{"paper_id":"798c4a46-7a73-4605-b1c8-4bb85526dde9","body_text":"Editorial\nSurgical Classi fication of Endometriosis\nJoão Nogueira Neto 1 Mauricio Simões Abrão 2,3 Eduardo Schor 4 Julio Cesar Rosa-e-Silva 5\n1 Department of Gynecology and Obstetrics, Faculdade de Medicina,\nUniversidade Federal do Maranhão, São Luis, MA, Brazil\n2 Department of Gynecology, Bene ficência Portuguesa de São Paulo,\nSão Paulo, SP , Brazil\n3 Department of Gynecology and Obstetrics, Faculdade de Medicina,\nUniversidade de São Paulo, São Paulo, SP, Brazil\n4 Department of Gynecology, Escola Paulista de Medicina,\nUniversidade Federal de São Paulo, São Paulo, SP, Brazil\n5 Department of Gynecology and Obstetrics, Faculdade de Medicina,\nRibeirão Preto, Universidade de São Paulo, Ribeirão Preto, SP , Brazil\nRev Bras Ginecol Obstet 2022;44(8):737 –739.\nEndometriosis is a chronic, benign, estrogen-dependent and\nmultifactorial gynecological disease that mainly affects\nwomen of reproductive age. It can be de fined by the\npresence of tissue that resembles the endometrial gland\nand/or stroma outside the uterus, predominantly although\nnot exclusively, in the female pelvis. 1 It is estimated that\n10% of women of reproductive age have this disease, which\nrepresents around 176 million women worldwide, generat-\ning direct costs to health systems and indirect costs due to\nreduced productivity, in addition to physical and psycho-\nlogical suffering secondary to pain and infertility, with\nconsequent loss of quality of life.\n2\nGiven the many difficulties imposed by endometriosis, it has\nbeen extensively researched in recent decades.3,4 Its classifica-\ntion is one of the dif ficulties faced. A reproducible, easy-to-\napply, and well-organized classification system is needed not\nonly to clarify communication between clinicians, but also to\nstandardize the optimal treatment strategy and clinical trials.2,5\nThe National Specialized Commission on Endometriosis of\nthe Brazilian Federation of Gynecology and Obstetrics Asso-\nciations – FEBRASGO analyzed the different forms of classi-\nfication chosen by the World Endometriosis Society (WES)\n5\nwith the objective to standardize the current classi fication\nnationwide for Brazilian services that diagnose and treat this\ndisease.\nAs a single classi fication that evaluates all possible man-\nifestations of endometriosis is lacking, four classi fications\nwere standardized, among which: the revised classi fication\nof the American Society for Reproductive Medicine (rASRM),\nthe ENZIAN classi fication, the Endometriosis Fertility Index\n(EFI) and the American Association of Gynecologic Laparos-\ncopists (AAGL) classi fication.\n2,6–10\nThe World Endometriosis Society (WES) published the\nfirst international consensus on the classi fication of endo-\nmetriosis using a rigorous methodology in 2017. 5 The lack of\na classi fication comprising all aspects of this disease led to\nthe proposal of a combination of the most relevant classi-\nfications that could be used by all professionals working with\nwomen with endometriosis, from which surgeons can select\nthe appropriate components and ensure its documentation\nin patients ’ records.5\nThe initial ASRM Classi fication proposed a single ap-\nproach in 1979. 6 The endometriosis stage is derived from a\ncumulative score according to the location and size of lesions\nobserved during surgery.\n2,6 The staging system underwent\nmodifications in 1996 and is currently divided into I (1-5\npoints, minimal), II (6-15 points, mild), III (16-40 points,\nmoderate) and IV (greater than 40 points, severe).\nThe advantages of this classi fication are its global accep-\ntance, being widely used, easy application and the fact of\nhelping patients to easily understand the stage of their\ndisease.