{"paper_id":"d7718372-1bf8-411b-b372-5303b5ebc533","body_text":"j coloproctol (rio j). 2 0 1 6; 3 6(2) :69–74\nwww.jcol.org.br\nJournal of\nColoproctology\nOriginal Article\nCorrelation of the three-dimensional ultrasound\nfindings  with pathology in patients with deep\npelvic infiltrating  endometriosis submitted to\nsurgery/H22845\nMaria Cecilia Lunardelli da Silva a, Doryane Maria dos Reis Lima a,b,∗,\nUnivaldo Etsuo Sagaeb,c,d\na Faculdade Assis Gurgacz (FAG), Cascavel, PR, Brazil\nb Universidade Federal do Ceará (UFC), Fortaleza, CE, Brazil\nc Universidade de São Paulo (USP), São Paulo, SP , Brazil\nd Universidade Estadual do Oeste do Paraná (UNIOESTE), Foz do Iguac¸u, PR, Brazil\na r t i c l e i n f o\nArticle history:\nReceived 12\n August 2013\nAccepted\n 3 March 2015\nAvailable\n online 21 March 2016\nKeywords:\nEndometriosis\nCorrelation\nUltrasound\nPathology\nDiagnosis\na b s t r a c t\nObjective: This study aims to correlate the findings  of the three-dimensional anorectal ultra-\nsonography\n (3D-AUS) with pathological findings  in patients with deep pelvic infiltrating\nendometriosis.\nMethods:\n Prospective study of a series of 40 patients with deep pelvic infiltrating  endometri-\nosis\n diagnosed by three-dimensional anorectal ultrasonography and who were submitted to\na\n laparoscopy. The specimens were examined histologically and compared with the results\nof\n the three-dimensional anorectal ultrasonography. The research was conducted between\nMarch 2008 and March 2011.\nResults:\n The results of the examinations were: 72.5% of patients (n = 29) with endometriosis,\n12.5%\n (n = 5) with nonspecific  chronic inflammatory  reaction, 5% (n = 2) with nonspecific\nfibrous\n tissue, 2.5% (n = 1) with adenomyoma, 2.5% (n = 1) with colonic mucosa with foci\nof\n recent hemorrhage, edema of lamina propria and superficial  erosions, 2.5% (n = 1) with\nhyperplasia\n of lymphoid follicles, and the remaining 2.5% (n = 1) with peritoneal tissue within\nnormal\n limits.\nConclusion:\n We conclude that the use of three-dimensional anorectal ultrasonography in\npatients\n with deep pelvic infiltrating  endometriosis aid in the diagnosis of rectal lesions,\nwhen\n compared with the pathological findings  of surgical specimens.\n©\n 2016 Sociedade Brasileira de Coloproctologia. Published by Elsevier Editora Ltda. This\nis\n an open access article under the CC BY -NC-ND license\n(http://creativecommons.org/licenses/by-nc-nd/4.0/).\n/H22845This study was conducted in Hospital Genesis, Gastroclínica Cascavel, Cascavel, PR, Brazil and in the Faculdade Assis Gurgacz (FAG),\nCascavel,\n PR, Brazil.\n∗ Corresponding author.\nE-mail:\n doryane@gmail.com (D.M. dos Reis Lima).\nhttp://dx.doi.org/10.1016/j.jcol.2015.03.005\n2237-9363/© 2016 Sociedade Brasileira de Coloproctologia. Published by Elsevier Editora Ltda. This is an open access article under the CC\nBY -NC-ND\n license (http://creativecommons.org/licenses/by-nc-nd/4.0/).\nArticle published online: 2021-02-17\n\n70 j coloproctol (rio j). 2 0 1 6; 3 6(2) :69–74\nCorrelac¸ão dos achados da ultrassonografia  tridimensional com o\nanatomopatológico\n em pacientes com endometriose pélvica infiltrativa\nprofunda\n submetidos a tratamento cirúrgico\nPalavras-chave:\nEndometriose\nCorrelac¸ã o\nUltrassonografia\nAnatomopatológico\nDiagnóstico\nr e s u m o\nObjetivo: Este estudo visa correlacionar os achados da ultrassonografia  tridimensional com\nos\n achados anatomopatológicos em pacientes com endometriose pélvica infiltrativa  pro-\nfunda submetidos a tratamento cirúrgico.\nMétodos:\n Estudo prospectivo de uma série de 40 pacientes com endometriose pélvica infil-\ntrativa\n profunda diagnosticados pela USR-3D e submetidos à videolaparoscopia. As pec¸a s\ncirúrgicas\n foram analisadas histologicamente e comparadas com os resultados das USR-3D.\nA\n pesquisa foi desenvolvida\n entre marc¸o  de 2008 a marc¸o  de 2011.