{"paper_id":"ceb1c7f3-1136-4236-97ce-41583fe09187","body_text":"Vol.:(0123456789)1 3\nArchives of Gynecology and Obstetrics (2023) 307:5–19 \nhttps://doi.org/10.1007/s00404-022-06766-z\nREVIEW\nExpert opinion on the use of transvaginal sonography for presurgical \nstaging and classification of endometriosis\nJ. Keckstein1,2,14,15,18  · M. Hoopmann3 · E. Merz4 · D. Grab2 · J. Weichert5 · S. Helmy‑Bader6,16 · M. Wölfler7,14,16 · \nM. Bajka8,17 · S. Mechsner9,14,15 · S. Schäfer10,14,15,18 · H. Krentel11,14,15,18 · G. Hudelist12,13,14,16,18\nReceived: 17 July 2022 / Accepted: 19 August 2022 / Published online: 11 November 2022 \n© The Author(s) 2022\nAbstract\nGynecological ultrasonography plays a central role in the management of endometriosis. The rapid technical development \nas well as the currently increasing evidence for non-invasive diagnostic methods require an updated compilation of recom-\nmendations for the use of ultrasound in the management of endometriosis. The present work aims to highlight the accuracy \nof sonography for diagnosing and classifying endometriosis and will formulate the present list of key messages and recom-\nmendations. This paper aims to demonstrate the accuracy of TVS in the diagnosis and classification of endometriosis and to \ndiscuss the clinical applications and consequences of TVS findings for indication, surgical planning and assessment of associ-\nated risk factors. (1) Sophisticated ultrasound is the primary imaging modality recommended for suspected endometriosis. \nThe examination procedure should be performed according to the IDEA Consensus. (2) Surgical intervention to confirm the \ndiagnosis alone is not recommended. A preoperative imaging procedure with TVS and/or MRI is strongly recommended. \n(3) Ultrasound examination does not allow the definitive exclusion of endometriosis. (4) The examination is primarily \ntransvaginal and should always be combined with a speculum and a bimanual examination. (5) Additional transabdominal \nultrasonography may enhance the accuracy of the examination in case of extra pelvic disease, extensive findings or limited \ntransvaginal access. (6) Sonographic assessment of both kidneys is mandatory when deep endometriosis (DE) and endome-\ntrioma are suspected. (7) Endometriomas are well defined by sonographic criteria. When evaluating the ovaries, the use of \nIOTA criteria is recommended. (8) The description of sonographic findings of deep endometriosis should be systematically \nrecorded and performed using IDEA terminology. (9) Adenomyosis uteri has sonographically well-defined criteria (MUSA) \nthat allow for detection with high sensitivity and specificity. MRI is not superior to differentiated skilled ultrasonography. \n(10) Classification of the extent of findings should be done according to the #Enzian classification. The current data situation \nproves the best possible prediction of the intraoperative situs of endometriosis (exclusive peritoneum) for the non-invasive \napplication of the #Enzian classification. (11) Transvaginal sonographic examination by an experienced examiner is not \ninferior to MRI diagnostics regarding sensitivity and specificity in the prediction of the extent of deep endometriosis. (12) \nThe major advantage of non-invasive imaging and classification of endometriosis is the differentiated planning or possible \navoidance of surgical interventions. The recommendations represent the opinion of experts in the field of non-invasive and \ninvasive diagnostics as well as therapy of endometriosis. They were developed with the participation of the following national \nand international societies: DEGUM, ÖGUM, SGUM, SEF, AGEM/DGGG, and EEL.\nKeywords Endometriosis · Ultrasound · Diagnostics · #Enzian classification · Recommendation\nWhat does this study add to the clinical work \nThe TVS is an efficient, accurate, and cost-effective \ntool for the non-invasive diagnosis of endometrio-\nsis. #Enzian classification for the description of \nTVS correlates very well with surgical findings, and \nwill provide clinicians with a standardized language \nfor the comprehensive description of endometriosis. * J. Keckstein \n joerg.keckstein@uni-ulm.de; joerg@keckstein.at\nExtended author information available on the last page of the article\n\n6 Archives of Gynecology and Obstetrics (2023) 307:5–19\n1 3\nIntroduction\nSophisticated ultrasound is the primary \nimaging modality recommended for suspected \nendometriosis: the examination procedure should \nbe performed according to the IDEA consensus\nFirst described in 1860 [1 ] and primarily diagnosed via \nbimanual palpation performed before surgery and histo -\nlogical confirmation, endometriosis can now be described \nwith high accuracy via several non-invasive imaging meth-\nods. Today, ovarian endometriomas and deep endometriosis \n(DE) can be detected by ultrasound or magnetic resonance \nimaging (MRI) [2 –5]. In addition, adhesions can also be \nvisualized indirectly using organ mobility and sliding signs \non transvaginal sonography (TVS) [6 , 7]. Accurate