\n2\nAmong the disadvantages are differences between histo-\nlogically diagnosed endometriosis and the stage made by\nvisualization, its low reproducibility, low correlation be-\ntween symptoms and its staging, not assessing the severity\nof pain and infertility, and not considering the presence of\ndeep in filtrating endometriosis in areas such as uterosacral\nligaments, bladder, vagina and intestine.\n2,6,11,12\nThe ENZIAN classi fication was introduced in 2005 to\ndetermine the extent of deep endometriosis during surgical\ntreatment, complementing the rASRM classi fication. This\nclassification was already revised in 2010 and 2011 to correct\nits overlap with the rASRM and make it easier to use.\n2,7 In\nAddress for correspondence\nJoão Nogueira Neto, MD, Praça\nGonçalves Dias, 65020-240,\nC e n t r o ,S ã oL u í s ,M A ,B r a z i l\n(e-mail: joao.nn@gmail.com).\nDOI https://doi.org/\n10.1055/s-0042-1755588.\nISSN 0100-7203.\n© 2022. Federação Brasileira de Ginecologia e Obstetrícia. All rights\nreserved.\nThis is an open access article published by Thieme under the terms of the\nCreative Commons Attribution License, permitting unrestricted use,\ndistribution, and reproduction so long as the original work is properly cited.\n(https://creativecommons.org/licenses/by/4.0/)\nThieme Revinter Publicações Ltda., Rua do Matoso 170, Rio de\nJaneiro, RJ, CEP 20270-135, Brazil\nTHIEME\nEditorial 737\nArticle published online: 2022-09-08\n\n2021, it was revised again to introduce the evaluation of the\nforms of peritoneal and ovarian endometriosis, and the\nassessment of tubal permeability through chromotubation\nand secondary adhesions.\n13 This last review aimed to pro-\npose a logical anatomical classi fication for use by a non-\ninvasive method (magnetic resonance imaging and pelvic\nultrasound), preoperatively, enabling a more adequate sur-\ngical planning, and intraoperatively, allowing a consistent\nand clear classification of deep endometriosis. Future studies\nare needed to assess its clinical validity, accuracy and\nreproducibility.\n2,13\nThe advantages are that it describes the retroperitoneal\nstructures, can be determined by imaging modality and used\nfor surgical planning, and the location and extent of the\ndisease are associated with the presence and severity of\ndifferent symptoms such as pain.\n2,5,14\nThe following are among the disadvantages: low level of\nglobal acceptance due to its complexity; patients ’ difficulty\nin understanding the classi fication informed given the com-\nplexity of stages and insuf ficient knowledge of pelvic anato-\nmy by lay people; the classi fication will be imprecise if the\nsurgical approach to deep lesions is performed incompletely\nor if the imaging study is not con firmed in the surgical\nprocedure; and finally, even if the classi fication is previously\nmade by imaging modality, there is still no scienti fic evi-\ndence on the usefulness of the classi fication determined by\nimage, although it has great future potential because of the\nincreasing percentage of patients in clinical follow-up of the\ndisease.2\nAnother existing classi fication, the EFI, aims to develop a\nFertility Index in patients with endometriosis, and predict\nthe rate of spontaneous pregnancy in patients with endome-\ntriosis undergoing surgical treatment who will not attempt\nto conceive with assisted reproduction techniques.\n8\nThe EFI system considers historical factors such as age,\nduration of infertility and previous pregnancies associated\nwith intraoperative findings. The functional score indicates\nthe situation of pelvic organs for a possible future spontane-\nous pregnancy. Functional scores are determined by the\nsurgeon and range from 0 to 4 points as follows; absent or\nnonfunctional as 0, severe dysfunction as 1, moderate dys-\nfunction as 2, mild dysfunction as 3, and normal as 4. Not\nonly the minimal functional score, but also other surgical\nfactors such as the rASRM total score and the rASRM endo-\nmetriosis lesion score are included. Finally, the final EFI score\nis calculated by adding the scores from the history and\nsurgical findings that range from 0 to 10 points, with 10\nindicating the best prognosis and 0 the worst prognosis.