\nResultados: Os resultados dos estudos histopatológicos foram: 72,5% das pacientes (n = 29)\ncom\n endometriose, 12,5% (n = 5) com reac¸ã o inflamatória  crônica inespecífica,  5% (n = 2) com\ntecido\n fibroso  inespecífico,  2,5% (n = 1) com adenomioma, 2,5% (n = 1) com mucosa colônica\ncom\n presenc¸a  de focos de hemorragia recente, edema de lâmina própria e erosões superfi-\nciais,\n 2,5% (n = 1) com hiperplasia de folículos linfoides e o restante, 2,5% (n = 1), com tecido\nperitoneal\n dentro dos limites da normalidade.\nConclusão:\n Conclui-se, portanto que a ultrassonografia  anorretal tridimensional em\npacientes\n portadoras de endometriose pélvica infiltrativa  profunda ajuda no diagnóstico\nde\n lesões retais,\n quando essa técnica é comparada com os achados anatomopatológicos das\npec¸a s cirúrgicas.\n© 2016 Sociedade Brasileira de Coloproctologia. Publicado por Elsevier Editora Ltda. Este\né\n um artigo Open Access sob a licença de CC BY -NC-ND\n(http://creativecommons.org/licenses/by-nc-nd/4.0/).\nIntroduction\nEndometriosis is characterized by the presence of tissue simi-\nlar to the endometrium outside the uterus, leading to a chronic\ninflammatory  reaction.1 The estimated prevalence of endo-\nmetriosis is 5–15%  of all women of childbearing age.2,3 Among\nwomen\n suffering from infertility, 20–68%  show an associated\nendometriosis.4 Studies report that 15–30%  of women with\nendometriosis have profound infiltrative  disease.5,6 Colorectal\ninvolvement is present in about 5–10%  of cases of the disease\nin its deep infiltrative  form.7\nPhysical examination, even during menstruation, has a\nlimited\n ability to diagnose and quantify the disease.8 The\ndiagnosis is usually established by laboratory tests, espe-\ncially by imaging techniques such as transvaginal ultrasound\n(TVUS),9–12 anorectal ultrasonography (AUS),13,14 endoscopic\ntransrectal ultrasonography (ETRUS),9,15 magnetic resonance\nimaging (MRI),10 computed tomography (CT),16 and barium\nenema.17 The imaging procedure must be able to indicate the\nnumber of foci present, the size and depth of the lesion, as\nwell as its distance from the anal margin.18,19 Many studies\nhave recently shown that preoperative AUS may be useful\nin predicting rectal infiltration  in patients with deep pelvic\nendometriosis,18,20 and in the surgical decision making in\nfavor\n of an intestinal resection.13\nWith the recent development of ultrasound equipment\nwith multiplanar vision and the acquisition of automatic\nimages, the mode that uses the three-dimensional probe was\nestablished in the anorectal complex assessment for the study\nof benign and malignant diseases,21–27 making it possible to\nevaluate and accurately measuring the longitudinal length\nof lesions and their distance to the sphincter muscles; thus,\nadditional information necessary for choosing the therapeutic\napproach can be obtained.\nTo date, surgery remains as the most successful option for\ntreating endometriosis, even in the face of the possible limi-\ntations, complications and sequelae.28\nThis study intends to correlate the findings  of three-\ndimensional ultrasonography\n with histopathological studies\nin\n patients with deep pelvic infiltrating  endometriosis submit-\nted to surgery.\nMaterials and methods\nThis is a prospective study of a series of 40 patients with sus-\npected\n deep pelvic infiltrating  endometriosis (DPIE) referred\nfrom the Gynecology outpatient clinic to the Coloproctology\nService outpatient clinic, Hospital Genesis/Gastroclínica Cas-\ncavel, in the period between March 2008 and March 2011. The\npatients had complaints such as dyspareunia, rectal pain, pain\nin right iliac fossa (RIF), constipation and/or tenesmus.