sono-\ngraphic evaluation of the different forms of endometriosis \nhas become one of the most important elements in the man-\nagement of affected women, which is now included in the \nrecommendations of the national and international societies \n[8–12]. However, the former lack of standardized definitions \nin the sonographic classification and divergent methods of \nclassifying the affected anatomical location and extent of \nthe disease led to evident and inconclusive variations in the \nreported diagnostic accuracy of TVS in the diagnosis of \nendometriosis. This problem was addressed by the Interna-\ntional Deep Endometriosis Analysis (IDEA) group in 2016. \nThey proposed a systematic approach for sonographic work-\nflow and specified terms, definitions, and measurements to \ndocument the dimension and location of the lesions [3 ].\nThis IDEA Consensus is the most widely used and \naccepted standard for the sonographic examination proce-\ndure in patients with endometriosis [13].\nSurgical intervention to confirm the diagnosis \nalone is not recommended: a preoperative imaging \nprocedure with TVS and/or MRI is required\nAlthough surgery is still considered the diagnostic gold \nstandard, especially in patients with the peritoneal disease, \nthis dogmatic approach brings three major problems that \nneed to be discussed. First and foremost, surgical and sub-\nsequent histologic diagnosis is again based on the surgeon’s \nvisualization of endometriosis. Extensive adhesions and \ndeep endometriosis (DE), some of which may be extra-\nperitoneal, may primarily obscure the extent of the disease. \nDissection of the occluded spaces requires experience and \nadvanced surgical skills of the surgeon to meet the require-\nments of a “gold standard test.” As a result, patients with \nsevere adhesions or a so-called “frozen pelvis” may under -\nestimate the true extent of endometriosis. Especially in \npatients with minor symptoms, the indication for surgery and \nin particular the extent of the procedure must be weighed \nagainst the potential risks [14]. Second, visualization of \ndisease—even in the case of minor peritoneal endometrio-\nsis—is by nature subjective. Hence, there is some evidence \nthat surgical subjectivity may lead to relevant discrepancies \nin final diagnosis and may even poorly correlate with his-\ntological proof of the disease, especially under non-tertiary \nreferral, and routine conditions [15].\nThird, uterine adenomyosis cannot always be confirmed \nvisually or even histologically in patients with fertility prob-\nlems, which may lead to a diagnostic dilemma regarding \nthe laparoscopic “gold standard test.” As a consequence, \nthe eminent European Society for Human Reproduction \n(ESHRE) states in the updated and probably most extensive \nand most cited endometriosis guideline regarding laparo-\nscopic identification of endometriosis as a gold standard test \nthat “…advances in the quality and availability of imaging \nmodalities for at least some forms of endometriosis on the \none hand and the operative risk, limited access to highly \nqualified surgeons and financial implications on the other, \ncalls for the urgent need for a refinement of this dogma [9], \nand delete the diagnostic laparoscopy as recommended gold \nstandard in the diagnosis of endometriosis, when imaging \nfinding shows changes suspected of endometriosis”.\nDiagnostic imaging methods include multiple modali -\nties such as MRI, computed tomography (CT), X-ray and \nsonography. Regarding the non-invasive diagnosis of endo-\nmetriosis, only MRI and sonography in form of TVS have \nbeen proven reliable and accurate tools for diagnosing the \ndisease [5, 16].\nUltrasonography does not allow the definite \nexclusion of endometriosis\nA Cochrane Review concerning the imaging modalities for \nendometriosis concludes that TVS and MRI help surgeons \nto better plan an operative procedure [17 ]. However, the \nauthors also state that none of the imaging techniques was \naccurate enough to ensure complete detection of total pelvic \nendometriosis. Superficial peritoneal endometriosis may be \nthe only entity which cannot be reliably diagnosed by any \nimaging method [18]. A recently published prospective, \nmulticentre study including 745 patients undergoing TVS \nand surgery found excellent sensitivities for DE and ovarian \nendometriosis [19]. But none of the analyzed anatomical \nsites reached a 100% detection rate. The lowest rates were \ndescribed for extrapelvic nodules such as DE in the intestine \n(above the rectosigmoid colon), diaphragm, lung, or nerves.\nThe different accuracy of sonographic diagnostics is \nmainly influenced by the size and localization of the find-\nings and the accessibility with the ultrasound probe, but \nalso by the skill and experience of the examiner. Learning \n\n7Archives of Gynecology and Obstetrics (2023) 307:5–19 \n1 3\nthe technique requires a certain number of examinations, as \nTammaa [20] demonstrated in Douglas obliteration and DE \non the rectum.