\n2,8\nThe EFI system has a clear advantage in predicting the\noutcome of pregnancy and re flects the possible future preg-\nnancy rate better than the rASRM classi fication, where a\nscore of 6 or more has better RA results than a score of 5 or\nless.\n2,15,16 This classi fication has already been validated\nexternally numerous times and seems to be an interesting\ntool for patients with endometriosis and infertility.\nHowever, the EFI system has the following disadvantages:\nthe classification score does not correlate with pain, as it was\nnot designed for this purpose; as the lowest function score is\njudged subjectively, the total score may vary by surgeon; it is\nmore complex to use than the rASRM classi fication and the\nENZIAN, as it requires the calculation and sum of scores from\nseveral categories. 2,8 We believe it is interesting and useful\nfor the group of patients with endometriosis and infertility\nand for the purpose of calculating probability of a future\npregnancy.\nIn 2010, the AAGL initiated a project to develop a new\nclassification of endometriosis.\n9 Thirty endometriosis spe-\ncialists were asked to assign scores ranging from 0 to 10\npoints, based on the pain, infertility, and surgical dif ficulty of\npatients with endometriosis. In addition, surgical dif ficulties\nwere categorized into four levels. 9 The visual analogue scale\nscores and infertility history of patients were collected\nbefore surgery for the validation of the scoring system. In\n2012, the AAGL Special Interest Group reported that prelim-\ninary results presented at the AAGL meeting in Las Vegas\nwere encouraging and the AAGL classi fication of endometri-\nosis was found to be related to pain, infertility, and surgical\ndifficulty.\n11\nThe next step was to conduct a prospective multicenter\nstudy with more than 1,500 patients to validate this informa-\ntion. According to its authors, it still requires adjustments and\nimprovements so that it is globally accepted and applied, as\nwell as further investigations and discussions about this new\nclassification. However, initial evaluations concluded that this\nclassification allows the identi fication of objective intra-\noperative findings that reliably discriminate the levels of\nsurgical complexity better than the ASRM staging system,\nand the severity stage correlates with the symptoms of pain\nand infertility with the ASRM stage.\n10 Another interesting\ndata of this classi fication is its easy application in the form\nof an application with the creation of a final version in pdf,\nwhich facilitates storage and a copy for patients (https://apps.\napple.com/us/app/aagl-endo-classification/id1592383297 or\nhttps://play.google.com/store/apps/details?id¼ br.com.medi-\ncinia.aagl&hl¼ en&gl ¼ US). AAGL, as one of the largest global\nMedical Societies in the field of Gynecological Surgery, is\nputting efforts to test the use of the classi fication even before\nsurgery, by imaging methods.\nIn conclusion, the search for better care for patients with\nendometriosis is constant given the great implications that\nthis disease brings to physical, social, sexual, reproductive\nand psychological health. Special attention to its classi fica-\ntion is needed so we can standardize it globally. In this sense,\nwe believe the classification recently proposed by AAGL may\nhave all the necessary requirements for its wide future use.\nConflicts of Interest:\nNone to declare.