\nThe patients were then submitted to a three-dimensional\nanorectal ultrasonography (3D-AUS) for evaluation. Those\nwomen with suspicious findings  of rectal involvement by 3D-\nAUS were referred to videolaparoscopic surgery performed by\na multidisciplinary team involving gynecologists and colorec-\ntal surgeons with experience in videolaparoscopy. The surgical\nspecimens were analyzed histologically and compared with\nthe results of 3D-AUS. Some patients had undergone hormone\ntreatment previous to 3D-AUS.\n\n\nj coloproctol (rio j). 2 0 1 6; 3 6(2) :69–74  71\n3D-AUS was performed by a colorectal surgeon with 2-year\nexperience in this type of exam. The device used in this study\nwas a BK Medical (Herlev, Denmark), with Pro-Focus probe\nwith transducer with 360, model 2050 rotatory with frequency\nof 9–16  MHz, with a focal length of 2.8–6.2  cm, with a 50 s auto-\nmatic scan, resulting in a 3-D cube displayed as a multiple\nsequence of axial images, as a cube image. For this exami-\nnation, the patients were positioned in left lateral decubitus,\nafter a rectal enema performed 2 h before the examination and\nusing a digital rectal examination, all of them under anesthetic\nsedation and without using a rigid rectoscope. Four automatic\nscans were performed in order to evaluate the anal canal,\nanorectal junction, and the lower and middle aspects of the\nrectum, respectively. The images obtained were evaluated in\nthe axial and longitudinal planes and, if needed, were associ-\nated with the diagonal plane. After completion of the scans,\nstill images\n have been properly analyzed. We considered as\nnormal\n those patients with no change in perirectal fat, and\nwith intact rectal wall layers.\nThe characteristics of the ultrasound lesions were as fol-\nlows: size of the endometriotic focus; the distance from this\nfocus to the puborectal muscle, and which layers of the\nintestinal\n wall that were affected. These findings  allowed the\nsurgeon to choose his/her surgical approach. The analyzed\nhistopathological criteria were: areas of fibrosis  associated\nwith endometrial tissue, characterized by glands and stroma\nwell\n differentiated\n and without atypia.\nPatients with deep pelvic infiltrating  endometriosis con-\nfirmed  by 3D-AUS who underwent videolaparoscopy by the\nteams of gynecologic surgery and of colorectal surgery, and\nwho subsequently obtained histopathological results, were\nincluded in this study. Patients with deep endometriosis who\nrefused the examination, patients who underwent the exam-\nination, but with negative results, patients who had a positive\nresult of 3D-AUS but were not submitted to laparoscopy, and\npatients who refused to participate in the study were excluded\nfrom the study.\nThe study was approved by the Ethics Committee in\nResearch of Faculdade Assis Gurgacz (protocol 232/2012).\nResults\nThe mean age of patients in this study was 35.1 (21–47)  years.\nOf the 40 patients evaluated, 13 (32.5%) had as main indica-\ntion an endometriosis, and had previously been diagnosed\nand treated with hormone. Nine patients (22.5%) had clini-\ncal pain when defecating in the menstrual period, associated\nwith dysmenorrhea and dyspareunia. Seven patients (17.5%)\nhad abdominal complaints of pain in the lower abdomen, with\nworsening\n during menstruation, in association with dyspare-\nunia. Five patients (12.5%) reported only dysmenorrhea. Four\npatients (10%) reported infertility and dyspareunia, and two\nother patients (5%) reported pain in the lower abdomen, dys-\npareunia and constipation.\nThe characteristics of 3D-AUS lesions are round or tri-\nangular,\n irregular, heterogeneous hypoechoic masses, with\na\n behavior of an invasion of the rectum into the perirectal\nintestinal lumen (located only in the perirectal fat) (Fig. 1A).\nSuch\n finding  was found 25 patients (62.5%) in this study, or\nalready invading at least the muscular layer of the rectum,\nwhich was observed in 15 patients (37.5%) (Fig. 1B). The mean\nsize of the foci was 2.1 (0.5–4)  cm, the average distance from\nthe focus to the anal sphincter was 4.2 (1.5–6)  cm (Fig. 2A and\nB).