{"paper_id":"a62ab4bc-d563-47f2-a05c-9f3c7bd94c57","body_text":"Elsadawy and Ali  Egypt J Radiol Nucl Med  (2023) 54:188 \nhttps://doi.org/10.1186/s43055-023-01130-w\nRESEARCH Open Access\n© The Author(s) 2023, corrected publication 2023. Open Access  This article is licensed under a Creative Commons Attribution 4.0 \nInternational License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you \ngive appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes \nwere made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated \notherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not \npermitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To \nview a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/.\nEgyptian Journal of Radiology\nand Nuclear Medicine\nMRI of Endometriosis: Single institute \nexperience including MRI classification \nand Laparoscopic correlation with ENZIAN \nclassification\nMomena Essam Ibrahim Elsadawy1*   and Heba Ibrahim Ali1 \nAbstract \nBackground Endometriosis is a chronic gynecological condition affecting women of reproductive age and may \ncause pelvic pain and infertility. MRI is the best imaging technique for mapping and preoperative staging of endome-\ntriosis as it provides a tool for the assessment of deep infiltrating endometriosis. The aim of this study was to evalu-\nate the role of magnetic resonance imaging (MRI) in detection and characterization of endometriosis in correlation \nbetween it and the laparoscopic findings according to ENZIAN classification.\nMethods We assessed 100 patients by MRI dedicated pelvis protocol for endometriosis with an assessment \nof the ovaries, uterus, uterosacral ligaments (USL), broad ligaments, and round ligaments, cul-de-sac, rectosigmoid \ncolon, bladder, ureters, and rectovaginal septum. All these patients are submitted for laparoscopy, and then, data \nfrom both investigations were correlated.\nResults MRI provided a road map for surgeons before laparoscopy. The sensitivity of MRI was 87.5% in small deep \ninfiltrating endometriosis (DIE) (grade A1) and 100% in large DIE (A2). MRI detected 82.3% of uterosacral ligament \ninvolvement, specificity 80%. Detection rate in rectal involvement was 71.4%, specificity 75%. There was 100% sensi-\ntivity and specificity in adenomyosis and urinary bladder endometriosis.\nConclusions Preoperative detection of endometriotic lesions is recommended using a dedicated MRI endometriosis \nprotocol to choose the surgical approach and for proper multidisciplinary teamwork planning.\nKeywords Endometriosis, MRI, DIE, ENZIAN classification\n*Correspondence:\nMomena Essam Ibrahim Elsadawy\nMomena.essam@yahoo.com\nFull list of author information is available at the end of the article\nBackground\nEndometriosis is defined as presence of ectopic endo -\nmetrial glands and stroma outside the normal uterine \ntissue. It is an estrogen-based condition, and it is a com -\nmon cause of pelvic pain, dyspareunia, dysmenorrhea, \ninfertility and sometimes can be asymptomatic, affect -\ning approximately 10% of premenopausal women. Symp -\ntoms usually depend on the site and the depth of the \ninfiltration and whether the endometriosis is complicated \nby adhesions [1].\nThe main and typical localizations of endometriosis \nare: ovarian endometrioma, retrocervical endometriosis, \ndeep bowel endometriosis, urinary bladder endometrio -\nsis and abdominal wall endometriosis [2].\nRadiologists should be familiar with the various imag -\ning manifestations of that disease as preoperative map -\nping of disease extension is important to decide whether \nsurgical intervention is indicated, and if so, for proper \npreoperative planning.\n\nPage 2 of 7Elsadawy and Ali  Egypt J Radiol Nucl Med  (2023) 54:188\nMagnetic resonance (MR) imaging has been recently \nwidely used for the detection and characterization of pel -\nvic endometriosis and has established its effectiveness [2].\nIt must be remembered that benign endometriomas, \nlike many pelvic malignancies, may exhibit restricted dif -\nfusion. Although women with endometriosis are at risk \nfor developing clear cell and endometrioid epithelial \novarian cancers (i.e. endometriosis-associated ovarian \ncancers), imaging findings such as enhancing mural nod -\nules should be confirmed before the diagnosis of ovarian \nmalignancy is offered. The presence of dilated fallopian \ntube, especially hematosalpinx, is often associated with \npelvic endometriosis [3].