\nReferences\n1 Federação Brasileira das Associações de Ginecologia e Obstetrícia.\nEndometriose. São Paulo: FEBRASGO; 2021. (Protocolo\nFEBRASGO-Ginecologia, no. 78/Comissão Nacional Especializada\nem Endometriose)\n2 Lee SY, Koo YJ, Lee DH. Classi fication of endometriosis. Yeungnam\nUniv J Med. 2021;38(01):10 –18. Doi: 10.12701/yujm.2020.00444\nRev Bras Ginecol Obstet Vol. 44 No. 8/2022 © 2022. Federação Bra sileira de Ginecologia e Obste trícia. All rights reserved.\nSurgical Classification of Endometriosis Nogueira Neto et al.738\n\n\n3 Dunselman GA, Vermeulen N, Becker C, et al; European Society of\nHuman Reproduction and Embryology. ESHRE guideline: man-\nagement of women with endometriosis. Hum Reprod. 2014;29\n(03):400–412. Doi: 10.1093/humrep/det457\n4 Keckstein J, Becker CM, Canis M, et al; Working group of ESGE,\nESHRE, and WES. Recommendations for the surgical treatment of\nendometriosis. Part 2: deep endometriosis. Hum Reprod Open.\n2020;2020(01):hoaa002. Doi: 10.1093/hropen/hoaa002\n5 Johnson NP, Hummelshoj L, Adamson GD, et al; World Endome-\ntriosis Society Sao Paulo Consortium. World Endometriosis Soci-\nety consensus on the classi fication of endometriosis. Hum\nReprod. 2017;32(02):315 –324. Doi: 10.1093/humrep/dew293\n6 Hornstein MD, Gleason RE, Orav J, et al. The reproducibility of the\nrevised American Fertility Society classi fication of endometriosis.\nFertil Steril. 1993;59(05):1015 –1021\n7 Tuttlies F, Keckstein J, Ulrich U, et al. [ENZIAN-score, a classi fica-\ntion of deep in filtrating endometriosis]. Zentralbl Gynäkol. 2005;\n127(05):275–281. Doi: 10.1055/s-2005-836904 German.\n8 Adamson GD, Pasta DJ. Endometriosis fertility index: the new,\nvalidated endometriosis staging system. Fertil Steril. 2010;94\n(05):1609–1615. Doi: 10.1016/j.fertnstert.2009.09.035\n9 Chapron C, Abrao MS, Miller CE. Endometriosis classi fications\nneed to be revisited: a new one is arriving. NewsScope.. 2012;26\n(04):9–10\n10 Abrao MS, Andres MP , Miller CE, et al. AAGL 2021 Endometriosis\nClassification: an anatomy-based surgical complexity score. J Min-\nim Invasive Gynecol. 2021;28(11):1941 –1950.e1. Doi: 10.1016/j.\njmig.2021.09.709\n11 Fernando S, Soh PQ, Cooper M, et al. Reliability of visual diagnosis\nof endometriosis. J Minim Invasive Gynecol. 2013;20(06):\n783–789. Doi: 10.1016/j.jmig.2013.04.017\n12 Vercellini P, Trespidi L, De Giorgi O, Cortesi I, Parazzini F, Cro-\nsignani PG. Endometriosis and pelvic pain: relation to disease\nstage and localization. Fertil Steril. 1996;65(02):299 –304\n13 Keckstein J, Saridogan E, Ulrich UA, et al. The #Enzian classi fica-\ntion: A comprehensive non-invasive and surgical description\nsystem for endometriosis. Acta Obstet Gynecol Scand. 2021;100\n(07):1165–1175. Doi: 10.1111/aogs.14099\n14 Montanari E, Dauser B, Keckstein J, Kirchner E, Nemeth Z, Hudelist\nG. Association between disease extent and pain symptoms in\npatients with deep in filtrating endometriosis. Reprod Biomed\nOnline. 2019;39(05):845 –851. Doi: 10.1016/j.rbmo.2019.06.006\n15 Zeng C, Xu JN, Zhou Y, Zhou YF, Zhu SN, Xue Q. Reproductive\nperformance after surgery for endometriosis: predictive value of\nthe revised American Fertility Society classi fication and the\nendometriosis fertility index. Gynecol Obstet Invest. 2014;77\n(03):180–185. Doi: 10.1159/000358390\n16 Wang W, Li R, Fang T, et al. Endometriosis fertility index score\nmaybe more accurate for predicting the outcomes of in vitro\nfertilisation than r-AFS classi fication in women with endometri-\nosis. Reprod Biol Endocrinol. 2013;11:112. Doi: 10.1186/1477-\n7827-11-112\nRev Bras Ginecol Obstet Vol. 44 No. 8/2022 © 2022. Federação Bras ileira de Ginecologia e Obstetrícia. All rights reserved.\nSurgical Classification of Endometriosis Nogueira Neto et al. 739","source_license":"CC-BY-4.0","license_restricted":false}