\nThree types of surgery were carried out: 20 patients (50%)\nunderwent excision of endometriosis foci, 13 patients (32.5%)\nwere treated with rectosigmoidectomy, and 7 patients (17.5%)\nunderwent a segmental colectomy with a stapled anastomo-\nsis. Decisions were based on 3D-AUS and laparoscopy findings.\nThe surgical specimens were sent for histopathological eval-\nuation by 2 pathologists.\nThe histopathological results were as follows: 72.5% of\npatients with endometriosis, 12.5% with nonspecific  chronic\ninflammatory  reaction, 5% with nonspecific  fibrous  tissue,\n2.5% with adenomyoma, 2.5% with colonic mucosa with foci of\nrecent hemorrhage,\n edema of lamina propria and superficial\nerosions,\n 2.5% with hyperplasia of lymphoid follicles, and the\nremaining 2.5% with peritoneal tissue within normal limits.\nDiscussion\nIn cases of deep endometriosis, is not always that the clini-\ncal treatment is effective, due to the high rate of occurrence\nof fibrous  lesions that are less likely to respond to hormonal\ntherapy.6 Surgical treatment may be the only appropriate ther-\napeutic\n option for severe endometriosis.29 However, if the\nlesions have not been previously diagnosed, these patients\nwill undergo an incomplete surgical treatment, and often\nthere may be a need for more than one surgery. There are\nseveral\n modalities for staging these lesions; the more accu-\nrate ones are the nuclear magnetic resonance imaging and\ntransvaginal ultrasonography with preparation.30 AUS has\nbeen used as an alternative to these modalities in the eval-\nuation of rectal infiltration  by endometriosis.31\nThe purpose of this study was to emphasize the impor-\ntance of the three-dimensional anorectal transducer in the\nposterior pelvic assessment in patients with endometri-\nosis. Due to the limitation to the examination of images in\nthe longitudinal plane, a transducer was developed which\nallows three-dimensional reconstruction after the capture of\nimages in two-dimensional mode. With AUS together with\nthree-dimensional mode used preoperatively, the surgeon\ncan evaluate the lesions in multiple planes and also deter-\nmine\n accurately the longitudinal length and the distance\nwith respect to the sphincter muscles. Thus, critical infor-\nmation for choosing the therapeutic approach is obtained.\nThe diagnostic accuracy provided by 3D-AUS is of fundamen-\ntal importance for patients with endometriosis, especially for\nyoung women who are seeking fertility, because this modality\nprevents countless surgeries.\nMRI is the most complete test for the staging of deep pelvic\nlesions; however, this method is less effective for the diagnosis\nof posterior pelvic endometriosis, because it do not accurately\nassesses the infiltration  of the rectal wall layers.18,20 Magnetic\nresonance\n imaging has a sensitivity, specificity  and accu-\nracy for the diagnosis of colorectal endometriosis of 88–90.9%\n77.8–97.8%  and 94.9%, respectively, demonstrated by several\nauthors.32 But MRI is a method that is only available in large\n\n\n72 j coloproctol (rio j). 2 0 1 6; 3 6(2) :69–74\nRectal\nMuscle lesion\nA B\nFig. 1 –  Injuries analyzed by 3D-AUS (axial cuts). (A) Lesion involving perirectal tissue and (B) a lesion involving the rectal\nmuscle\n layer.\ncities and, in addition, is an expensive examination. Ser-\nvices that do not have MRI may have computed tomography;\nhowever, this modality proves to be more difficult  in distin-\nguishing and delimiting pelvic organs and injuries. As a rule,\nMRI provides less important information in comparison to\nthose obtained with a transvaginal ultrasound performed by\nan experienced professional.33,34\nThe development\n of imaging methods provided important\nqualitative and quantitative contributions to the diagnosis\nand thus to define  the most appropriate therapeutic approach.\nThus, there is a tendency in favor of the incorporation of these\ntests in the preoperative routine.