\nThe present work should contribute as a basis for the \nestablishment of standardized sonographic diagnostics of \nendometriosis, which in the future should affect the stand-\nards of training and required quality of diagnostics.\nThe examination is primarily transvaginal \nand should always be combined with a speculum \nand a bimanual examination\nTVS has proven to be a cost-effective, easy-at-hand tool \nshowing real-time assessment of the uterus, the pouch of \nDouglas, and ovaries. In addition, the visualization and \nassessment of the ureters, urinary bladder, and rectum facili-\ntate the diagnosis of anatomical changes due to endome-\ntriosis. Compared to bimanual examination, several papers \nhave shown the diagnostic superiority of TVS. However, \nespecially in patients with vaginal lesions, the combination \nof imaging techniques and clinical examination, including \nspeculum examination and bimanual palpation, leads to a \nclearer view of the structures involved [21–23]. In addition, \nthe dynamic examination includes not only imaging of endo-\nmetriosis but also assessment of motility of the pelvic organs \n(sliding signs), tissue elasticity, and tenderness of affected \norgans (compartments) [6, 24].\nAdditional transabdominal ultrasonography \nmay enhance the accuracy of sonography in case \nof extrapelvic disease, extensive findings or limited \ntransvaginal access\nHigher resolution and anatomical proximity are key advan-\ntages of TVS for a pelvic examination, but in cases with the \nsevere extent of DE, lesions can exceed beyond the pelvic \nregion (e.g., in higher sections of the intestine, abdominal \nwall, or diaphragm, Fig.  1). In these cases, transabdominal \nsonography can help to complete the anatomical evaluation. \nFurthermore, in some patients, the favored vaginal ultra-\nsound access is not feasible (for example, due to vaginal \nstenosis or vaginismus), so the transabdominal route can \nbe used as an alternative. The performance of abdominal \nsonography is primarily based on symptoms. However, \nsonography of the kidneys is also essential in asymptomatic \ndeep endometriosis.\nAssessment of the kidneys by transabdominal \nsonography is mandatory when deep endometriosis \nand endometriomas are suspected\nHydronephrosis is a common and relevant complication \nof DE, especially in cases with ureteral endometriosis. \nSubjective urinary tract symptoms may be present, but a \nsilent loss of kidney function occurs in a significant part \nof the patients. Transabdominal ultrasound is an easy and \nreliable method for detecting and evaluating hydronephro-\nsis [25]. In case of endometrioma, the probability of con -\ncomitant DE of the pelvic wall is high and needs also more \nextensive attention [6].\nEndometriomas are well defined by sonographic \ncriteria: when evaluating the ovaries, the use \nof IOTA criteria is recommended\nRegarding the diagnosis of ovarian endometriomas, a \nCochrane review on non-invasive tests for diagnosis of \nendometriosis by Nisenblat et al. [26] summarizes 8 studies \nincluding 765 patients with endometriomas demonstrated an \noverall sensitivity and specificity of 93% and 96%, respec-\ntively. Endometriomas are among the most common preoper-\native findings of adnexa with a pathognomonic sonomorpho-\nlogic appearance. The international ovarian tumor analysis \n(IOTA) group has, therefore, summarized the typical picture \nof endometriomas as benign simple descriptor: unilocular \ntumor with ground-glass echogenicity in a premenopausal \nwoman (Fig.  2a, b) [27]. This is the most common but not \nthe only presentation of endometriomas. They can also be \nmultilocular (Fig.  3), but then they do not have more than \nfour cysts. Papillary projections are found in 10%, but most \noften without internal blood flow. Occasionally, peripheral \npunctate echogenic foci and sludge are seen with endome-\ntriomas. CA125 may be moderately elevated (median 44 U/\nmL) [28]. Mascilini’s study [29] showed that it is possible \nto distinguish decidualized endometriomas with papillary \nprojections from borderline tumors with papillary features \nby assessing the contour of the papillary projection and the \nechogenicity of the cyst fluid. This differentiated description \ncan significantly reduce the number of unnecessary surgeries \nfor adnexa during pregnancy.\nThe description of sonographic findings of deep \nendometriosis should be systematically recorded \nand performed using IDEA terminology\nDE is a particular form of endometriosis that penetrates \nmore than 5 mm under the peritoneal layer thereby causing \ntypical sonoanatomical changes in affected organs such as \nthe urinary bladder, vagina, parametrial tissues, and intes-\ntines [30]. The IDEA criterion additionally differentiates the \ndepth of infiltration into the affected organs [3 ]. There is \ngood evidence that there is a direct correlation between the \nextent of DE and the severity of symptoms [31].