\nIn superficial endometriosis—also known as Sampson’s \nsyndrome—superficial plaques are scattered across the \nperitoneum, ovaries, and uterine ligaments.\nDeep infiltrating endometriosis—also known as Cul -\nlen’s syndrome—can involve the pelvic ligaments, ante -\nrior rectosigmoid colon, bladder, uterus, and cul-de-sac, \nas well as surgical scars; the lesions often have poorly \ndefined margins and T2 signal hypo-intensity as a result \nof fibrosis. The presence of sub-centimetric foci with T2 \nhyperintensity representing ectopic endometrial glands \nwithin these infiltrating fibrotic masses may help estab -\nlish the diagnosis [4].\nT1-weighted fat-suppressed pulse sequences are rec -\nommended for all MR examinations of the female pelvis \nbecause such sequence facilitates the detection of small \nendometriomas and aids in their differentiation from \nmature cystic teratomas [4].\nOur work aimed to evaluate the role of magnetic reso -\nnance imaging (MRI) in detection and characterization \nof endometriosis in correlation between it and the lapa -\nroscopic findings according to ENZIAN classification.\nMethods\nThe study was conducted during the period from July 2020 \ntill July 2022. Out of 200 scanned patients, only 100 patients \nwere selected in this retrospective single-institution study, \nand the included patients underwent dynamic ultrasound \nfollowed by MRI endometriosis protocol then laparoscopy.\nInclusion criteria were patient in child bearing period \nwith clinical diagnosis of endometriosis who could do \nthe MRI (not claustrophobic, not pregnant, and has no \nrenal impairment), and patients who did laparoscopic \ncorrelation.\nExclusion criteria included patients who did not per -\nform laparoscopy or failed to complete MRI study, due \nto renal function impairment or claustrophobia or MRI \nincompatible prosthesis implementation.\nThe study was approved by the Institutional Ethics \nCommittee, approval number 23–2020. No consent was \nobtained from patients due to the nature of the study.\nPatient aged 27 to 42 years, MRI was performed any -\ntime during the month after 4–6 h fasting, and enema \nwas administered 2–3 h before the examination. Urinary \nbladder was moderately-filled; the examination finished \nin 35 to 40 min with no complication.\nMRI acquisition\nA dedicated MRI protocol was applied using 1.5 Tesla \nsuperconducting unit (Signa LX, GE Healthcare) and \nhigh-resolution phased array coils.\nThe protocol sequences and parameters included: \nT1WI in axial and sagittal planes, T2WI in axial, sagit -\ntal and coronal plane FOV 38, 32, and 32 mm, respec -\ntively, axial T2 with fat suppression, coronal T2WI of the \nabdomen including the kidneys interslice gap 0.5 mm, \nsection thickness 5 mm, axial DWI 5 mm slice thickness \nand interslice gap 1 mm, b-value 1000, fat-suppressed \nT1-weighted 3D gradient-echo LAVA sequence in three \nplanes 3.4 mm slice thickness. Intravenous (IV) gado -\npentetate contrast (70–80 ml) was administrated fol -\nlowed by repetition of the LAVA in three planes.\nMRI interpretation\nThe images were interpreted by a radiologist who has \n3-year experience in endometriosis cases. ENZIAN clas -\nsification which provides a complete assessment of endo-\nmetriosis was used (Fig. 1). [5, 6].\nENZIAN classification for deep endometriosis is based \non pelvic three compartments classification (A—vagina, \nrectovaginal space (RVS); B—uterosacral ligaments \n(USL)/cardinal ligaments/pelvic sidewall; and C—rec -\ntum) as well as the urinary bladder (FB), the ureters (FU), \nand other extragenital lesions (FO).\nThe extent (size) of endometriosis is represented by the \nnumbers 1, 2, and 3 in compartments P , O, T, A, B, and C.\nThe individual anatomical regions are defined by capi -\ntal letters, and the size of the foci is divided into catego -\nries [7, 8].\nAssessment included:\n1. Pelvic endometriotic nodules DIE was mentioned (A) \nwith location and size description.\n2. Uterosacral ligaments on both sides (B0 and B1) were \nmeasured, and any thickening was reported.