\nThe staging of the lesions with 3D-AUS preoperatively\nfavors the orientation with respect to the surgical procedure to\nbe adopted in each case. Thus, one can predict the need, or not,\nof an approach and/or intestinal resection, as well as the pos-\nsibility of a protective ostomy. With 3D-AUS, the surgeon will\nobtain\n important information, such as the distance from the\nendometriotic lesion to the anal sphincter, and whether in this\nlesion there is perirectal fat or rectum invasion. In the other\nhand, this modality can define  if the invasion affects muscle\nand/or, submucosal layer, or rectal mucosa. Thus, it may be\nsuggested that in cases of foci greater than 2 cm in length or\noccurring in\n more\n than\n one third of rectal circumference, it\nwould\n be less likely a local economic resection.\nAmong patients diagnosed with endometriosis, the corre-\nlation\n of the pathology report with 3D-AUS findings  occurred\nin 72.5% of 40 patients undergoing surgery for removal of\nlesions suggestive of endometriosis and detected by this\nexamination.\nMicroscopically, endometriosis is defined  by the pres-\nence of typical endometrial glands and stroma, deposition of\nhemosiderin, erythrocytes, and macrophages, and fibrous  tis-\nsue containing inflammatory  cells. The fact of not having a\ncorrelation in all cases may be related to a previous medical\ntreatment, or by being older lesions, with scars and peritoneal\nretraction.\n The anatomopathological correlation is generally\nobserved in active lesions.35 Pathological examination of the\nlesions should be used as an auxiliary method of diagno-\nsis, by not being positive in all cases. The main limitation of\nour\n study arises from the need for training pathologists, in\norder to review the surgical pieces of endometriosis for the\nLower rectumA B\nUterus\nPuborectal\nPuborectal\nMuscle lesion\n1\n2\n1\nFig. 2 –  Injuries analyzed by 3D-AUS (sagittal section). (A) The distance from the focus to sphincter apparatus and (B)\ndetermination of longitudinal size of the endometriotic focus.\n\n\nj coloproctol (rio j). 2 0 1 6; 3 6(2) :69–74  73\ndefinitive  diagnosis. Another limiting factor is the fact that\nours is a referral service and that, moreover, many of the\npatients had already undergone medical treatment and/or\nsurgery. Thus, the resulting injuries lost their glandular his-\ntological characteristic.\nConclusion\nThus, we can conclude that the use of three-dimensional\nanorectal ultrasonography in patients with deep pelvic infil-\ntrating endometriosis aid in the diagnosis of rectal lesions,\nwhen compared with the pathological findings  of surgical\nspecimens.\nConflicts  of interest\nThe authors declare no conflicts  of interest.\nr e f e r e n c e s\n1. Kennedy S, Bergqvist A, Chapron C, D’Hooghe T, Dunselman\nG,\n Greb R, et al. ESHRE guideline for the diagnosis and\ntreatment\n of endometriosis. Hum Reprod. 2005;20:2698–704.\n2. Leyendecker G, Herbertz M, Kunz G, Mall G. Endometriosis\nresults\n from the dislocation of basal endometrium. Hum\nReprod.\n 2002;17:2725–36.\n3. Leyendecker G, Kunz G, Noe M, Herbertz M, Mall G.\nEndometriosis:\n a dysfunction and disease of the archimetra.\nHum\n Reprod Update. 1998;4:752–62.\n4. Koninckx PR, Meuleman C, Demeyere S, Lesaffre E, Cornillie\nFJ.\n Suggestive evidence that pelvic endometriosis is a\nprogressive\n disease, whereas deeply infiltrating\nendometriosis\n is associated with pelvic pain. Fertil Steril.\n1991;55:759–65.\n5. Keckstein\n J, Ulrich U, Kandolf O, Wiesinger H, Wustlich M.\nLaparoscopic therapy of intestinal endometriosis and the\nranking of drug treatment. Zentralbl Gynako. 2003;125:259–66.\n6. Fauconnier A, Chapron C. Endometriosis and pelvic pain:\nepidemiological\n evidence of the relationship and\nimplications.\n Hum Reprod Update. 2005;11:595–606.\n7. Balleyguier C, Chapron C, Dubuisson JB, Kinkel K, Fauconnier\nA,\n Vieira M, et al. 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