\nTVS has been recommended as the first-line diagnostic \ntool to assess patients with suspected DE [32, 33]. Although \nthe utility of TVS for diagnosing DE is proven, it should \n\n8 Archives of Gynecology and Obstetrics (2023) 307:5–19\n1 3\nbe discussed that the method is strictly operator-dependent. \nConsequently, TVS performed by an untrained and/or non-\ngynecologic operator has limited diagnostic potential. Thus, \nhigh-quality TVS is limited to experienced sonographers \nand/or certified tertiary referral centers [20, 34].\nTo create uniform terms and definitions for DE and TVS \nin combination with a structured protocol on how to assess \nand document DE with TVS, the International Deep Endo-\nmetriosis Analysis (IDEA) group published a consensus \nstatement in 2016 [3 ]. As the first one of its kind, it pro-\nvides clinicians with concise definitions of DE visualized \non TVS and allows for a structured step-by-step assessment \nof pelvic organs of the so-called anterior with urinary blad-\nder (Figs.  4, 5a, b) and ureters and posterior compartment \n(intestines, uterosacral ligaments, rectovaginal septum and \nvagina, Figs.  6, 7, 8, 9, 10).\nThe high diagnostic accuracy of TVS for diagnosing DE \nis well documented. In their Cochrane review, Nisenblat \net al. [ 26] report a mean sensitivity of 79% (95% CI 69–89%) \nand specificity of 94% (CI 88–100%) for TVS-based diagno-\nsis of DE, thereby fulfilling the criteria of a triage test to rule \nin endometriosis. So far, additional four systematic reviews \nand meta-analyses have examined the validity of TVS for \ndiagnosing DE over the past decade [2, 5, 35, 36]. Following \nprevious works, recently published pooled sensitivities and \nspecificities for colorectal DE are 89% and 97% and 55% and \n99% for DE affecting the urinary bladder with relevant het-\nerogeneity of the reviewed studies on this anatomical loca-\ntion. Notably lower values were observed for uterosacral DE \nwith a sensitivity of 64% (95% CI 50–79%) and specificity \nof 97% (93–100%) [17], which is in line with the recently \npublished work by Gerges et al. [5 ].\nAdenomyosis uteri has sonographically well‑defined \ncriteria (MUSA) that allow for detection with high \nsensitivity and specificity: MRI is not superior \nto a differentiated experienced ultrasound \nexamination\nAdenomyosis uteri is defined as the presence of ectopic, \nnon-neoplastic endometrial glands and stroma within the \nmyometrium. As a rule, the ectopic endometrium is sur -\nrounded by hypertrophic and hyperplastic myometrium. In \nsevere cases, the entire structure of the myometrium, i.e., \nthe architecture of the uterine wall, is completely destroyed. \nEspecially young patients with adenomyosis uteri frequently \nsuffer from pain and dysmenorrhea. Furthermore, adeno-\nmyosis uteri affects the reproductive outcome and leads to \npregnancy and obstetrical complications [37]. Therefore, \ndiagnosing adenomyosis as early as possible is crucial with \nnon-invasive imaging techniques. For decades, adenomyosis \ncould only be reliably diagnosed by performing a targeted \nbiopsy or hysterectomy and histopathological analysis of the \ntissue. It is only since the 1980s, with the advent of high-\nresolution ultrasound and the development of magnetic reso-\nnance imaging (MRI), that the diagnosis of adenomyosis can \nbe made accurately and with sufficient sensitivity without \nthe need for surgery or removal of the uterus. Knowledge of \nthe imaging criteria is critical in this regard. The manifesta-\ntions are heterogeneous, but typical criteria of adenomyosis \nuteri are [38]:\nFig. 1  Transabdominal \nultrasound to identify a deep \nendometriosis nodule in the \nabdominal wall (#Enzian(u) \nFOabd. wall)\n\n\n9Archives of Gynecology and Obstetrics (2023) 307:5–19 \n1 3\nFig. 2  a Typical unilocu-\nlar endometrioma (diam-\neter > 7 cm = #Enzian(u)O3). \nEchogenicity: ground glass-like \nechogenicity. b Sonographic \nimage of an atypical multilocu-\nlar ovarian endometrioma with \ndifferent echogenicity of the \nlocules\nFig. 3  Multilocular endome-\ntrioma (sum of all diameters \n6.5 cm = #Enzian(u)O2)\n\n\n10 Archives of Gynecology and Obstetrics (2023) 307:5–19\n1 3\n• globally enlarged uterus\n• asymmetry between the anterior and posterior wall of the \nuterus\n• irregular and/or ill-defined lesions without rim\n• fan-shaped shadowing\n• non-uniform, mixed echogenicity with cysts, hyperecho-\ngenic islands and/or sub-endometrial lines and buds\n• in Doppler sonography depiction of a translesional flow\n• the junctional zone is often thickened, irregular or ill-\ndefined\n• depictable interruption of the junctional zone\nUsually, not all the above criteria are met at the same \ntime (Figs.  11, 12). The terms and definitions have been \nFig. 4  Cystoscopic view of a deep endometriosis nodule in the poste-\nrior bladder wall (#Enzian(s)FB)\nFig. 5  a Sonographic view of \nDE of the bladder (#Enzian(u)\nFB), presenting a full thick-\nness defect at the bladder \ndome by a large inhomoge-\nneous deep endometriosis \nnodule. b 3D demonstration \nof a severe bladder endome-\ntriosis (30.8 × 17.1 × 23.5 mm) \noriginating