\n3. Rectosigmoid involvement (C) was mentioned with \ndetailed localization in relation to the anal verge, and \nsize was mentioned.\n4. The presence of adenomyosis (FA) was reported as \npresent or absent.\n5. The presence of urinary bladder wall thickening (FU) \nwas reported and the size measurement.\n\nPage 3 of 7\nElsadawy and Ali  Egypt J Radiol Nucl Med  (2023) 54:188\n \nLaparoscopic interpretation\nPatients underwent laparoscopic surgery by the same \nsurgical team within a period not exceeding two \nmonths from the MRI examination, and otherwise, \nMRI was repeated.\nENZIAN classification was done based on laparo -\nscopic findings.\nMRI and laparoscopic correlation (Table 1)\nData of MRI ENZIAN classification including A, B, and \nC were reported and compared to the corresponding \nlaparoscopic ENZIAN classification.\nStatistical analysis\nStatistical evaluation was performed using the SPSS \n(version 20.0; SPSS Inc., Chicago, IL, USA) software. \nFisher’s exact or chi-square test was performed for \ncategorical data, and the Kruskal–Wallis test was per -\nformed for continuous variables.\nSurgical results were accepted as standard, and pre -\noperative MRI findings were compared.\nSensitivity and specificity scores were calculated.\nResults\nRegarding ENZIAN classification in MRI, A0 was \nreported in 1 patient (1%), A1 was reported in 70 patients \n(70%) (Fig. 2), and A2 was reported in 2 patients (2%). B0 \nwas reported in 30 patients (30%), and B1 was reported in \n70 patients (70%) (Figs. 2, 3 and 4). C0 was reported in 50 \npatients (50%), and C1 was reported in 50 patients (50%) \n(Figs. 3 and 4). FA was reported in 90 patients (90%), and \nFU was reported in 20 patients (20%).\nRegarding ENZIAN classification in laparoscopy, \nA0 was reported in none (0%), A1 was reported in 80 \npatients (80%) and A2 was reported in 2 patients (2%). B0 \nwas reported in 15 patients (15%), and B1 was reported \nin 85 patients (85%). C0 was reported in 30 patients \n(30%), and C1 was reported in 70 patients (70%). FA was \nreported in 80 patients (80%), and FU was reported in 20 \npatients (20%) (Table 2).\nRegarding detection of DIE, the sensitivity of MRI \nwas 87.5% in small DIE (grade A1) while the detection \nFig. 1 Shows the schematic representation of the ENZIAN classification\n\nPage 4 of 7Elsadawy and Ali  Egypt J Radiol Nucl Med  (2023) 54:188\nrate was 100% in large DIE (A2). MRI detected 82.3% of \nuterosacral ligament involvement, specificity 80%. Detec-\ntion rate in rectal involvement was 71.4%, specificity 75%. \nThere was 100% sensitivity and specificity in adenomyo -\nsis and urinary bladder endometriosis.\nRegarding pelvic compartments, MRI showed same \nrate of detection like laparoscopy in cases of DIE of the \nanterior compartment with sensitivity of 100%. For the \nmiddle compartment, MRI showed sensitivity of 90% in \ndetecting DIE in correlation with laparoscopy. Regard -\ning the posterior compartment, MRI showed sensitivity \nof 68.3% compared to laparoscopy.\nFinally, regarding the size of DIE, MRI detection rate \ncompared to laparoscopy was higher in bigger lesions; \nthe sensitivity of MRI in detecting A1 lesions was \n87.5%, while MRI sensitivity in detecting A2 lesions \nwas 100%.\nTable 1 Data of MRI ENZIAN classification including A, B, and C were reported and compared to the corresponding laparoscopic \nENZIAN classification\nMRI ENZIAN classification Laparoscopic ENZIAN classification\nA B B C FA FU A B B C FA FU\n1 1 1 1 0  + 1 1 1 1  + \n2 1 1 0 0  + 1 1 1 1  + \n3 1 0 1 1  + 1 0 1 1  + \n4 1 1 1 0  +  + 1 1 1 0  +  + \n5 1 1 0 1 − 1 1 1 1 −\n6 1 0 0 1  + 1 1 0 1  + \n7 1 1 1 0  +  + 1 1 1 0  +  + \n8 0 1 0 0  + 1 1 0 0  + \n9 2 1 1 1  + 2 1 1 1  + \n10 2 1 1 1  + 2 1 1 1  + \nFig. 2 MRI sagittal T2WI A showing focal adenomyosis (long \narrow), focal DIE at the back of the uterus (arrow head). Axial T2WI \nB shows thickening of the right uterosacral ligament (long arrow). \nLaparoscopic image C shows thickened uterosacral ligament (long \narrow) and the DIE (short arrow). ENZIAN classification by MRI was A1 \nB1 B0 C0 FA and by laparoscopy A1 B1 B0 C1 FA\nFig. 3 MRI axial T2WI A shows thickening of the right uterosacral \nligament (long arrow). Axial T2WI B shows focal DIE on the serosal \nsurface of the rectum (long arrow). Laparoscopic image C shows \nthickened uterosacral ligament (long arrow). ENZIAN classification \nby MRI was A1 B1 B0 C1 and by laparoscopy A1 B1 B0 C1\n\nPage 5 of 7\nElsadawy and Ali  Egypt J Radiol Nucl Med  (2023) 54:188\n \nDiscussion\nEndometriosis is a chronic multifocal gynecologic dis -\nease that commonly affects females of reproductive age \nand may cause pelvic pain and infertility. The etiology \nof endometriosis is unknown [9]. The disease is charac -\nterized by the growth of functional ectopic endometrial \nglands outside the uterus.