stage (advanced): segmental colon \nresection with anastomosis, preferably without a \nstoma.\nWe believe that the present study contributes to a \nstaged surgical management plan for patients with \ncolorectal endometriosis, in addition to serving as a \nbasis for comparing results between centers and \nopening new avenues for prospective research.\nTable 5. Distribution of patients based on colorectal endometriosis \ndamage\nEnzian THS\nStage Patients Stage Patients\nC1 17 1 8\nC2 1 2 6\nC3 1 3 5\nTable 6. 2 × 2 table for the sensitivity and specificity of THS 3 and \nsurgical complications \nCurrent complication Absent complication\nPresent THS 3 4 1\nAbent THS 3 1 13\nSensitivity: 80%.\nSpecificity: 93%.\n\nA. Cepeda-Silva et al. Colorectal endometriosis. Treatment\n109\nConclusions\nColorectal endometriosis is a common condition \nthat requires a planned and comprehensive approach \nto reduce complications from overtreatment or subop -\ntimal management, which should be based on a good \npreoperative diagnosis including comprehensive \nphysical examination, bimanual examination, digital \nrectal examination, and speculoscopy, complemented \nby transvaginal ultrasound and sometimes magnetic \nresonance imaging with rectal and vaginal contrast.\nCurrently, the most widely used classifications for \nendometriosis, such as Enzian, especially for colorectal \ninvolvement, only consider the size of the nodule, which \nwe believe to be insufficient for surgical decision-\nmaking. Therefore, we propose a classification that \nconsiders a more comprehensive approach based on \nthe patient’s history, nodule characteristics, and \nintraoperative conditions.\nIn our patients, advanced endometriotic disease de -\ntermined by THS classification positively correlated with \nthe presence of complications, so we consider the pres-\nent staged classification for colorectal endometriosis an \napproach to achieve disease staging by organizing the \ninternational experience already available in the man -\nagement of these patients, allowing us to define stage-\nbased treatments and compare results between \nhospitals.\nDue to its limitations, this study should pave the way \nfor prospective studies that, with appropriate statisti -\ncal analysis, should allow us to refine the scale and \nincrease its utility, to offer patients the best option for \npersonalized surgical management and perform \nplanned interventions with a multidisciplinary team in \na single procedure.\nAcknowledgments\nThe authors would like to thank Dr. Ana Cristina Artea-\nga Gómez, Dr. Minerva Guedea Téllez, and Brenda Sán-\nchez Ramírez for their help reviewing the text, Dr. Myrna \nSouraye Godínez Enríquez for her support and advice in \ninitiating the project, and Dr.  Luis Hernández López for \nhis support in making this work possible.\nFunding\nNone declared.\nConflicts of interest\nNone declared.\nEthical disclosures\nProtection of human and animal subjects.  The \nauthors declare that no experiments were performed \non humans or animals for this study.\nConfidentiality of data.  The authors declare that \nthey have followed the protocols of their work center \non the publication of patient data.\nRight to privacy and informed consent.  The au -\nthors have obtained approval from the Ethics Commit -\ntee for analysis and publication of routinely acquired \nclinical data and informed consent was not required \nfor this retrospective observational study.\nUse of artificial intelligence for generating \ntext. The authors declare that they have not used \nany type of generative artificial intelligence for the \nwriting of this manuscript, nor for the creation of \nimages, graphics, tables, or their corresponding \ncaptions.\nReferences\n 1. Becker CM, Bokor A, Heikinheimo O, Horne A, Jansen F, Kiesel L. \nESHRE Guideline: endometriosis. Hum Reprod Open. 2022;2022:hoac009.\n 2. 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The #Enzian classification: a comprehensive non‐invasive and \nsurgical description system for endometriosis. Acta Obstet Gynecol \nScand. 2021;100:1165-75.","source_license":"CC0","license_restricted":false}