from the posterior \nbladder wall (#Enzian(u)\nFB). A–C Multiplanar glass \nbody demonstration (grey \nscale + color Doppler): A = sag-\nittal view, B = transverse view, \nC = coronal view. 3D = surface \ndemonstration of the cut plane \nwith monochromic demonstra-\ntion of the vascularization\n\n\n11Archives of Gynecology and Obstetrics (2023) 307:5–19 \n1 3\nstandardized and described in a consensus paper of the Mor-\nphological Uterine Sonographic Assessment (MUSA) group \n[38]. These diagnostic criteria are also anchored in the cur -\nrent quality requirements for DEGUM level 2 for gyneco-\nlogical sonography [11]. The diagnostic accuracy of TVS is \nhigh. In a recent meta-analysis, the sensitivity and specificity \nwere 78% (AUC 0.73) [39]. The combination of 2D and \n3D ultrasound tended to improve diagnostic accuracy. The \nso-called question mark sign describes the position of the \nuterus fixed in retroflection [3 ]. Adhesions and DE lesions \nprimarily cause this. However, the sonographic picture of the \nquestion mark sign also correlates with adenomyosis uteri. \nIn a further meta-analysis, the addition of the sonographic \nquestion mark sign leads to an ameliorated overall sensi-\ntivity and specificity of transvaginal ultrasound, which was \n83% and 88%, respectively [40]. No diagnostic superiority of \nMRI could be found, so transvaginal sonography is recom-\nmended as a first-line method due to its better availability \nand lower costs [39, 41].\nClassification of the extent of findings should \nbe done according to the #Enzian classification: \nthe current data prove the best possible prediction \nof the intraoperative situs of endometriosis \n(exclusive peritoneum) for the non‑invasive \napplication of the #Enzian classification\nThe accurate documentation can be done individually \n(description) or in a standardized form, e.g., by a uni -\nform classification. This is of great advantage both for the \nrapid assessment of the findings and for interdisciplinary \ncommunication.\nThe ideal system for classifying endometriosis should be \napplicable for imaging and surgical interventions. Although \nseveral scores and systems have been proposed over the past \n50 years [42], the main surgical classification systems which \nare currently used in everyday clinical practice worldwide \nare the rASRM score [43], the Enzian classification [44] and \nthe so-called EFI (endometriosis fertility index) [45] which \nis rather a prediction model for fertility purposes follow -\ning surgery for endometriosis. Finally, the American Asso-\nciation of Gynaecological Laparoscopists (AAGL) recently \nproposed the so-called AAGL score for surgical staging and \ndescription of endometriosis [46]. To date, several studies \nhave tried to evaluate the use of TVS in combination with \nthe rASRM and Enzian classification. High-quality studies \non the applicability of TVS with other classification systems \nare lacking so far.\nThe rASRM classification, which has been in use over \ndecades, primarily focuses on the effects of endometriosis \non fertility in association with peritoneal and ovarian disease \nand secondary adhesions. This excludes the detailed descrip-\ntion of DE which is considered the main disadvantage of \nthis score [44, 47]. Nevertheless, there have been attempts \nto use TVS in combination with the rASRM score. In a ret-\nrospective study including 204 women, Leonardi et al. [48] \nfound the accuracy of TVS for the prediction of the surgical \nrASRM stage to be 53.4% for stage 1, and 93.8%, 89.7% \nand 93.1% for stages 2, 3 and 4, respectively. Sensitivities, \nspecificities, positive predictive values (PPVs) and negative \npredictive values (NPVs) of TVS were 18.2%, 94.7%, 80% \nand 49.7% for rASRM stage 1, 22.7%, 96.7%, 45.5% and \n91.2% for stage 2, 62.5%, 92.0%, 40.0% and 96.7% for stage \nFig. 6  Transvaginal image of a deep rectal endometriosis nodule \n(length 1.9  cm = #Enzian(u)C2). A = thickened intestinal muscle \nlayer with deep nodule (hypodense), B = mucosal layer (hyperdense), \nC = muscle layer of the posterior rectal wall (hypodense), and D = the \nlumen of the intestine\nFig. 7  Sonographic image of an irregular deep endometriosis nod-\nule in the rectal anterior wall (length 1.8  cm = #Enzian(u)C2). The \nhypodense area (A) represents the marked widening of the muscle \nlayer due to a deep endometriosis nodule, accompanied by fibrosis or \nmyohyperplasia of the layer. The normal pattern of the muscle layer \nis visible in the caudal direction and the parts of the posterior wall \n(B). The lesion lies directly underneath the mucosa (full thickness \ndefect) (C)\n\n12 Archives of Gynecology and Obstetrics (2023) 307:5–19\n1 3\n3 and 71.9%, 97.1%, 82.1% and 94.9% for stage 4, suggest-\ning higher accuracy for TVS in higher disease stages. In a \nprospective study including 201 women, Holland et al. [7 ] \nalso found good agreement between TVS findings and the \nsurgical rASRM stage (absent, minimal, mild, moderate, and \nsevere endometriosis; quadratic weighted kappa = 0.786). \nHowever, they also observed low sensitivity for TVS \ndiagnosing minimal and mild endometriosis but accuracy \nof 94% for TVS for detecting moderate and severe disease.