\nIn this study, MRI and laparoscopic scores showed \nsignificant concordance regarding compartments A, B, \nO, and C, which was compatible as well with previous \nstudies using ENZIAN classification.\nRegarding ENZIAN classification in MRI, our results \ndemonstrated 73% sensitivity and specificity of MRI in \nevaluation of compartment A, while a study done by \nBurla et al. [10] demonstrated 100% MRI sensitivity and \nspecificity in compartment A lesions.\nRegarding detection of DIE, the sensitivity of MRI \nwas 87.5% in small DIE (grade A1), while the detection \nrate was 100% in large DIE (A2), in comparison with \na study done by Bazot et al. [11] and found that diag -\nnostic values of MRI for DIE are quite high: sensitivity, \n90%; specificity, 91%; positive predictive value (PPV), \n92%; negative predictive value (NPV), 89%; and accu -\nracy, 90%, while pelvic MRI has a reported sensitivity of \n90.3% for the detection of DIE in a study performed by \nSiegelman et al. [1 ].\nHottat et al. reported MRI sensitivity of 96.3% and NPV \nof 93.3% in endometriosis and DIE detection [12].\nMedeiros et al. [13] recently published one meta-analy-\nsis on the diagnostic efficiency of pelvic MRIs in the diag-\nnosis of deep endometriosis. Such meta-analysis reviews \n20 studies published comparing the findings from high \nfield MRIs (1.0–3.0T) to surgical findings (laparoscopic \nor open) and histology as a reference pattern. MRI stud -\nies showed 83 percent sensitivity and 90 percent speci -\nficity in the diagnosis of injuries due to endometriosis. \nThe location that showed the highest sensitivity was \nthe pouch of Douglas (sensitivity = 89 percent, specific -\nity = 94 percent), while in the anterior compartment, the \nMRI sensitivity was lower (bladder sensitivity = 64 per-\ncent, specificity = 98 percent). This may be due to the fact \nthat since the posterior compartment is the most com -\nmon location of deep endometriosis, the MRI is more \nprecise tool for its detection.\nSensitivity and negative predictive values of MRI con -\nfirmed by surgery were 95.2% and 91.7% (lesions in the \nvaginal/rectovaginal space), 78.4% and 56% (uterosacral \nligaments), 91.4% and 89.7% (rectum/sigmoid colon), \n57.1% and 94.1% (myometrium), 85.7% and 98.3% (blad -\nder) in a study performed by Laurin et al. [14], while in \nour study, the sensitivity of MRI was 87.5% in small DIE \n(grade A1), while the detection rate was 100% in large \nDIE (A2). MRI detected 82.3% of uterosacral ligament \ninvolvement, specificity 80%. Detection rate in rectal \ninvolvement was 71.4%, specificity 75%. There was 100% \nsensitivity and specificity in adenomyosis and urinary \nbladder endometriosis.\nDi Paola et  al. [15] compared preoperative MRI find -\nings with intraoperative laparoscopic results by means \nof the ENZIAN score and found an overall correlation \nof 95%, with a sensitivity of 94%. In this study, the val -\nues are almost similar values specially in compartment \nFig. 4 MRI sagittal T2WI A shows focal nodule of DIE at the back \nof the cervix (long arrow); note the diffuse thickening \nof the transitional zone consistent with adenomyosis. Axial T2WI B \nshows thickening of the both uterosacral ligaments (long arrows). \nLaparoscopic image C shows thickened of the uterosacral ligaments \n(long arrows). ENZIAN classification by MRI was A1 B1 B1 C1 FA \nand by laparoscopy A1 B1 B1 C1 FA\nTable 2 Percentage of laparoscopic findings according to \nENZIAN classification\nENZIAN classification Laparoscopic \nfindings (%)\nA0 0\nA1 80\nA2 20\nB0 15\nB1 85\nC0 30\nC1 70\nFA 90\nFU 20\n\nPage 6 of 7Elsadawy and Ali  Egypt J Radiol Nucl Med  (2023) 54:188\nA with the highest value of the preoperative MRI-based \nENZIAN score could be confirmed.