\nTo overcome the lack of adequately describing DE, the \nEnzian classification was developed in 2003 [44, 49] and \nfurther extended to ovarian endometriosis and secondary \nadhesions in 2021 [50] (Fig.  13). Up to date, three studies \nhave evaluated the accuracy of TVS in combination with the \nEnzian classification. Hudelist et al. evaluated 195 women \nwith DE undergoing TVS and surgery and found good agree-\nment, especially for Enzian compartments A (vagina, rec-\ntovaginal space), C (rectum) and FB (urinary bladder. DE \nin compartments A, B, C, and FB were diagnosed with a \nsensitivity of 84%, 91%, 92%, and 88%, respectively, and a \nspecificity of 85%, 73%, 95%, and 99% [51]. Enzelsberger \n[52] classified deep endometriosis preoperatively by one or \ncombined methods (clinical examination, TVS, MRI) using \nthe cEnzian classification. Less accurate results could be \nexplained by a lack of standardized requirements in the clas-\nsification application and possibly nonvalidated expertise of \nthe different investigators in this study, which is not yet part \nof the certification requirements for participating centers. \nThe problem of the lack of comprehensive documentation \nof endometriosis with the available classification systems \nhas been increasingly discussed [53], especially since non-\ninvasive diagnostics have gained considerably in accuracy \nand are increasingly regarded as a fundamental part of the \ntreatment of patients. Instead of combining different clas -\nsification systems, a single system such as the #Enzian clas-\nsification can be used for both non-invasive and invasive \ndiagnostics [50]. Di Giovanni et al. [54] retrospectively \ninvestigated 93 patients undergoing TVS and surgery using \nFig. 8  Image of a deep nodule \npresenting a full thickness \ndefect in the anterior rectum \nwall with prominent spikes \ntowards the bowel lumen with \nextrinsic reaction (hypodense \narea; zig-zagged shaped)\nFig. 9  Schematic drawing of the ultrasound probe position for \nexact evaluation of the uterosacral ligaments and the parametrium \n(= #Enzian B compartment). The probe is moved slightly laterally in \nthe uterine fornix and then tilted between 20 and 90 degrees\n\n13Archives of Gynecology and Obstetrics (2023) 307:5–19 \n1 3\nFig. 10  Sonographic image \n(hypodense areal) of the right \nuterosacral ligament (USL) \n(length 1, 2 cm = #Enzian(u)\nB0/2). The ligament is infil-\ntrated by endometriosis and \nsignificantly thickened. In the \nleft part of the image, parts of \nthe cervix uteri are also visible. \nThe vaginal wall is sonographi-\ncally inconspicuous and has a \nnormal thickness\nFig. 11  Adenomyosis \n(#Enzian(u)FA): asymme-\ntry between the anterior and \nposterior wall of the uterus; fan-\nshaped shadowing non-uniform; \nmixed echogenicity with cysts, \nhyperechogenic islands\nthe #Enzian classification. Sensitivities and specificities for \nTVS in compartments were between 86 and 100% (Table 1).\nRecently, a prospective, multicentre study including 745 \npatients undergoing TVS in combination with the #Enzian \nclassification and surgery [19] documented sensitivities for \nthe detection of DE ranging from 50% (#Enzian compart-\nment FI—other intestinal locations) to 95% (#Enzian A), \nspecificities from 86% (#Enzian T left) to 99% (#Enzian FI) \nand 100% (#Enzian FB—urinary bladder, FU—ureters and \nFO—other extragenital locations) with positive predictive \nvalues of 90% (#Enzian T right) to 100% (#Enzian FO), \nnegative predictive values of 74% (#Enzian B left) to 99% \n(#Enzian FB and FU) and accuracies of 88% (#Enzian B \nright) to 99% (#Enzian FB). These data support that DE can \nbe accurately evaluated using TVS in combination with the \n#Enzian classification (Table  1 and Figs.  13, 14a, b)).\nTherefore, the ISGE recommends the best possible detec-\ntion of endometriosis using the systematic IDEA criteria \nand the comprehensive classification by the #Enzian clas-\nsification [13].\nTransvaginal sonographic examination \nby an experienced examiner is not inferior \nto MRI diagnostics in sensitivity and specificity \nin the prediction of the extent of deep \nendometriosis\nSeveral meta-analyses confirmed the equivalence of TVS \nand MRI in the diagnosis of the specific pelvic anatomic \nlocation of endometriosis lesions [17, 55, 56]. Prospec-\ntive studies to compare TVS and MRI in the diagnosis of \nendometriosis are rare. Indrielle-Kelly et al. assessed the \n\n14 Archives of Gynecology and Obstetrics (2023) 307:5–19\n1 3\ndiagnostic accuracy of TVS and MRI in preoperative pel -\nvic DE mapping on the same cohort of 51 patients, using 1 \nstandardized IDEA-based protocol [23, 57]. They found that \nTVS and MRI were similar in their performance in endo-\nmetriosis mapping. The dynamic aspect of ultrasonography \ncombined with the high-resolution transvaginal ultrasound \nprobe increases the detection rate of the obliteration of the \npouch of Douglas and the overall accuracy of the ultrasound. \nDue to the non-superiority of MRI in most anatomic locali-\nzations, its better availability, and lower cost, TVS is recom-\nmended as the method of the first choice. MRI examination \nis superior to ultrasound for technical/physical reasons, espe-\ncially in cases of exclusive pelvic wall involvement, possibly \ninvolving nerves, diaphragm, and/or lung. Furthermore, it \nshould be mentioned that the #Enzian score is also applica-\nble to MRI, but minor modifications are suggested [58, 59].