\nAysun et  al. [16] found that MRI has higher sensitiv -\nity and specificity in showing the lesions of the compart -\nments O (ovarian lesions), A (rectovaginal septum and \nposterior vaginal fornix), and B (uterosacral ligaments \nand parametrium) (100–100%, 100–100%, and 97–100%, \nrespectively, p < 0.001) compared to the other compart -\nments. The lowest sensitivity, specificity, accuracy, and \nPPV of the MRI were found in compartment P (14%, 76%, \n70%, and 7%, respectively).\nOur study agreed with Keckstein et  al., [17] that the \ncorrelation between preoperative imaging and surgical \nstaging using ENZIAN classification allows for a consist -\nent and clear classification of endometriosis.\nIn this study, the diagnosis of endometriosis was based \non the laparoscopic findings, and then the histopatho -\nlogic results as a second-line confirmation.\nLimitations of this study are its retrospective study \napproach with a limited patients number as well as limi -\ntations of patients compliance to MRI and single institute \nstudy and also having single radiologist for image reading \nlacks inter-reader interpretation.\nFurther prospective studies in a multicentric setting \nwith consistent diagnostic protocols will be required.\nAdvances in noninvasive multiparametric imag -\ning modalities are of special importance as diagnostic \nstandard value of endometriosis with systematic diag -\nnostic approach for better preoperative planning that \nwill lead to a reduction of recurrent or non-indicated \ninterventions.\nConclusions\nMRI highly correlates with the ENZIAN score and has \n95% accuracy in the detection and localization of endo -\nmetriosis, with specially 100% detection accuracy in the \nanterior compartment in concordance with laparoscopic \nfindings.\nIn conclusion, MRI is a valuable diagnostic tool for \nendometriosis, enabling a better pre-laparoscopic plan -\nning, allowing to for proper preoperative detection and \nbetter laparoscopic and clinical outcome.\nThe ENZIAN score detected by MRI is well correlated \nwith the laparoscopic findings.\nThe ENZIAN score may be used as an anatomical map-\nping and valuable communication language between the \nradiologists and the referring gynecologists.\nAbbreviations\nMRI  Magnetic resonance imaging\nDWI  Diffusion-weighted imaging\nDIE  Deep infiltrating endometriosis\nAcknowledgements\nThis research was carried out at King’s College Hospital, Dubai, which is fully \nequipped by dedicated machines for proper breast imaging. We want to \nthank our colleagues who helped us to do such research work.\nAuthor contributions\nHA collected patient data from the dedicated cases and was responsible for \ncorrespondence to journal. ME performed the statistical analysis and partici-\npated in manuscript drafting, writing the manuscript, and its revision. The \nauthors have read and approved the manuscript.\nFunding\nThere are no funding sources.\nAvailability of data and materials\nThe data sets used and analyzed during the current study are available from \nthe corresponding author on reasonable request.\nDeclarations\nEthics approval and consent to participate\nThe protocol was reviewed and approved by the local ethical committee of \n“Research Ethics Committee at the Faculty of Medicine, Ain Shams University.” \nIt ruled that no formal ethics approval was required in this retrospective study, \nand so no reference number was given by the IRB.\nConsent for publication\nThis research is based on retrospective study, yet, written consent for publica-\ntion was obtained for these cases.\nCompeting interests\nThere is no financial or non-financial competing interest.\nAuthor details\n1 Department of Radiodiagnosis and Nuclear Medicine, Ain Shams University, \nCairo, Egypt. \nReceived: 22 February 2023   Accepted: 17 October 2023\nPublished: 6 November 2023\nReferences\n 1. 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Acta Obstetr Gynecol Scand \n(AOGS) 100(7):1165–1175\nPublisher’s Note\nSpringer Nature remains neutral with regard to jurisdictional claims in pub-\nlished maps and institutional affiliations.","source_license":"CC0","license_restricted":false}