\nFig. 12  Cystic adenomyosis (#Enzian(u)FA). Typical signs: asymme-\ntry; mixed echogenicity; sub-endometrial cystic lesion\nFig. 13  #Enzian classification for the comprehensive description and \nclassification of endometriosis. The individual affected compartments \nare classified according to the localization and size of the findings \nusing a code. The compartments are marked with capital letters and \nin the case of paired organs or structures (ovary, tube, USL and ure-\nter); the sides are also shown separately behind the respective letters. \nThe lesions are classified with a code that takes into account both \nthe location and the size of the different findings. The results of soft \nmarkers (sliding signs) and tube perturbation (e.g., with HyCoSy) \nare also shown. The classification can be used for both non-invasive \n(TVS = (u), MRI = (m)) and invasive ((s) = surgery) diagnostics\n\n15Archives of Gynecology and Obstetrics (2023) 307:5–19 \n1 3\nThe significant advantage of non‑invasive \nimaging and classification of endometriosis \nis the differentiated planning or possible avoidance \nof radical surgical interventions\nThe risk factors for surgical complexity and postoperative \ncomplications after more or less radical colorectal surgery \nin DE are well known. The lesion's location and size sig-\nnificantly impact this [60, 61]. For example, in intestinal \nendometriosis, the height of surgical anastomosis [62], the \nextent of parametrial involvement and the surgical technique \n[63] are essential factors. Similarly, ureteral and parame-\ntrial involvement or the combination of different pelvic DE \nlesions influences both symptoms and the expected complex-\nity of surgical treatment. Proper preinvasive recognition of \ndisease extent and #Enzian classification using sonography \nor MRI can help to ensure an accurate assessment of both \nthe indication and the anticipated surgical procedure [57, \n64]. Both improve patient counseling and the planning of \ninterdisciplinary procedures, if necessary. For example, TVS \nhas been shown to correctly determine the size of colorec-\ntal DE before surgery [65]. Aas-Eng and colleagues have \nalso demonstrated that TVS correctly reflects the distance \nbetween colorectal DE lesion and the anal verge and ade -\nquately estimates the height of the final surgical anastomosis \n[66], which is important for risk assessment. Rectal endo-\nscopic sonography RES [55, 67], although an alternative for \ndetermining the location and extent of the lesion, requires \nappropriate gastroenterological expertise and cannot be used \nto assess other pelvic structures.\nThe risk for surgical complications correlates with \nthe extent of lesions and, therefore, with a higher \nEnzian/#Enzian score in certain anatomic compartments. \nFor example, Poupon et al. developed a nomogram classi-\nfication [68] showing a direct correlation between compli -\ncation risk and Enzian classification. Similar observations \nwere made by Nicolaus et al. [69].\nTherefore, the use of TVS for non-invasive assessment of \nsurgical complexity and risk factors for surgical complica-\ntions is recommended.\nConclusions and perspective\nThe use of TVS is an efficient and accurate tool for the \nnon-invasive diagnosis of endometriosis. Although this \nimaging technique does have limitations such as operator \ndependency, it is cost-effective and enables the clinician \nto establish a diagnosis in cases of the ovarian and deep \ndisease. Many doctors still rely on surgical and histologi-\ncal confirmation as a gold standard test. This approach is \nhighly questionable and may not be up to date. The authors \nadvocate for using of TVS as a primary tool to evaluate \nwomen with suspected endometriosis and to stratify these \npatients into low- and high-risk patients based on the results \nof TVS-based preoperative assessment. A nearly complete \nTable 1  The accuracy of \nsonographic classification \n(#Enzian(u)) of endometriosis \ncompared with the result \nof surgical classification \n#Enzian(s) (retrospective study \nby di Giovanni A. et al. [54] and \nprospective study of Montanari \nE. [19])\nO = ovary; T = adhesions of the adnexa; A = vagina, rectovaginal septum, torus uteri; B = USL, parame-\ntrium; C = rectum; FB = bladder; FI = intestinal above the rectosigmoid (> 16 cm from the anus); FU = ure-\nteral obstruction; FO = other lesions\n*For #Enzian compartment T, it was not possible to calculate sensitivities and specificities, as there were \ntoo few cases without any lesion during TVS or surgery\ndi Giovanni et al. Montanari et al.\nn = 93 (retrospective) n = 745 (prospective)\n#Enzian compart-\nment\nSensitivity (%) Specificity (%) Sensitivity (%) Specificity (%)\nO left 100 (92–100) 96 (86–100) 90 (86–94) 96 (94–98)\nO right 100 (87–100) 98 (87–100) 89 (84–92) 98 (96–99)\nT left *(87–93) *(82–90) 90 (87–93) 86 (82–90)\nT right *(84–91) *(87–93) 88 (84–91) 90 (87–93)\nA 97 (90–100) 86 (64–97) 95 (92–96) 93 (89–96)\nB left 97 (90–100) 70 (47–87) 91 (88–93) 88 (83–93)\nB right 100 (95–100) 90 (70–99) 83 (79–87) 94 (91–96)\nC 100 (92–100) 96 (86–100) 93 (90–95) 95 (92–98)\nFB 86 (42–100) 100 (96–100) 94 (87–98) 100 (99–100)\nFI 100 (80–100) 100 (95–100) 50 (41–59) 99 (98–100)\nFU 100 (75–100) 100 (95–100) 78 (63–89) 100 (99–100)\nFO 100 (48–100) 98 (92–100) 57 (37–76) 100 (99–100)\n\n16 Archives of Gynecology and Obstetrics (2023) 307:5–19\n1 3\nnon-invasive diagnosis of endometriosis opens up new per-\nspectives for conservative and surgical treatment. Using the \n#Enzian classification, also in the context of sonographic \nassessment, provides clinicians with a uniform “language” \nfor a comprehensive and easily reproducible description of \nendometriosis.\nAuthor contributions All the authors contributed to the study concep-\ntion and design. The first draft of the manuscript was written by JK, \nMH and GH, and all the authors commented on previous versions of \nthe manuscript. All the authors read and approved the final manuscript.\nFunding The authors declare that no funds, grants, or other support \nwere received during the preparation of this manuscript.\nDeclarations \nConflict of interest The authors declare that they have no conflict of \ninterest: J. Keckstein, M. Hoopmann, E. Merz D. Grab, J. Weichert \nS. Helmy-Bader M. Wölfler, M. Bajka, S. Mechsner, S. Schäfer, H. \nKrentel, and G. Hudelist.\nOpen Access This article is licensed under a Creative Commons Attri-\nbution 4.0 International License, which permits use, sharing, adapta-\ntion, distribution and reproduction in any medium or format, as long \nas you give appropriate credit to the original author(s) and the source, \nprovide a link to the Creative Commons licence, and indicate if changes \nwere made. The images or other third party material in this article are \nincluded in the article's Creative Commons licence, unless indicated \notherwise in a credit line to the material. If material is not included in \nthe article's Creative Commons licence and your intended use is not \npermitted by statutory regulation or exceeds the permitted use, you will \nneed to obtain permission directly from the copyright holder. To view a \ncopy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/.\nReferences\n 1. Rokitansky K (1860) Ueber uterusdruesen-neubildung. 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Arch Gynecol Obstet 301(3):699–706\nPublisher's Note Springer Nature remains neutral with regard to \njurisdictional claims in published maps and institutional affiliations.\n\n19Archives of Gynecology and Obstetrics (2023) 307:5–19 \n1 3\nAuthors and Affiliations\nJ. Keckstein1,2,14,15,18  · M. Hoopmann3 · E. Merz4 · D. Grab2 · J. Weichert5 · S. Helmy‑Bader6,16 · M. Wölfler7,14,16 · \nM. Bajka8,17 · S. Mechsner9,14,15 · S. Schäfer10,14,15,18 · H. Krentel11,14,15,18 · G. Hudelist12,13,14,16,18\n1 Endometriosis Clinic Dres, Jörg und Sigrid Keckstein, \nRichard Wagner Strasse18, Villach, Austria\n2 Department of Obstetrics and Gynaecology, Medical \nUniversity Ulm, Ulm, Germany\n3 Department of Obstetrics and Gynaecology, Medical \nUniversity Tübingen, Tübingen, Germany\n4 Centre for Ultrasound and Prenatal Medicine, Frankfurt, \nGermany\n5 Department of Obstetrics and Gynaecology, University \nHospital of Schleswig-Holstein, Lübeck, Germany\n6 Department of Obstetrics and Gynaecology, Medical \nUniversity Vienna, Vienna, Austria\n7 Department of Obstetrics and Gynaecology, Centre \nfor Endometriosis, Medical University Graz, Graz, Austria\n8 OB/GYN Volketswil, Volketswil, Switzerland\n9 Department of Gynaecology, Endometriosis Centre Charité, \nCharite Berlin University Hospital, Berlin, Germany\n10 Department of Gynaecology and Obstetrics, University \nHospital Muenster, Münster, Germany\n11 Department of Obstetrics and Gynaecology, Bethesda \nHospital Duisburg, Duisburg, Germany\n12 Department of Gynaecology, Centre for Endometriosis, \nHospital St. John of God, Vienna, Austria\n13 Rudolfinerhaus Private Clinic and Campus, Vienna, Austria\n14 SEF, Scientific Endometriosis Foundation (Stiftung \nEndometrioseforschung), Westerstede, Germany\n15 AGEM, Arbeitsgemeinschaft Endometriose of the DGGG , \nBerlin, Germany\n16 ÖGUM, Österreichische Gesellschaft für Ultraschall in der \nMedizin, Vienna, Austria\n17 SGUM, Schweizer Gesellschaft für Ultraschall in der \nMedizin, Aarau, Switzerland\n18 EEL, European Endometriosis League, Unterhaching, \nGermany","source_license":"CC0","license_restricted":false}